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{{Short description|Genetic segments that can enhance their own transmission at the expense of other genes}} | ||
'''Selfish genetic elements''' (historically also referred to as selfish genes, ultra-selfish genes, selfish DNA, parasitic DNA |
'''Selfish genetic elements''' (historically also referred to as '''selfish genes''', '''ultra-selfish genes''', '''selfish DNA''', '''parasitic DNA''' and '''genomic outlaws''') are genetic segments that can enhance their own transmission at the expense of other genes in the genome, even if this has no positive or a net negative effect on organismal fitness.<ref name=":0">{{cite journal | vauthors = Werren JH, Nur U, Wu CI | title = Selfish genetic elements | journal = Trends in Ecology & Evolution | volume = 3 | issue = 11 | pages = 297–302 | date = November 1988 | pmid = 21227262 | doi = 10.1016/0169-5347(88)90105-x | s2cid = 3014674 }}</ref><ref>{{cite journal | vauthors = Hurst GD, Hurst LD, Johnstone RA | title = Intranuclear conflict and its role in evolution | journal = Trends in Ecology & Evolution | volume = 7 | issue = 11 | pages = 373–8 | date = November 1992 | pmid = 21236071 | doi = 10.1016/0169-5347(92)90007-x }}</ref><ref>{{cite journal | vauthors = Hurst LD, Atlan A, Bengtsson BO | title = Genetic conflicts | journal = The Quarterly Review of Biology | volume = 71 | issue = 3 | pages = 317–64 | date = September 1996 | pmid = 8828237 | doi = 10.1086/419442 | s2cid = 24853836 }}</ref><ref name=":1">{{cite journal | vauthors = Hurst GD, Werren JH | title = The role of selfish genetic elements in eukaryotic evolution | journal = Nature Reviews. Genetics | volume = 2 | issue = 8 | pages = 597–606 | date = August 2001 | pmid = 11483984 | doi = 10.1038/35084545 | s2cid = 2715605 }}</ref><ref name=":21">{{cite journal | vauthors = McLaughlin RN, Malik HS | title = Genetic conflicts: the usual suspects and beyond | journal = The Journal of Experimental Biology | volume = 220 | issue = Pt 1 | pages = 6–17 | date = January 2017 | pmid = 28057823 | pmc = 5278622 | doi = 10.1242/jeb.148148 }}</ref><ref>{{cite journal | vauthors = Gardner A, Úbeda F | title = The meaning of intragenomic conflict | journal = Nature Ecology & Evolution | volume = 1 | issue = 12 | pages = 1807–1815 | date = December 2017 | pmid = 29109471 | doi = 10.1038/s41559-017-0354-9 | bibcode = 2017NatEE...1.1807G | hdl = 10023/13307 | s2cid = 3314539 | url = https://research-repository.st-andrews.ac.uk/bitstream/10023/13307/1/Gardner_2017_Meaning_intragenomic_NatEcolEvol_AAM.pdf | hdl-access = free }}</ref> Genomes have traditionally been viewed as cohesive units, with genes acting together to improve the fitness of the organism. | ||
Early observations of selfish genetic elements were made almost a century ago, but the topic did not get widespread attention until several decades later. Inspired by the |
Early observations of selfish genetic elements were made almost a century ago, but the topic did not get widespread attention until several decades later. Inspired by the ] popularized by ]<ref name=":2">{{cite book |last=Williams |first=George Christopher |title=Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought |date= |publisher=Princeton University Press |year=1966 |isbn=978-1-4008-2010-8 |publication-place=Princeton, New Jersey |doi=10.1515/9781400820108 |orig-date= |name-list-style=vanc}}</ref> and ],<ref name="TSG">{{Cite book |title=The Selfish Gene |last=Dawkins|first=Richard | name-list-style = vanc |author-link=Richard Dawkins |publisher=Oxford University Press|year=1976|isbn=978-0-19-109306-7 |oclc=953456293}}</ref> two papers were published back-to-back in ''Nature'' in 1980 – by ] and ]<ref name=":3">{{cite journal | vauthors = Orgel LE, Crick FH | title = Selfish DNA: the ultimate parasite | journal = Nature | volume = 284 | issue = 5757 | pages = 604–7 | date = April 1980 | pmid = 7366731 | doi = 10.1038/284604a0 | bibcode = 1980Natur.284..604O | s2cid = 4233826 | author2-link = Francis Crick }}</ref> and by ] and ]<ref name=":4">{{cite journal | vauthors = Doolittle WF, Sapienza C | title = Selfish genes, the phenotype paradigm and genome evolution | journal = Nature | volume = 284 | issue = 5757 | pages = 601–3 | date = April 1980 | pmid = 6245369 | doi = 10.1038/284601a0 | bibcode = 1980Natur.284..601D | s2cid = 4311366 }}</ref> – introducing the concept of selfish genetic elements (at the time called "selfish DNA") to the wider scientific community. Both papers emphasized that genes can spread in a population regardless of their effect on organismal fitness as long as they have a transmission advantage. | ||
Selfish genetic elements have now been described in most groups of organisms, and they demonstrate a remarkable diversity in the ways by which they promote their own transmission.<ref>{{Cite book| |
Selfish genetic elements have now been described in most groups of organisms, and they demonstrate a remarkable diversity in the ways by which they promote their own transmission.<ref name=":30">{{Cite book|doi = 10.4159/9780674029118|title=Genes in Conflict |last1=Burt|first1=Austin |last2=Trivers|first2=Robert | name-list-style = vanc |author2-link=Robert Trivers |date=2006-01-31|publisher=Harvard University Press|isbn=978-0-674-02911-8 |location=Cambridge, MA and London, England|s2cid=90469073 }}</ref> Though long dismissed as genetic curiosities, with little relevance for evolution, they are now recognized to affect a wide swath of biological processes, ranging from genome size and architecture to speciation.<ref>{{cite journal | vauthors = Werren JH | title = Selfish genetic elements, genetic conflict, and evolutionary innovation | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 108 Suppl 2 | issue = Supplement 2 | pages = 10863–70 | date = June 2011 | pmid = 21690392 | pmc = 3131821 | doi = 10.1073/pnas.1102343108 | bibcode = 2011PNAS..10810863W | doi-access = free }}</ref> | ||
==History== | ==History== | ||
===Early observations === | ===Early observations === | ||
Observations of what |
Observations of what is now referred to as selfish genetic elements go back to the early days in the ]. Already in 1928, Russian geneticist ] reported the discovery of a driving ] in ''Drosophila obscura''.<ref name=":5">{{cite journal | vauthors = Gershenson S | title = A New Sex-Ratio Abnormality in DROSOPHILA OBSCURA | journal = Genetics | volume = 13 | issue = 6 | pages = 488–507 | date = November 1928 | doi = 10.1093/genetics/13.6.488 | pmid = 17246563 | pmc = 1200995 }}</ref> Crucially, he noted that the resulting female-biased sex ratio may drive a population extinct (see ]). The earliest clear statement of how chromosomes may spread in a population not because of their positive fitness effects on the individual organism, but because of their own "parasitic" nature came from the Swedish botanist and cytogeneticist ] in 1945.<ref name=":6">{{cite journal | vauthors = Östergren G | title = Parasitic nature of extra fragment chromosomes. | journal = Botaniska Notiser | date = 1945 | volume = 2 | pages = 157–163 }}</ref> Discussing ]s in plants he wrote:<ref name=":6" /> | ||
<blockquote>In many cases these chromosomes have no useful function at all to the species carrying them, but that they often lead an exclusively parasitic existence ... need not be useful for the plants. They need only be useful to themselves.</blockquote> | |||
Around the same time, several other examples of selfish genetic elements were reported. For example, the American maize geneticist ] described how chromosomal knobs led to female ] in maize.<ref>{{cite journal | vauthors = Rhoades MM | title = Preferential Segregation in Maize | journal = Genetics | volume = 27 | issue = 4 | pages = 395–407 | date = July 1942 | doi = 10.1093/genetics/27.4.395 | pmid = 17247049 | pmc = 1209167 }}</ref> Similarly, this was also when it was first suggested that an ] between ] mitochondrial genes and biparentally inherited nuclear genes could lead to ] in plants.<ref name=":7">{{cite journal | vauthors = Lewis D | title = Male sterility in natural populations of hermaphrodite plants the equilibrium between females and hermaphrodites to be expected with different types of inheritance. | journal = New Phytologist | date = April 1941 | volume = 40 | issue = 1 | pages = 56–63 | doi = 10.1111/j.1469-8137.1941.tb07028.x | doi-access = free }}</ref> Then, in the early 1950s, ] published a series of papers describing the existence of ]s, which are now recognized to be among the most successful selfish genetic elements.<ref name=":8">{{cite journal | vauthors = McClintock B | title = The origin and behavior of mutable loci in maize | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 36 | issue = 6 | pages = 344–55 | date = June 1950 | pmid = 15430309 | pmc = 1063197 | doi = 10.1073/pnas.36.6.344 | bibcode = 1950PNAS...36..344M | doi-access = free }}</ref> The discovery of transposable elements led to her being awarded the ]. | |||
=== Conceptual developments === | === Conceptual developments === | ||
The empirical study of selfish genetic elements benefited greatly from the emergence of the so-called gene-centred view of evolution in the nineteen sixties and seventies.<ref>{{ |
The empirical study of selfish genetic elements benefited greatly from the emergence of the so-called gene-centred view of evolution in the nineteen sixties and seventies.<ref name=":25">{{cite journal | vauthors = Ågren JA | title = Selfish genetic elements and the gene's-eye view of evolution | journal = Current Zoology | volume = 62 | issue = 6 | pages = 659–665 | date = December 2016 | pmid = 29491953 | pmc = 5804262 | doi = 10.1093/cz/zow102 }}</ref> In contrast with Darwin's original formulation of the theory of evolution by natural selection that focused on individual organisms, the gene's-eye view takes the gene to be the central unit of selection in evolution.<ref>{{citation |title=Selfish Genes |last1= Ågren |first1=Jon Arvid |last2=Hurst |first2=Greg | name-list-style = vanc |date=2017-10-25 |website=Oxford Bibliographies Online Datasets |doi=10.1093/obo/9780199941728-0094 }}</ref> It conceives evolution by natural selection as a process involving two separate entities: replicators (entities that produce faithful copies of themselves, usually genes) and vehicles (or interactors; entities that interact with the ecological environment, usually organisms).<ref>{{Cite book|title=The extended phenotype : the long reach of the gene|last=Dawkins |first=Richard | name-list-style = vanc |author-link=Richard Dawkins|publisher=Oxford University Press|year=1982|oclc=610269469}}</ref><ref>{{cite book | vauthors = Dawkins R | chapter = Replicators and vehicles | editor = King's College Sociobiology Group, Cambridge | title = Current Problems in Sociobiology. | publisher = Cambridge University Press | date = June 1982 | pages = 45–64 | isbn = 978-0-521-28520-9 }}</ref><ref>{{cite book | vauthors = Hull DL | chapter = Units of Evolution: A Metaphysical Essay | veditors = Jensen UJ, Harré R | title = The Philosophy of Evolution | publisher = St. Martin's Press | date = 1981 | pages = 23–44 }}</ref> | ||
] | |||
Since organisms are temporary occurrences, present in one generation and gone in the next, genes (replicators) are the only entity faithfully transmitted from parent to offspring. Viewing evolution as a struggle between competing replicators made it easier to recognize that not all genes in an organism would share the same evolutionary fate. | Since organisms are temporary occurrences, present in one generation and gone in the next, genes (replicators) are the only entity faithfully transmitted from parent to offspring. Viewing evolution as a struggle between competing replicators made it easier to recognize that not all genes in an organism would share the same evolutionary fate.<ref name=":25" /> | ||
The |
The gene's-eye view was a synthesis of the population genetic models of the modern synthesis, in particular the work of ], and the social evolution models of ]. The view was popularized by ]'s '']''<ref name=":2" /> and ]'s best seller '']''.<ref name="TSG"/> Dawkins summarized a key benefit from the gene's-eye view as follows: | ||
<blockquote> |
<blockquote>"If we allow ourselves the license of talking about genes as if they had conscious aims, always reassuring ourselves that we could translate our sloppy language back into respectable terms if we wanted to, we can ask the question, what is a single selfish gene trying to do?" — Richard Dawkins, ''The Selfish Gene''<ref name="TSG"/>{{rp|p. 88}}</blockquote> | ||
In 1980, two high |
In 1980, two high-profile papers published back-to-back in ''Nature'' by Leslie Orgel and Francis Crick, and by Ford Doolittle and Carmen Sapienza, brought the study of selfish genetic elements to the centre of biological debate.<ref name=":3" /><ref name=":4" /> The papers took their starting point in the contemporary debate of the so-called ], the lack of correlation between genome size and perceived complexity of a species. Both papers attempted to counter the prevailing view of the time that the presence of differential amounts of non-coding DNA and transposable elements is best explained from the perspective of individual fitness, described as the "phenotypic paradigm" by Doolittle and Sapienza. Instead, the authors argued that much of the genetic material in eukaryotic genomes persists, not because of its phenotypic effects, but can be understood from a gene's-eye view, without invoking individual-level explanations. The two papers led to a series of exchanges in ''Nature''.<ref>{{cite journal | vauthors = Cavalier-Smith T | title = How selfish is DNA? | journal = Nature | volume = 285 | issue = 5767 | pages = 617–8 | date = June 1980 | pmid = 7393317 | doi = 10.1038/285617a0 | bibcode = 1980Natur.285..617C | s2cid = 27111068 | doi-access = free }}</ref><ref>{{cite journal | vauthors = Dover G | title = Ignorant DNA? | journal = Nature | volume = 285 | issue = 5767 | pages = 618–20 | date = June 1980 | pmid = 7393318 | doi = 10.1038/285618a0 | bibcode = 1980Natur.285..618D | s2cid = 4261755 | doi-access = free }}</ref><ref>{{cite journal | vauthors = Dover G, Doolittle WF | title = Modes of genome evolution | journal = Nature | volume = 288 | issue = 5792 | pages = 646–7 | date = December 1980 | pmid = 6256636 | doi = 10.1038/288646a0 | bibcode = 1980Natur.288..646D | s2cid = 8938434 | doi-access = free }}</ref><ref>{{cite journal | vauthors = Orgel LE, Crick FH, Sapienza C | title = Selfish DNA | journal = Nature | volume = 288 | issue = 5792 | pages = 645–6 | date = December 1980 | pmid = 7453798 | doi = 10.1038/288645a0 | bibcode = 1980Natur.288..645O | s2cid = 4370178 }}</ref> | ||
=== Current views === | === Current views === | ||
If the |
If the selfish DNA papers marked the beginning of the serious study of selfish genetic elements, the subsequent decades have seen an explosion in theoretical advances and empirical discoveries. ] and ] wrote a landmark review about the conflict between maternally inherited cytoplasmic genes and biparentally inherited nuclear genes.<ref name=":20">{{cite journal | vauthors = Cosmides LM, Tooby J | title = Cytoplasmic inheritance and intragenomic conflict | journal = Journal of Theoretical Biology | volume = 89 | issue = 1 | pages = 83–129 | date = March 1981 | pmid = 7278311 | doi = 10.1016/0022-5193(81)90181-8 | bibcode = 1981JThBi..89...83M | s2cid = 36815174 }}</ref> The paper also provided a comprehensive introduction to the logic of genomic conflicts, foreshadowing many themes that would later be subject of much research. Then in 1988 ] and colleagues wrote the first major empirical review of the topic.<ref name=":0" /> This paper achieved three things. First, it coined the term selfish genetic element, putting an end to a sometimes confusingly diverse terminology (selfish genes, ultra-selfish genes, selfish DNA, parasitic DNA, genomic outlaws). Second, it formally defined the concept of selfish genetic elements. Finally, it was the first paper to bring together all different kinds of selfish genetic elements known at the time (], for example, was not covered).<ref name=":0" /> | ||
In the late 1980s, most molecular biologists considered selfish genetic elements to be the exception, and that genomes were best thought of as highly integrated networks with a coherent effect on organismal fitness.<ref name=":0" /><ref name=":30" /> In 2006, when ] and ] published the first book-length treatment of the topic, the tide was changing.<ref name=":30" /> While their role in evolution long remained controversial, in a review published a century after their first discovery, ] concluded that "nothing in genetics makes sense except in the light of genomic conflicts".<ref>{{Cite journal|last=Rice|first=William R. | name-list-style = vanc |date=2013-11-23|title=Nothing in Genetics Makes Sense Except in Light of Genomic Conflict |journal=Annual Review of Ecology, Evolution, and Systematics|volume=44|issue=1|pages=217–237|doi=10.1146/annurev-ecolsys-110411-160242|issn=1543-592X}}</ref> | |||
== Logic == | == Logic == | ||
Though selfish genetic elements show a remarkable diversity in the way they promote their own transmission, some generalizations about their biology can be made. In a classic 2001 review, Gregory D.D. Hurst and John H. Werren proposed two |
Though selfish genetic elements show a remarkable diversity in the way they promote their own transmission, some generalizations about their biology can be made. In a classic 2001 review, Gregory D.D. Hurst and John H. Werren proposed two ‘rules' of selfish genetic elements.<ref name=":1" /> | ||
=== Rule 1: |
=== Rule 1: Spread requires sex and outbreeding === | ||
Sexual reproduction involves the mixing of genes from two individuals. According to ], alleles in a sexually reproducing organism have a 50% chance of being passed from parent to offspring. Meiosis is therefore sometimes referred to as |
Sexual reproduction involves the mixing of genes from two individuals. According to ], alleles in a sexually reproducing organism have a 50% chance of being passed from parent to offspring. Meiosis is therefore sometimes referred to as "fair".<ref>{{Cite journal|last=Levinton|first=Jeffrey | name-list-style = vanc |date= June 1972 |title=Adaptation and Diversity. Natural History and the Mathematics of Evolution. Egbert Giles Leigh |journal=The Quarterly Review of Biology|volume=47|issue=2|pages=225–226|doi=10.1086/407257 | department = Book Review |title-link=Egbert Giles Leigh }}</ref> | ||
Highly self-fertilizing or asexual genomes are expected to experience less conflict between selfish genetic elements and the rest of the host genome than outcrossing sexual genomes.<ref>{{Cite journal|last= |
Highly self-fertilizing or asexual genomes are expected to experience less conflict between selfish genetic elements and the rest of the host genome than outcrossing sexual genomes.<ref>{{Cite journal |last=Hickey |first=Donal A. | name-list-style = vanc |date=October 1984 |title=DNA can be a selfish parasite |journal=Nature|volume=311|issue=5985|pages=417–418|doi=10.1038/311417d0|bibcode=1984Natur.311..417H |s2cid=4362210 }}</ref><ref>{{cite journal | vauthors = Wright S, Finnegan D | title = Genome evolution: sex and the transposable element | journal = Current Biology | volume = 11 | issue = 8 | pages = R296–9 | date = April 2001 | pmid = 11369217 | doi = 10.1016/s0960-9822(01)00168-3 | s2cid = 2088287 | doi-access = free | bibcode = 2001CBio...11.R296W }}</ref><ref>{{cite book |last1=Wright |first1=Stephen I. |last2=Schoen |first2=Daniel J. | name-list-style = vanc |title=Transposon dynamics and the breeding system|date=2000| work=Transposable Elements and Genome Evolution|volume=107 |issue=1–3 |pages=139–148|publisher=Springer Netherlands|pmid=10952207 |isbn=9789401058124 }}</ref> There are several reasons for this. First, sex and outcrossing put selfish genetic elements into new genetic lineages. In contrast, in a highly selfing or asexual lineage, any selfish genetic element is essentially stuck in that lineage, which should increase variation in fitness among individuals. The increased variation should result in stronger purifying selection in selfers/asexuals, as a lineage without the selfish genetic elements should out-compete a lineage with the selfish genetic element. Second, the increased homozygosity in selfers removes the opportunity for competition among homologous alleles. Third, theoretical work has shown that the greater linkage disequilibrium in selfing compared to outcrossing genomes may in some, albeit rather limited, cases cause selection for reduced transposition rates.<ref name=":13">{{cite journal | vauthors = Charlesworth B, Langley CH | title = The evolution of self-regulated transposition of transposable elements | journal = Genetics | volume = 112 | issue = 2 | pages = 359–83 | date = February 1986 | doi = 10.1093/genetics/112.2.359 | pmid = 3000868 | pmc = 1202706 }}</ref> Overall, this reasoning leads to the prediction that asexuals/selfers should experience a lower load of selfish genetic elements. One caveat to this is that the evolution of selfing is associated with a reduction in the ].<ref>{{cite journal | vauthors = Nordborg M | title = Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization | journal = Genetics | volume = 154 | issue = 2 | pages = 923–9 | date = February 2000 | doi = 10.1093/genetics/154.2.923 | pmid = 10655241 | pmc = 1460950 }}</ref> A reduction in the effective population size should reduce the efficacy of selection and therefore leads to the opposite prediction: higher accumulation of selfish genetic elements in selfers relative to outcrossers. | ||
Empirical evidence for the importance of sex and outcrossing comes from a variety of selfish genetic elements, including transposable elements,<ref>{{ |
Empirical evidence for the importance of sex and outcrossing comes from a variety of selfish genetic elements, including transposable elements,<ref>{{cite journal | vauthors = Arkhipova I, Meselson M | title = Transposable elements in sexual and ancient asexual taxa | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 97 | issue = 26 | pages = 14473–7 | date = December 2000 | pmid = 11121049 | pmc = 18943 | doi = 10.1073/pnas.97.26.14473 | bibcode = 2000PNAS...9714473A | doi-access = free }}</ref><ref>{{cite journal | vauthors = Agren JÅ, Wang W, Koenig D, Neuffer B, Weigel D, Wright SI | title = Mating system shifts and transposable element evolution in the plant genus Capsella | journal = BMC Genomics | volume = 15 | issue = 1 | pages = 602 | date = July 2014 | pmid = 25030755 | pmc = 4112209 | doi = 10.1186/1471-2164-15-602 | doi-access = free }}</ref> self-promoting plasmids,<ref>{{cite journal | vauthors = Harrison E, MacLean RC, Koufopanou V, Burt A | title = Sex drives intracellular conflict in yeast | journal = Journal of Evolutionary Biology | volume = 27 | issue = 8 | pages = 1757–63 | date = August 2014 | pmid = 24825743 | doi = 10.1111/jeb.12408 | s2cid = 23049054 | doi-access = free }}</ref> and B chromosomes.<ref>{{Cite journal| vauthors = Burt A, Trivers R | date=1998-01-22|title=Selfish DNA and breeding system in flowering plants |journal=Proceedings of the Royal Society B: Biological Sciences|volume=265|issue=1391|pages=141–146|doi=10.1098/rspb.1998.0275| pmc=1688861}}</ref> | ||
=== Rule 2: |
=== Rule 2: Presence is often revealed in hybrids === | ||
The presence of selfish genetic elements can be difficult to detect in natural populations. Instead, their phenotypic consequences often become apparent in hybrids. The first |
The presence of selfish genetic elements can be difficult to detect in natural populations. Instead, their phenotypic consequences often become apparent in hybrids. The first reason for this is that some selfish genetic elements rapidly sweep to fixation, and the phenotypic effects will therefore not be segregating in the population. Hybridization events, however, will produce offspring with and without the selfish genetic elements and so reveal their presence. The second reason is that host genomes have evolved mechanisms to suppress the activity of the selfish genetic elements, for example the small RNA administered silencing of transposable elements.<ref>{{cite journal | vauthors = Aravin AA, Hannon GJ, Brennecke J | title = The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race | journal = Science | volume = 318 | issue = 5851 | pages = 761–4 | date = November 2007 | pmid = 17975059 | doi = 10.1126/science.1146484 | bibcode = 2007Sci...318..761A | s2cid = 8532459 | doi-access = | url = https://resolver.caltech.edu/CaltechAUTHORS:20190509-083948927 }}</ref> The co-evolution between selfish genetic elements and their suppressors can be rapid, and follow a ], which may mask the presence of selfish genetic elements in a population. Hybrid offspring, on the other hand, may inherit a given selfish genetic element, but not the corresponding suppressor and so reveal the phenotypic effect of the selfish genetic element.<ref name=":9">{{cite journal | vauthors = Crespi B, Nosil P | title = Conflictual speciation: species formation via genomic conflict | journal = Trends in Ecology & Evolution | volume = 28 | issue = 1 | pages = 48–57 | date = January 2013 | pmid = 22995895 | doi = 10.1016/j.tree.2012.08.015 }}</ref><ref name=":10">{{cite journal | vauthors = Ågren JA | title = Selfish genes and plant speciation. | journal = Evolutionary Biology | date = September 2013 | volume = 40 | issue = 3 | pages = 439–449 | doi = 10.1007/s11692-012-9216-1 | bibcode = 2013EvBio..40..439A | s2cid = 19018593 }}</ref> | ||
== Examples == | == Examples == | ||
=== Segregation distorters === | === Segregation distorters === | ||
] | ] | ||
Some selfish genetic elements manipulate the ] to their own advantage, and so end up being overrepresented in the gametes. Such distortion can occur in various ways, and the umbrella term that encompasses all of them is segregation distortion. Some elements can preferentially be transmitted in egg cells as opposed to polar bodies during meiosis, where only the former will be fertilized and transmitted to the next generation. Any gene that can manipulate the odds of ending up in the egg rather than the polar body will have a transmission advantage, and will increase in frequency in a population. | Some selfish genetic elements manipulate the ] to their own advantage, and so end up being overrepresented in the gametes. Such distortion can occur in various ways, and the umbrella term that encompasses all of them is segregation distortion. Some elements can preferentially be transmitted in egg cells as opposed to ] during meiosis, where only the former will be fertilized and transmitted to the next generation. Any gene that can manipulate the odds of ending up in the egg rather than the polar body will have a transmission advantage, and will increase in frequency in a population.<ref name=":21" /> | ||
Segregation distortion can happen in several ways. When this process occurs during meiosis it is referred to as ]. Many forms of segregation distortion occur in male gamete formation, where there is differential mortality of spermatids during the process of sperm maturation or ]. The |
Segregation distortion can happen in several ways. When this process occurs during meiosis it is referred to as ]. Many forms of segregation distortion occur in male gamete formation, where there is differential mortality of spermatids during the process of sperm maturation or ]. The segregation distorter (SD) in ''Drosophila melanogaster'' is the best studied example, and it involves a nuclear envelope protein Ran-GAP and the X-linked repeat array called Responder (Rsp), where the SD allele of Ran-GAP favors its own transmission only in the presence of a Rsp<sup>sensitive</sup> allele on the homologous chromosome.<ref>{{cite journal | vauthors = Brittnacher JG, Ganetzky B | title = On the components of segregation distortion in Drosophila melanogaster. III. Nature of enhancer of SD | journal = Genetics | volume = 107 | issue = 3 | pages = 423–34 | date = July 1984 | doi = 10.1093/genetics/107.3.423 | pmid = 6428976 | pmc = 1202333 }}</ref><ref name=":26">{{cite journal | vauthors = Brittnacher JG, Ganetzky B | title = On the Components of Segregation Distortion in Drosophila melanogaster. II. Deletion Mapping and Dosage Analysis of the SD Locus | journal = Genetics | volume = 103 | issue = 4 | pages = 659–73 | date = April 1983 | doi = 10.1093/genetics/103.4.659 | pmid = 17246120 | pmc = 1202047 }}</ref><ref>{{cite journal | vauthors = Brittnacher JG, Ganetzky B | title = On the components of segregation distortion in Drosophila melanogaster. IV. Construction and analysis of free duplications for the Responder locus | journal = Genetics | volume = 121 | issue = 4 | pages = 739–50 | date = April 1989 | doi = 10.1093/genetics/121.4.739 | pmid = 2498160 | pmc = 1203657 }}</ref><ref>{{cite journal | vauthors = Powers PA, Ganetzky B | title = On the components of segregation distortion in Drosophila melanogaster. V. Molecular analysis of the Sd locus | journal = Genetics | volume = 129 | issue = 1 | pages = 133–44 | date = September 1991 | doi = 10.1093/genetics/129.1.133 | pmid = 1936954 | pmc = 1204561 }}</ref><ref>{{cite journal | vauthors = Larracuente AM, Presgraves DC | title = The selfish Segregation Distorter gene complex of Drosophila melanogaster | journal = Genetics | volume = 192 | issue = 1 | pages = 33–53 | date = September 2012 | pmid = 22964836 | pmc = 3430544 | doi = 10.1534/genetics.112.141390 }}</ref> SD acts to kill RSP<sup>sensitive</sup> sperm, in a post-meiotic process (hence it is not strictly speaking meiotic drive). Systems like this can have interesting rock-paper-scissors dynamics, oscillating between the SD-RSP<sup>insensitive</sup>, SD+-RSP<sup>insensitive</sup> and SD+-RSP<sup>sensitive</sup> haplotypes. The SD-RSP<sup>sensitive</sup> haplotype is not seen because it essentially commits suicide.<ref name=":26" /> | ||
When segregation distortion acts on sex chromosomes, they can skew the sex ratio. The SR system in ''Drosophila pseudoobscura'', for example, is on the X chromosome, and XSR/Y males produce only daughters, whereas females undergo normal meiosis with Mendelian proportions of gametes.<ref name=":11">Curtsinger JW, Feldman MW |
When segregation distortion acts on sex chromosomes, they can skew the sex ratio. The SR system in ''Drosophila pseudoobscura'', for example, is on the X chromosome, and XSR/Y males produce only daughters, whereas females undergo normal meiosis with Mendelian proportions of gametes.<ref name=":11">{{cite journal | vauthors = Curtsinger JW, Feldman MW | title = Experimental and Theoretical Analysis of the "Sex-Ratio" Polymorphism in Drosophila pseudoobscura | journal = Genetics | volume = 94 | issue = 2 | pages = 445–66 | date = February 1980 | doi = 10.1093/genetics/94.2.445 | pmid = 17249004 | pmc = 1214151 }}</ref><ref>{{cite journal | vauthors = Curtsinger JW | title = Artificial selection on the sex ratio in Drosophila pseudoobscura | journal = Journal of Heredity | date = 1981 | volume = 72 | issue = 6 | pages = 377–381 | doi = 10.1093/oxfordjournals.jhered.a109535 }}</ref> Segregation distortion systems would drive the favored allele to fixation, except that most of the cases where these systems have been identified have the driven allele opposed by some other selective force. One example is the lethality of the t-haplotype in mice,<ref name=":14">{{cite journal | vauthors = Lyon MF | title = Transmission ratio distortion in mice | journal = Annual Review of Genetics | volume = 37 | pages = 393–408 | date = 2003 | pmid = 14616067 | doi = 10.1146/annurev.genet.37.110801.143030 }}</ref> another is the effect on male fertility of the Sex Ratio system in ''D. pseudoobscura''.<ref name=":11" /> | ||
=== Homing endonucleases === | === Homing endonucleases === | ||
] | ] | ||
A phenomenon closely related to segregation distortion is ].<ref name=":15">Burt A |
A phenomenon closely related to segregation distortion is ]s.<ref name=":15">{{cite journal | vauthors = Burt A | title = Site-specific selfish genes as tools for the control and genetic engineering of natural populations | journal = Proceedings. Biological Sciences | volume = 270 | issue = 1518 | pages = 921–8 | date = May 2003 | pmid = 12803906 | pmc = 1691325 | doi = 10.1098/rspb.2002.2319 }}</ref><ref>{{cite journal | vauthors = Burt A, Koufopanou V | title = Homing endonuclease genes: the rise and fall and rise again of a selfish element | journal = Current Opinion in Genetics & Development | volume = 14 | issue = 6 | pages = 609–15 | date = December 2004 | pmid = 15531154 | doi = 10.1016/j.gde.2004.09.010 }}</ref><ref>{{cite journal | vauthors = Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H, Ulge UY, Hovde BT, Baker D, Monnat RJ, Burt A, Crisanti A | title = A synthetic homing endonuclease-based gene drive system in the human malaria mosquito | journal = Nature | volume = 473 | issue = 7346 | pages = 212–5 | date = May 2011 | pmid = 21508956 | pmc = 3093433 | doi = 10.1038/nature09937 | bibcode = 2011Natur.473..212W }}</ref> These are enzymes that cut DNA in a sequence-specific way, and those cuts, generally double-strand breaks, are then "healed" by the regular DNA repair machinery. Homing endonucleases insert themselves into the genome at the site homologous to the first insertion site, resulting in a conversion of a heterozygote into a homozygote bearing a copy of the homing endonuclease on both homologous chromosomes. This gives homing endonucleases an allele frequency dynamics rather similar to a segregation distortion system, and generally unless opposed by strong countervailing selection, they are expected to go to fixation in a population. ] technology allows the artificial construction of homing endonuclease systems. These so-called "gene drive" systems pose a combination of great promise for biocontrol but also potential risk.<ref name=":16">Gantz VM, Bier E. Genome editing. The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science. 2015;348: 442–444.</ref><ref name=":17">{{cite journal | vauthors = Esvelt KM, Smidler AL, Catteruccia F, Church GM | title = Concerning RNA-guided gene drives for the alteration of wild populations | journal = eLife | volume = 3 | date = July 2014 | pmid = 25035423 | pmc = 4117217 | doi = 10.7554/eLife.03401 | doi-access = free }}</ref> | ||
=== Transposable elements === | === Transposable elements === | ||
] | ] | ||
Transposable elements (TEs) include a wide variety of DNA sequences that all have the ability to move to new locations in the genome of their host. Transposons do this by a direct cut-and-paste mechanism, whereas retrotransposons need to produce an RNA intermediate to move. TEs were first discovered in maize by ] in the 1940s<ref name=":8" /> and their ability to occur in both active and quiescent states in the genome was also first elucidated by McClintock.<ref>Ravindran S |
Transposable elements (TEs) include a wide variety of DNA sequences that all have the ability to move to new locations in the genome of their host. Transposons do this by a direct cut-and-paste mechanism, whereas retrotransposons need to produce an RNA intermediate to move. TEs were first discovered in maize by ] in the 1940s<ref name=":8" /> and their ability to occur in both active and quiescent states in the genome was also first elucidated by McClintock.<ref>{{cite journal | vauthors = Ravindran S | title = Barbara McClintock and the discovery of jumping genes | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 109 | issue = 50 | pages = 20198–9 | date = December 2012 | pmid = 23236127 | pmc = 3528533 | doi = 10.1073/pnas.1219372109 | doi-access = free }}</ref> TEs have been referred to as selfish genetic elements because they have some control over their own propagation in the genome. Most random insertions into the genome appear to be relatively innocuous, but they can disrupt critical gene functions with devastating results.<ref>Lisch D. How important are transposons for plant evolution? Nat Rev Genet. 2013;14: 49–61.</ref> For example, TEs have been linked to a variety of human diseases, ranging from cancer to haemophilia.<ref name=":29">{{cite journal | vauthors = Hancks DC, Kazazian HH | title = Roles for retrotransposon insertions in human disease | journal = Mobile DNA | volume = 7 | pages = 9 | date = 2016 | pmid = 27158268 | pmc = 4859970 | doi = 10.1186/s13100-016-0065-9 | doi-access = free }}</ref> TEs that tend to avoid disrupting vital functions in the genome tend to remain in the genome longer, and hence they are more likely to be found in innocuous locations.<ref name=":29" /> | ||
Both plant and animal hosts have evolved means for reducing the fitness impact of TEs, both by directly silencing them and by reducing their ability to transpose in the genome. It would appear that hosts in general are fairly tolerant of TEs in their genomes, since a sizable portion (30-80%) of the genome of many animals and plants is TEs.<ref name=":18">Ågren JA, Wright SI |
Both plant and animal hosts have evolved means for reducing the fitness impact of TEs, both by directly silencing them and by reducing their ability to transpose in the genome. It would appear that hosts in general are fairly tolerant of TEs in their genomes, since a sizable portion (30-80%) of the genome of many animals and plants is TEs.<ref name=":18">{{cite journal | vauthors = Ågren JA, Wright SI | title = Co-evolution between transposable elements and their hosts: a major factor in genome size evolution? | journal = Chromosome Research | volume = 19 | issue = 6 | pages = 777–86 | date = August 2011 | pmid = 21850458 | doi = 10.1007/s10577-011-9229-0 | s2cid = 25148109 }}</ref><ref name=":19">T{{cite journal | vauthors = Tenaillon MI, Hollister JD, Gaut BS | title = A triptych of the evolution of plant transposable elements | journal = Trends in Plant Science | volume = 15 | issue = 8 | pages = 471–8 | date = August 2010 | pmid = 20541961 | doi = 10.1016/j.tplants.2010.05.003 }}</ref> When the host is able to stop their movement, TEs can simply be frozen in place, and it then can take millions of years for them to mutate away. The fitness of a TE is a combination of its ability to expand in numbers within a genome, to evade host defenses, but also to avoid eroding host fitness too drastically. The effect of TEs in the genome is not entirely selfish. Because their insertion into the genome can disrupt gene function, sometimes those disruptions can have positive fitness value for the host. Many adaptive changes in ''Drosophila''<ref>{{cite journal | vauthors = Aminetzach YT, Macpherson JM, Petrov DA | title = Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila | journal = Science | volume = 309 | issue = 5735 | pages = 764–7 | date = July 2005 | pmid = 16051794 | doi = 10.1126/science.1112699 | bibcode = 2005Sci...309..764A | s2cid = 11640993 }}</ref> and dogs<ref>{{cite journal | vauthors = Cordaux R, Batzer MA | title = Teaching an old dog new tricks: SINEs of canine genomic diversity | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 103 | issue = 5 | pages = 1157–8 | date = January 2006 | pmid = 16432182 | pmc = 1360598 | doi = 10.1073/pnas.0510714103 | bibcode = 2006PNAS..103.1157C | doi-access = free }}</ref> for example, are associated with TE insertions. | ||
=== B chromosomes === | === B chromosomes === | ||
] refer to chromosomes that are not required for the viability or fertility of the organism, but exist in addition to the normal (A) set.<ref>Douglas RN, Birchler JA |
]s refer to chromosomes that are not required for the viability or fertility of the organism, but exist in addition to the normal (A) set.<ref>{{cite book | vauthors = Douglas RN, Birchler JA | veditors = Bhat T, Wani A | chapter = B Chromosomes | title = Chromosome Structure and Aberrations | publisher = Springer | location = New Delhi | date = 2017 | pages = 13–39 | doi = 10.1007/978-81-322-3673-3_2 | isbn = 978-81-322-3673-3 }}</ref> They persist in the population and accumulate because they have the ability to propagate their own transmission independently of the A chromosomes. They often vary in copy number between individuals of the same species. | ||
B chromosomes were first detected over a century ago.<ref>Wilson E |
B chromosomes were first detected over a century ago.{{When|date=December 2021}}<ref>{{cite journal | vauthors = Wilson E | title = The supernumerary chromosomes of Hemiptera. | journal = Science | date = 1907 | volume = 26 | pages = 870–871 }}</ref> Though typically smaller than normal chromosomes, their gene poor, heterochromatin-rich structure made them visible to early cytogenetic techniques. B chromosomes have been thoroughly studied and are estimated to occur in 15% of all eukaryotic species.<ref>{{cite journal | vauthors = Beukeboom LW | title = Bewildering Bs: an impression of the first B-Chromosome Conference. | journal = Heredity | year = 1994 | volume = 73 | issue = 3 | pages = 328–336 | doi = 10.1038/hdy.1994.140 | doi-access = free }}</ref> In general, they appear to be particularly common among eudicot plants, rare in mammals, and absent in birds. In 1945, they were the subject of Gunnar Östergren's classic paper "Parasitic nature of extra fragment chromosomes", where he argues that the variation in abundance of B chromosomes between and within species is because of the parasitic properties of the Bs.<ref name=":6" /> This was the first time genetic material was referred to as "parasitic" or "selfish". B chromosome number correlates positively with genome size<ref name=":12">{{cite journal | vauthors = Trivers R, Burt A, Palestis BG | title = B chromosomes and genome size in flowering plants | journal = Genome | volume = 47 | issue = 1 | pages = 1–8 | date = February 2004 | pmid = 15060596 | doi = 10.1139/g03-088 }}</ref> and has also been linked to a decrease in egg production in the grasshopper ''Eyprepocnemis plorans''.<ref>{{cite journal | vauthors = Zurita S, Cabrero J, López-León MD, Camacho JP | title = Polymorphism regeneration for a neutralized selfish B chromosome | journal = Evolution; International Journal of Organic Evolution | volume = 52 | issue = 1 | pages = 274–277 | date = February 1998 | pmid = 28568137 | doi = 10.1111/j.1558-5646.1998.tb05163.x | s2cid = 2588754 }}.</ref> | ||
]). While mitochondrial and chloroplast genes are generally maternally inherited, B chromosomes can be preferentially transmitted through both males and females. |
]). While mitochondrial and chloroplast genes are generally maternally inherited, B chromosomes can be preferentially transmitted through both males and females.]] | ||
=== Selfish mitochondria === | === Selfish mitochondria === | ||
Genomic conflicts often arise because not all genes are inherited in the same way. Probably the best example of this is the conflict between ] (usually but not always, maternally) inherited mitochondrial and biparentally inherited nuclear genes. Indeed, one of the earliest clear |
Genomic conflicts often arise because not all genes are inherited in the same way. Probably the best example of this is the conflict between ] (usually but not always, maternally) inherited mitochondrial and biparentally inherited nuclear genes. Indeed, one of the earliest clear statements about the possibility of genomic conflict was made by the English botanist Dan Lewis in reference to the conflict between maternally inherited mitochondrial and biparentally inherited nuclear genes over sex allocation in ] plants.<ref name=":7" /> | ||
A single cell typically contains multiple mitochondria, creating a situation for competition over transmission. Uniparental inheritance been suggested to be a way to reduce the opportunity for selfish mitochondria to spread, as it ensures all mitochondria share the same genome, thus removing the opportunity for competition.<ref name=":20" /><ref>Hadjivasiliou Z, Lane N, Seymour RM, Pomiankowski A |
A single cell typically contains multiple mitochondria, creating a situation for competition over transmission. Uniparental inheritance has been suggested to be a way to reduce the opportunity for selfish mitochondria to spread, as it ensures all mitochondria share the same genome, thus removing the opportunity for competition.<ref name=":20" /><ref>{{cite journal | vauthors = Hadjivasiliou Z, Lane N, Seymour RM, Pomiankowski A | title = Dynamics of mitochondrial inheritance in the evolution of binary mating types and two sexes | journal = Proceedings. Biological Sciences | volume = 280 | issue = 1769 | pages = 20131920 | date = October 2013 | pmid = 23986113 | pmc = 3768323 | doi = 10.1098/rspb.2013.1920 }}</ref><ref>{{cite journal | vauthors = Law R, Hutson V | title = Intracellular symbionts and the evolution of uniparental cytoplasmic inheritance | journal = Proceedings. Biological Sciences | volume = 248 | issue = 1321 | pages = 69–77 | date = April 1992 | pmid = 1355912 | doi = 10.1098/rspb.1992.0044 | bibcode = 1992RSPSB.248...69L | s2cid = 45755461 }}</ref> This view remains widely held, but has been challenged.<ref>{{cite journal | vauthors = Christie JR, Schaerf TM, Beekman M | title = Selection against heteroplasmy explains the evolution of uniparental inheritance of mitochondria | journal = PLOS Genetics | volume = 11 | issue = 4 | pages = e1005112 | date = April 2015 | pmid = 25880558 | pmc = 4400020 | doi = 10.1371/journal.pgen.1005112 | doi-access = free }}</ref> Why inheritance ended up being maternal, rather than paternal, is also much debated, but one key hypothesis is that the mutation rate is lower in female compared to male gametes.<ref>{{cite journal | vauthors = Greiner S, Sobanski J, Bock R | title = Why are most organelle genomes transmitted maternally? | journal = BioEssays | volume = 37 | issue = 1 | pages = 80–94 | date = January 2015 | pmid = 25302405 | pmc = 4305268 | doi = 10.1002/bies.201400110 }}</ref> | ||
The conflict between mitochondrial and nuclear genes is especially easy to study in flowering plants.<ref> |
The conflict between mitochondrial and nuclear genes is especially easy to study in flowering plants.<ref>{{cite journal | vauthors = Liu XQ, Xu X, Tan YP, Li SQ, Hu J, Huang JY, Yang DC, Li YS, Zhu YG | title = Inheritance and molecular mapping of two fertility-restoring loci for Honglian gametophytic cytoplasmic male sterility in rice (Oryza sativaL.) | journal = Molecular Genetics and Genomics | volume = 271 | issue = 5 | pages = 586–94 | date = June 2004 | pmid = 15057557 | doi = 10.1007/s00438-004-1005-9 | s2cid = 1898106 }}</ref><ref>{{cite journal | vauthors = Schnable PS, Wise RP | title = The molecular basis of cytoplasmic male sterility and fertility restoration. | journal = Trends Plant Sci. | date = 1998 | volume = 3 | issue = 5 | pages = 175–180 | doi = 10.1016/S1360-1385(98)01235-7 }}</ref> Flowering plants are typically hermaphrodites,<ref>Barrett SCH. The evolution of plant sexual diversity. Nat Rev Genet. 2002;3: 274–284.</ref> and the conflict thus occurs within a single individual. Mitochondrial genes are typically only transmitted through female gametes, and therefore from their point of view the production of pollen leads to an evolutionary dead end. Any mitochondrial mutation that can affect the amount of resources the plant invests in the female reproductive functions at the expense of the male reproductive functions improves its own chance of transmission. ] is the loss of male fertility, typically through loss of functional pollen production, resulting from a mitochondrial mutation.<ref>{{cite journal | vauthors = Hanson MR, Bentolila S | title = Interactions of mitochondrial and nuclear genes that affect male gametophyte development | journal = The Plant Cell | volume = 16 | issue = Suppl | pages = S154–69 | date = 2004 | pmid = 15131248 | pmc = 2643387 | doi = 10.1105/tpc.015966 }}</ref> In many species where cytoplasmic male sterility occurs, the nuclear genome has evolved so-called restorer genes, which repress the effects of the cytoplasmic male sterility genes and restore the male function, making the plant a hermaphrodite again.<ref>{{cite journal | vauthors = Budar F, Pelletier G | title = Male sterility in plants: occurrence, determinism, significance and use | journal = Comptes Rendus de l'Académie des Sciences, Série III | volume = 324 | issue = 6 | pages = 543–50 | date = June 2001 | pmid = 11455877 | doi = 10.1016/S0764-4469(01)01324-5}}</ref><ref>{{cite journal | vauthors = Budar F, Touzet P, De Paepe R | title = The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited | journal = Genetica | volume = 117 | issue = 1 | pages = 3–16 | date = January 2003 | pmid = 12656568 | doi = 10.1023/A:1022381016145 | s2cid = 20114356 }}</ref> | ||
The co-evolutionary arms race between selfish mitochondrial genes and nuclear compensatory alleles can often be detected by crossing individuals from different species that have different combinations of male sterility genes and nuclear restorers, resulting in hybrids with a mismatch.<ref>Case AL, Finseth FR, Barr CM, Fishman L |
The co-evolutionary arms race between selfish mitochondrial genes and nuclear compensatory alleles can often be detected by crossing individuals from different species that have different combinations of male sterility genes and nuclear restorers, resulting in hybrids with a mismatch.<ref>{{cite journal | vauthors = Case AL, Finseth FR, Barr CM, Fishman L | title = Selfish evolution of cytonuclear hybrid incompatibility in Mimulus | journal = Proceedings. Biological Sciences | volume = 283 | issue = 1838 | pages = 20161493| date = September 2016 | pmid = 27629037 | pmc = 5031664 | doi = 10.1098/rspb.2016.1493 }}</ref> | ||
Another consequence of the maternal inheritance of the mitochondrial genome is the so-called ].<ref>Gemmell NJ, Metcalf VJ, Allendorf FW |
Another consequence of the maternal inheritance of the mitochondrial genome is the so-called ].<ref>{{cite journal | vauthors = Gemmell NJ, Metcalf VJ, Allendorf FW | title = Mother's curse: the effect of mtDNA on individual fitness and population viability | journal = Trends in Ecology & Evolution | volume = 19 | issue = 5 | pages = 238–44 | date = May 2004 | pmid = 16701262 | doi = 10.1016/j.tree.2004.02.002 }}</ref> Because genes in the mitochondrial genome are strictly maternally inherited, mutations that are beneficial in females can spread in a population even if they are deleterious in males.<ref>{{cite journal | vauthors = Frank SA, Hurst LD | title = Mitochondria and male disease | journal = Nature | volume = 383 | issue = 6597 | pages = 224 | date = September 1996 | pmid = 8805695 | doi = 10.1038/383224a0 | bibcode = 1996Natur.383..224F | s2cid = 4337540 | doi-access = free }}</ref> Explicit screens in fruit flies have successfully identified such female-neutral but male-harming mtDNA mutations.<ref>{{cite journal | vauthors = Camus MF, Clancy DJ, Dowling DK | title = Mitochondria, maternal inheritance, and male aging | journal = Current Biology | volume = 22 | issue = 18 | pages = 1717–21 | date = September 2012 | pmid = 22863313 | doi = 10.1016/j.cub.2012.07.018 | doi-access = free | bibcode = 2012CBio...22.1717C }}</ref><ref>{{cite journal | vauthors = Patel MR, Miriyala GK, Littleton AJ, Yang H, Trinh K, Young JM, Kennedy SR, Yamashita YM, Pallanck LJ, Malik HS | title = A mitochondrial DNA hypomorph of cytochrome oxidase specifically impairs male fertility in Drosophila melanogaster | journal = eLife | volume = 5 | date = August 2016 | pmid = 27481326 | pmc = 4970871 | doi = 10.7554/eLife.16923 | doi-access = free }}</ref> Furthermore, a 2017 paper showed how a mitochondrial mutation causing ], a male-biased eye disease, was brought over by one of the ] that arrived in Quebec, Canada, in the 17th century and subsequently spread among many descendants.<ref>{{cite journal | vauthors = Milot E, Moreau C, Gagnon A, Cohen AA, Brais B, Labuda D | title = Mother's curse neutralizes natural selection against a human genetic disease over three centuries | journal = Nature Ecology & Evolution | volume = 1 | issue = 9 | pages = 1400–1406 | date = September 2017 | pmid = 29046555 | doi = 10.1038/s41559-017-0276-6 | bibcode = 2017NatEE...1.1400M | s2cid = 4183585 }}</ref> | ||
=== Genomic |
=== Genomic imprinting === | ||
] | ] | ||
Another sort of conflict that genomes face is that between the mother and father competing for control of gene expression in the offspring, including the complete silencing of one parental allele. Due to differences in methylation status of gametes, there is an inherent asymmetry to the maternal and paternal genomes that can be used to drive a differential parent-of-origin expression. This results in a violation of |
Another sort of conflict that genomes face is that between the mother and father competing for control of gene expression in the offspring, including the complete silencing of one parental allele. Due to differences in methylation status of gametes, there is an inherent asymmetry to the maternal and paternal genomes that can be used to drive a differential parent-of-origin expression. This results in a violation of Mendel's rules at the level of expression, not transmission, but if the gene expression affects fitness, it can amount to a similar result.<ref name=":22" /> | ||
Imprinting seems like a maladaptive phenomenon, since it essentially means giving up diploidy, and heterozygotes for one defective allele are in trouble if the active allele is the one that is silenced. Several human diseases, such as ] and ] syndromes, are associated with defects in imprinted genes. The asymmetry of maternal and paternal expression suggests that some kind of conflict between these two genomes might be driving the evolution of imprinting. In particular, several genes in placental mammals display expression of paternal genes that maximize offspring growth, and maternal genes that tend to keep that growth in check. Many other conflict-based theories about the evolution of genomic imprinting have been put forward.<ref>Moore T, Haig D |
Imprinting seems like a maladaptive phenomenon, since it essentially means giving up diploidy, and heterozygotes for one defective allele are in trouble if the active allele is the one that is silenced. Several human diseases, such as ] and ] syndromes, are associated with defects in imprinted genes. The asymmetry of maternal and paternal expression suggests that some kind of conflict between these two genomes might be driving the evolution of imprinting. In particular, several genes in placental mammals display expression of paternal genes that maximize offspring growth, and maternal genes that tend to keep that growth in check. Many other conflict-based theories about the evolution of genomic imprinting have been put forward.<ref>{{cite journal | vauthors = Moore T, Haig D | title = Genomic imprinting in mammalian development: a parental tug-of-war | journal = Trends in Genetics | volume = 7 | issue = 2 | pages = 45–9 | date = February 1991 | pmid = 2035190 | doi = 10.1016/0168-9525(91)90230-N }}</ref><ref>{{cite journal | vauthors = Haig D | title = Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting | journal = Heredity | volume = 113 | issue = 2 | pages = 96–103 | date = August 2014 | pmid = 24129605 | pmc = 4105449 | doi = 10.1038/hdy.2013.97 }}</ref> | ||
At the same time, genomic or sexual conflict are not the only possible mechanisms whereby imprinting can evolve.<ref>Spencer HG, Clark AG |
At the same time, genomic or sexual conflict are not the only possible mechanisms whereby imprinting can evolve.<ref name=":22">{{cite journal | vauthors = Spencer HG, Clark AG | title = Non-conflict theories for the evolution of genomic imprinting | journal = Heredity | volume = 113 | issue = 2 | pages = 112–8 | date = August 2014 | pmid = 24398886 | pmc = 4105448 | doi = 10.1038/hdy.2013.129 }}</ref> Several molecular mechanisms for genomic imprinting have been described, and all have the aspect that maternally and paternally derived alleles are made to have distinct epigenetic marks, in particular the degree of methylation of cytosines. An important point to note regarding genomic imprinting is that it is quite heterogeneous, with different mechanisms and different consequences of having single parent-of-origin expression. For example, examining the imprinting status of closely related species allows one to see that a gene that is moved by an inversion into close proximity of imprinted genes may itself acquire an imprinted status, even if there is no particular fitness consequence of the imprinting.<ref name=":22" /> | ||
=== Greenbeards === | === Greenbeards === | ||
A ] is a gene that |
A ] is a gene that has the ability to recognize copies of itself in other individuals and then make its carrier act preferentially toward such individuals. The name itself comes from thought-experiment first presented by William Hamilton<ref name=":27">{{cite journal | vauthors = Hamilton WD | title = The genetical evolution of social behaviour. I | journal = Journal of Theoretical Biology | volume = 7 | issue = 1 | pages = 1–16 | date = July 1964 | pmid = 5875341 | doi = 10.1016/0022-5193(64)90038-4| bibcode = 1964JThBi...7....1H | s2cid = 5310280 }}</ref> and then it was developed and given its current name by Richard Dawkins in ''The Selfish Gene.'' The point of the thought experiment was to highlight that from a gene's-eye view, it is not the genome-wide relatedness that matters (which is usually how kin selection operates, i.e. cooperative behavior is directed towards relatives), but the relatedness at the particular locus that underlies the social behavior.<ref name="TSG" /><ref name=":27" /> | ||
] | ] | ||
The point of the thought experiment was to highlight that from a gene’s-eye view, it is not the genome-wide relatedness that matters (which is usually how kin selection operates, i.e. cooperative behavior is directed towards relatives), but the relatedness at the particular locus that underlies the social behavior. | |||
Following Dawkins, a greenbeard is usually defined as a gene, or set of closely linked genes, that has three effects:<ref>Gardner A, West SA |
Following Dawkins, a greenbeard is usually defined as a gene, or set of closely linked genes, that has three effects:<ref>{{cite journal | vauthors = Gardner A, West SA | title = Greenbeards | journal = Evolution; International Journal of Organic Evolution | volume = 64 | issue = 1 | pages = 25–38 | date = January 2010 | pmid = 19780812 | doi = 10.1111/j.1558-5646.2009.00842.x | s2cid = 221733134 }}</ref> | ||
# It gives carriers of the gene a phenotypic label, such as a greenbeard. | # It gives carriers of the gene a phenotypic label, such as a greenbeard. | ||
Line 93: | Line 100: | ||
# The carrier then behaves altruistically towards individuals with the same label. | # The carrier then behaves altruistically towards individuals with the same label. | ||
Greenbeards |
Greenbeards were long thought to be a fun theoretical idea, with limited possibility of them actually existing in nature. However, since its conception, several examples have been identified, including in yeast,<ref>{{cite journal | vauthors = Smukalla S, Caldara M, Pochet N, Beauvais A, Guadagnini S, Yan C, Vinces MD, Jansen A, Prevost MC, Latgé JP, Fink GR, Foster KR, Verstrepen KJ | display-authors = 6 | title = FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast | journal = Cell | volume = 135 | issue = 4 | pages = 726–37 | date = November 2008 | pmid = 19013280 | pmc = 2703716 | doi = 10.1016/j.cell.2008.09.037 }}</ref> slime moulds,<ref>{{cite journal | vauthors = Queller DC, Ponte E, Bozzaro S, Strassmann JE | title = Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum | journal = Science | volume = 299 | issue = 5603 | pages = 105–6 | date = January 2003 | pmid = 12511650 | doi = 10.1126/science.1077742 | bibcode = 2003Sci...299..105Q | s2cid = 30039249 }}</ref> and fire ants.<ref>{{cite journal | vauthors = Keller L, Ross KG | title = Selfish genes: a green beard in the red fire ant. | journal = Nature | year = 1998 | volume = 394 | issue = 6693 | pages = 573–575 | doi = 10.1038/29064 | bibcode = 1998Natur.394..573K | s2cid = 4310467 }}</ref> | ||
⚫ | There has been some debate whether greenbeard genes should be considered selfish genetic elements.<ref>{{cite journal | vauthors = Ridley M, Grafen A | title = Are green beard genes outlaws? | journal = Anim. Behav. | date = 1981 | volume = 29 | issue = 3 | pages = 954–955 | doi = 10.1016/S0003-3472(81)80034-6 | s2cid = 53167671 }}</ref><ref>{{cite journal | vauthors = Alexander RD, Bargia G | title = Group Selection, Altruism, and the Levels of Organization of Life. | journal = Annu Rev Ecol Syst | date = 1978 | volume = 9 | pages = 449–474 | doi = 10.1146/annurev.es.09.110178.002313 }}</ref><ref name=":23">{{cite journal | vauthors = Biernaskie JM, West SA, Gardner A | title = Are greenbeards intragenomic outlaws? | journal = Evolution; International Journal of Organic Evolution | volume = 65 | issue = 10 | pages = 2729–42 | date = October 2011 | pmid = 21967416 | doi = 10.1111/j.1558-5646.2011.01355.x | s2cid = 6958192 }}</ref> Conflict between a greenbeard locus and the rest of the genome can arise because during a given social interaction between two individuals, the relatedness at the greenbeard locus can be higher than at other loci in the genome. As a consequence, it may in the interest of the greenbeard locus to perform a costly social act, but not in the interest of the rest of the genome.<ref name=":23" /> | ||
In conjunction with selfish genetic elements, greenbeard selection has also been used as a theoretical explanation for suicide.<ref>{{Cite journal|last=Wiley|first=James C.|date=2020-12-01|title=Psychological Aposematism: An Evolutionary Analysis of Suicide|journal=Biological Theory|language=en|volume=15|issue=4|pages=226–238|doi=10.1007/s13752-020-00353-8|s2cid=219734814|issn=1555-5550|doi-access=free}}</ref> | |||
⚫ | There has been some debate whether greenbeard genes should be considered selfish genetic elements.<ref>Ridley M, Grafen A |
||
== Consequences to the host == | == Consequences to the host == | ||
=== Species extinction === | === Species extinction === | ||
Perhaps one of the clearest ways to see that the process of natural selection does not always have organismal fitness as the sole driver is when selfish genetic elements have their way without restriction. In such cases, selfish elements can, in principle, result in species extinction. This possibility was pointed out already in 1928 by Sergey Gershenson<ref name=":5" /> and then in 1967, ]<ref>Hamilton WD |
Perhaps one of the clearest ways to see that the process of natural selection does not always have organismal fitness as the sole driver is when selfish genetic elements have their way without restriction. In such cases, selfish elements can, in principle, result in species extinction. This possibility was pointed out already in 1928 by Sergey Gershenson<ref name=":5" /> and then in 1967, ]<ref>{{cite journal | vauthors = Hamilton WD | title = Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology | journal = Science | volume = 156 | issue = 3774 | pages = 477–88 | date = April 1967 | pmid = 6021675 | doi = 10.1126/science.156.3774.477}}</ref> developed a formal population genetic model for a case of segregation distortion of sex chromosomes driving a population to extinction. In particular, if a selfish element should be able to direct the production of sperm, such that males bearing the element on the Y chromosome would produce an excess of Y-bearing sperm, then in the absence of any countervailing force, this would ultimately result in the Y chromosome going to fixation in the population, producing an extremely male-biased sex ratio. In ecologically challenged species, such biased sex ratios imply that the conversion of resources to offspring becomes very inefficient, to the point of risking extinction.<ref>{{Cite book|title=Allee effects in ecology and conservation|last=Franck.|first=Courchamp|date=2009|publisher=Oxford University Press|isbn=978-0199567553|oclc=929797557}}</ref> | ||
=== Speciation === | === Speciation === | ||
Selfish genetic elements have been shown to play a role in ].<ref name=": |
Selfish genetic elements have been shown to play a role in ].<ref name=":9" /><ref name=":10" /><ref>{{cite journal | vauthors = Patten MM | title = Selfish X chromosomes and speciation | journal = Molecular Ecology | volume = 27 | issue = 19 | pages = 3772–3782 | date = October 2018 | pmid = 29281152 | doi = 10.1111/mec.14471 | bibcode = 2018MolEc..27.3772P | s2cid = 20779621 }}</ref> This could happen because the presence of selfish genetic elements can result in changes in morphology and/or life history, but ways by which the co-evolution between selfish genetic elements and their suppressors can cause reproductive isolation through so-called ] has received particular attention. | ||
An early striking example of hybrid dysgenesis induced by a selfish genetic element was the ''P'' element in ''Drosophila''.<ref>Engels WR |
An early striking example of hybrid dysgenesis induced by a selfish genetic element was the ''P'' element in ''Drosophila''.<ref>{{cite journal | vauthors = Engels WR | title = The origin of P elements in Drosophila melanogaster | journal = BioEssays | volume = 14 | issue = 10 | pages = 681–6 | date = October 1992 | pmid = 1285420 | doi = 10.1002/bies.950141007 | s2cid = 20741333 }}</ref><ref>{{cite journal | vauthors = Kidwell MG | title = Evolution of hybrid dysgenesis determinants in Drosophila melanogaster | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 80 | issue = 6 | pages = 1655–9 | date = March 1983 | pmid = 6300863 | pmc = 393661 | doi = 10.1073/pnas.80.6.1655| bibcode = 1983PNAS...80.1655K | doi-access = free }}</ref> If males carrying the ''P'' element were crossed to females lacking it, the resulting offspring suffered from reduced fitness. However, offspring of the reciprocal cross were normal, as would be expected since ] are maternally inherited. The ''P'' element is typically present only in wild strains, and not in lab strains of ''D. melanogaster'', as the latter were collected before the ''P'' elements were introduced into the species, probably from a closely related ''Drosophila'' species. The ''P'' element story is also a good example of how the rapid co-evolution between selfish genetic elements and their silencers can lead to incompatibilities on short evolutionary time scales, as little as within a few decades.<ref name=":9" /> | ||
Several other examples of selfish genetic elements causing reproductive isolation have since been demonstrated. Crossing different species of ''Arabidopsis'' results in both higher activity of transposable elements<ref>Josefsson C, Dilkes B, Comai L. Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol. 2006;16: 1322–1328.</ref> and disruption in imprinting,<ref>Walia H, Josefsson C, Dilkes B, Kirkbride R, Harada J, Comai L |
Several other examples of selfish genetic elements causing reproductive isolation have since been demonstrated. Crossing different species of ''Arabidopsis'' results in both higher activity of transposable elements<ref>Josefsson C, Dilkes B, Comai L. Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol. 2006;16: 1322–1328.</ref> and disruption in imprinting,<ref>{{cite journal | vauthors = Walia H, Josefsson C, Dilkes B, Kirkbride R, Harada J, Comai L | title = Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility | journal = Current Biology | volume = 19 | issue = 13 | pages = 1128–32 | date = July 2009 | pmid = 19559614 | pmc = 6754343 | doi = 10.1016/j.cub.2009.05.068 | bibcode = 2009CBio...19.1128W }}</ref> both of which have been linked to fitness reduction in the resulting hybrids. Hybrid dysgenesis has also been shown to be caused by centromeric drive in barley<ref>{{cite journal | vauthors = Sanei M, Pickering R, Kumke K, Nasuda S, Houben A | title = Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 108 | issue = 33 | pages = E498–505 | date = August 2011 | pmid = 21746892 | pmc = 3158150 | doi = 10.1073/pnas.1103190108 | doi-access = free }}</ref> and in several species of angiosperms by mito-nuclear conflict.<ref>{{cite journal | vauthors = Rieseberg LH, Blackman BK | title = Speciation genes in plants | journal = Annals of Botany | volume = 106 | issue = 3 | pages = 439–55 | date = September 2010 | pmid = 20576737 | pmc = 2924826 | doi = 10.1093/aob/mcq126 }}</ref> | ||
=== Genome |
=== Genome-size variation === | ||
Attempts to understand the extraordinary variation in genome size (])—animals vary 7,000 fold and land plants some 2,400-fold—has a long history in biology.<ref>Ryan Gregory T |
Attempts to understand the extraordinary variation in genome size (])—animals vary 7,000 fold and land plants some 2,400-fold—has a long history in biology.<ref>{{cite book | last = Ryan | first = Gregory T | title = The Evolution of the Genome | publisher = Academic Press | date = 2005 | isbn = 978-0-12-301463-4 }}</ref> However, this variation is poorly correlated with gene number or any measure of organismal complexity, which led CA Thomas to coin the term C-value paradox in 1971.<ref>{{cite journal | vauthors = Thomas CA | title = The genetic organization of chromosomes | journal = Annu Rev Genet | date = December 1971 | volume = 5 | pages = 237–256 | doi = 10.1146/annurev.ge.05.120171.001321 | pmid = 16097657 }}</ref> The discovery of non-coding DNA resolved some of the paradox, and most current researchers now use the term "C-value enigma".<ref>{{cite journal | vauthors = Gregory TR | title = Macroevolution, hierarchy theory, and the C-value enigma. | journal = Paleobiology | year = 2004 | volume = 30 | issue = 2 | pages = 179–202 | doi = 10.1666/0094-8373(2004)030<0179:MHTATC>2.0.CO;2 | bibcode = 2004Pbio...30..179G | s2cid = 86214775 }}</ref> | ||
Two kinds of selfish genetic elements in particular have been shown to contribute to genome |
Two kinds of selfish genetic elements in particular have been shown to contribute to genome-size variation: B chromosomes and transposable elements.<ref name=":12" /><ref>{{cite journal | vauthors = Ågren JA, Wright SI | title = Selfish genetic elements and plant genome size evolution | journal = Trends in Plant Science | volume = 20 | issue = 4 | pages = 195–6 | date = April 2015 | pmid = 25802093 | doi = 10.1016/j.tplants.2015.03.007 }}</ref> The contribution of transposable elements to the genome is especially well studied in plants.<ref name=":18" /><ref name=":19" /><ref>{{cite journal | vauthors = Wright SI, Agren JA | title = Sizing up Arabidopsis genome evolution | journal = Heredity | volume = 107 | issue = 6 | pages = 509–10 | date = December 2011 | pmid = 21712843 | pmc = 3242632 | doi = 10.1038/hdy.2011.47 }}</ref> A striking example is how the genome of the model organism '']'' contains the same number of genes as that of the Norwegian spruce (''Picea abies''), around 30,000, but accumulation of transposons means that the genome of the latter is some 100 times larger. Transposable element abundance has also been shown to cause the unusually large genomes found in salamanders.<ref>{{cite journal | vauthors = Sun C, Shepard DB, Chong RA, López Arriaza J, Hall K, Castoe TA, Feschotte C, Pollock DD, Mueller RL | title = LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders | journal = Genome Biology and Evolution | volume = 4 | issue = 2 | pages = 168–83 | date = 2012 | pmid = 22200636 | pmc = 3318908 | doi = 10.1093/gbe/evr139 }}</ref> | ||
The presence of an abundance of transposable elements in many eukaryotic genomes was a central theme of the original selfish DNA papers mentioned above (See ]). Most people quickly accepted the central message of those papers, that the existence of transposable elements can be explained by selfish selection at the gene level and there is no need to invoke individual level selection. However, the idea that organisms keep transposable elements around as genetic reservoir to |
The presence of an abundance of transposable elements in many eukaryotic genomes was a central theme of the original selfish DNA papers mentioned above (See ]). Most people quickly accepted the central message of those papers, that the existence of transposable elements can be explained by selfish selection at the gene level and there is no need to invoke individual level selection. However, the idea that organisms keep transposable elements around as genetic reservoir to "speed up evolution" or for other regulatory functions persists in some quarters.<ref>{{cite journal | vauthors = Fedoroff NV | title = Presidential address. Transposable elements, epigenetics, and genome evolution | journal = Science | volume = 338 | issue = 6108 | pages = 758–67 | date = November 2012 | pmid = 23145453 | doi = 10.1126/science.338.6108.758| doi-access = free }}</ref> In 2012, when the ] published a paper claiming that 80% of the human genome can be assigned a function, a claim interpreted by many as the death of the idea of ], this debate was reignited.<ref>{{cite journal | vauthors = Elliott TA, Linquist S, Gregory TR | title = Conceptual and empirical challenges of ascribing functions to transposable elements | journal = The American Naturalist | volume = 184 | issue = 1 | pages = 14–24 | date = July 2014 | pmid = 24921597 | doi = 10.1086/676588 | s2cid = 14549993 | url = http://philsci-archive.pitt.edu/11636/1/Conceptual_and_Empirical_Challenges_%28preprint_version%29.pdf }}</ref><ref>{{cite journal | vauthors = Palazzo AF, Gregory TR | title = The case for junk DNA | journal = PLOS Genetics | volume = 10 | issue = 5 | pages = e1004351 | date = May 2014 | pmid = 24809441 | pmc = 4014423 | doi = 10.1371/journal.pgen.1004351 | doi-access = free }}</ref> | ||
== Applications in agriculture and biotechnology == | == Applications in agriculture and biotechnology == | ||
=== Cytoplasmic male sterility in plant breeding === | === Cytoplasmic male sterility in plant breeding === | ||
A common problem for plant breeders is unwanted self-fertilization. This is particularly a problem when breeders try to cross two different strains to create a new hybrid strain. One way to avoid this is manual emasculation, i.e. physically removing anthers to render the individual male sterile. Cytoplasmic male sterility offers an alternative to this laborious exercise.<ref>Wise RP, Pring DR |
A common problem for plant breeders is unwanted self-fertilization. This is particularly a problem when breeders try to cross two different strains to create a new hybrid strain. One way to avoid this is manual emasculation, i.e. physically removing anthers to render the individual male sterile. Cytoplasmic male sterility offers an alternative to this laborious exercise.<ref>{{cite journal | vauthors = Wise RP, Pring DR | title = Nuclear-mediated mitochondrial gene regulation and male fertility in higher plants: Light at the end of the tunnel? | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 99 | issue = 16 | pages = 10240–2 | date = August 2002 | pmid = 12149484 | pmc = 124896 | doi = 10.1073/pnas.172388899 | bibcode = 2002PNAS...9910240W | doi-access = free }}</ref> Breeders cross a strain that carries a cytoplasmic male sterility mutation with a strain that does not, the latter acting as the pollen donor. If the hybrid offspring are to be harvested for their seed (like maize), and therefore needs to be male fertile, the parental strains need to be homozygous for the restorer allele. In contrast, in species that harvested for their vegetable parts, like onions, this is not an issue. This technique has been used in a wide variety of crops, including rice, maize, sunflower, wheat, and cotton.<ref>{{cite journal | vauthors = Bohra A, Jha UC, Adhimoolam P, Bisht D, Singh NP | title = Cytoplasmic male sterility (CMS) in hybrid breeding in field crops | journal = Plant Cell Reports | volume = 35 | issue = 5 | pages = 967–93 | date = May 2016 | pmid = 26905724 | doi = 10.1007/s00299-016-1949-3 | s2cid = 15935454 }}</ref> | ||
=== PiggyBac vectors === | === PiggyBac vectors === | ||
While many transposable elements seem to do no good for the host, some transposable elements have been |
While many transposable elements seem to do no good for the host, some transposable elements have been "tamed" by molecular biologists so that the elements can be made to insert and excise at the will of the scientist. Such elements are especially useful for doing genetic manipulations, like inserting foreign DNA into the genomes of a variety of organisms.<ref>{{cite journal | vauthors = Ryder E, Russell S | title = Transposable elements as tools for genomics and genetics in Drosophila | journal = Briefings in Functional Genomics & Proteomics | volume = 2 | issue = 1 | pages = 57–71 | date = April 2003 | pmid = 15239944 | doi = 10.1093/bfgp/2.1.57 | doi-access = }}</ref> | ||
One excellent example of this is ], a transposable element that can efficiently move between cloning vectors and chromosomes using a "cut and paste" mechanism.<ref>Fraser MJ, Ciszczon T, Elick T, Bauser C |
One excellent example of this is ], a transposable element that can efficiently move between cloning vectors and chromosomes using a "cut and paste" mechanism.<ref>{{cite journal | vauthors = Fraser MJ, Ciszczon T, Elick T, Bauser C | title = Precise excision of TTAA-specific lepidopteran transposons piggyBac (IFP2) and tagalong (TFP3) from the baculovirus genome in cell lines from two species of Lepidoptera | journal = Insect Molecular Biology | volume = 5 | issue = 2 | pages = 141–51 | date = May 1996 | pmid = 8673264 | doi = 10.1111/j.1365-2583.1996.tb00048.x| s2cid = 42758313 }}</ref> The investigator constructs a PiggyBac element with the desired payload spliced in, and a second element (the PiggyBac transposase), located on another plasmid vector, can be co-transfected into the target cell. The PiggyBac transposase cuts at the inverted terminal repeat sequences located on both ends of the PiggyBac vector and efficiently moves the contents from the original sites and integrates them into chromosomal positions where the sequence TTAA is found. The three things that make PiggyBac so useful are the remarkably high efficiency of this cut-and-paste operation, its ability to take payloads up to 200 kb in size, and its ability to leave a perfectly seamless cut from a genomic site, leaving no sequences or mutations behind.<ref>{{cite journal | vauthors = Yusa K | title = Seamless genome editing in human pluripotent stem cells using custom endonuclease-based gene targeting and the piggyBac transposon | journal = Nature Protocols | volume = 8 | issue = 10 | pages = 2061–78 | date = October 2013 | pmid = 24071911 | doi = 10.1038/nprot.2013.126 | s2cid = 12746945 }}</ref> | ||
=== CRISPR gene drive and homing endonuclease systems === | === CRISPR gene drive and homing endonuclease systems === | ||
] allows the construction of artificial homing endonucleases, where the construct produces guide RNAs that cut the target gene, and homologous flanking sequences then allow insertion of the same construct harboring the Cas9 gene and the guide RNAs. Such gene drives ought to have the ability to rapidly spread in a population (see ]), and one practical application of such a system that has been proposed is to apply it to a pest population, greatly reducing its numbers or even driving it extinct.<ref name=": |
] allows the construction of artificial homing endonucleases, where the construct produces guide RNAs that cut the target gene, and homologous flanking sequences then allow insertion of the same construct harboring the Cas9 gene and the guide RNAs. Such gene drives ought to have the ability to rapidly spread in a population (see ]), and one practical application of such a system that has been proposed is to apply it to a pest population, greatly reducing its numbers or even driving it extinct.<ref name=":17" /> This has not yet been attempted in the field, but gene drive constructs have been tested in the lab, and the ability to insert into the wild-type homologous allele in heterozygotes for the gene drive has been demonstrated.<ref name=":16" /> Unfortunately, the double-strand break that is introduced by Cas9 can be corrected by ], which would make a perfect copy of the drive, or by ], which would produce "resistant" alleles unable to further propagate themselves. When Cas9 is expressed outside of meiosis, it seems like non-homologous end joining predominates, making this the biggest hurdle to practical application of gene drives.<ref>{{cite journal | vauthors = Champer J, Reeves R, Oh SY, Liu C, Liu J, Clark AG, Messer PW | title = Novel CRISPR/Cas9 gene drive constructs reveal insights into mechanisms of resistance allele formation and drive efficiency in genetically diverse populations | journal = PLOS Genetics | volume = 13 | issue = 7 | pages = e1006796 | date = July 2017 | pmid = 28727785 | pmc = 5518997 | doi = 10.1371/journal.pgen.1006796 | doi-access = free }}</ref> | ||
== Mathematical theory == | == Mathematical theory == | ||
Much of the confusion regarding ideas about selfish genetic elements center on the use of language and the way the elements and their evolutionary dynamics are described.<ref>Gardner A, Welch JJ |
Much of the confusion regarding ideas about selfish genetic elements center on the use of language and the way the elements and their evolutionary dynamics are described.<ref name=":24">{{cite journal | vauthors = Gardner A, Welch JJ | title = A formal theory of the selfish gene | journal = Journal of Evolutionary Biology | volume = 24 | issue = 8 | pages = 1801–13 | date = August 2011 | pmid = 21605218 | doi = 10.1111/j.1420-9101.2011.02310.x | s2cid = 14477476 }}</ref> Mathematical models allow the assumptions and the rules to be given ''a priori'' for establishing mathematical statements about the expected dynamics of the elements in populations. The consequences of having such elements in genomes can then be explored objectively. The mathematics can define very crisply the different classes of elements by their precise behavior within a population, sidestepping any distracting verbiage about the inner hopes and desires of greedy selfish genes. There are many good examples of this approach, and this article focuses on segregation distorters, gene drive systems and transposable elements.<ref name=":24" /> | ||
=== Segregation distorters === | === Segregation distorters === | ||
The mouse t-allele is a classic example of a segregation distorter system that has been modeled in great detail.<ref name=": |
The mouse t-allele is a classic example of a segregation distorter system that has been modeled in great detail.<ref name=":14" /><ref>{{cite journal | vauthors = Lewontin RC, Dunn LC | title = The Evolutionary Dynamics of a Polymorphism in the House Mouse | journal = Genetics | volume = 45 | issue = 6 | pages = 705–22 | date = June 1960 | doi = 10.1093/genetics/45.6.705 | pmid = 17247957 | pmc = 1210083 }}</ref> Heterozygotes for a t-haplotype produce >90% of their gametes bearing the t (see ]), and homozygotes for a t-haplotype die as embryos. This can result in a stable polymorphism, with an equilibrium frequency that depends on the drive strength and direct fitness impacts of t-haplotypes. This is a common theme in the mathematics of segregation distorters:virtually every example we know entails a countervailing selective effect, without which the allele with biased transmission would go to fixation and the segregation distortion would no longer be manifested. Whenever sex chromosomes undergo segregation distortion, the population sex ratio is altered, making these systems particularly interesting. Two classic examples of segregation distortion involving sex chromosomes include the "Sex Ratio" X chromosomes of ''Drosophila pseudoobscura''<ref name=":11" /> and Y chromosome drive suppressors of ''Drosophila mediopunctata''.<ref>{{cite journal | vauthors = Carvalho AB, Vaz SC, Klaczko LB | title = Polymorphism for Y-linked suppressors of sex-ratio in two natural populations of Drosophila mediopunctata | journal = Genetics | volume = 146 | issue = 3 | pages = 891–902 | date = July 1997 | doi = 10.1093/genetics/146.3.891 | pmid = 9215895 | pmc = 1208059 }}</ref> A crucial point about the theory of segregation distorters is that just because there are fitness effects acting against the distorter, this does not guarantee that there will be a stable polymorphism. In fact, some sex chromosome drivers can produce frequency dynamics with wild oscillations and cycles.<ref>{{cite journal | vauthors = Clark AG | title = Natural selection and Y-linked polymorphism | journal = Genetics | volume = 115 | issue = 3 | pages = 569–77 | date = March 1987 | doi = 10.1093/genetics/115.3.569 | pmid = 3569883 | pmc = 1216358 }}</ref> | ||
=== Gene |
=== Gene-drive systems === | ||
The idea of spreading a gene into a population as a means of population control is actually quite old, and models for the dynamics of introduced compound chromosomes date back to the 1970s.<ref>Fitz-Earle M, Holm DG, Suzuki DT |
The idea of spreading a gene into a population as a means of population control is actually quite old, and models for the dynamics of introduced compound chromosomes date back to the 1970s.<ref>{{cite journal | vauthors = Fitz-Earle M, Holm DG, Suzuki DT | title = Genetic control of insect population. I. Cage studies of chromosome replacement by compound autosomes in Drosophila melanogaster | journal = Genetics | volume = 74 | issue = 3 | pages = 461–75 | date = July 1973 | doi = 10.1093/genetics/74.3.461 | pmid = 4200686 | pmc = 1212962 }}</ref> Subsequently, the population genetics theory for homing endonucleases and CRISPR-based gene drives has become much more advanced.<ref name=":15" /><ref name=":28">{{cite journal | vauthors = Deredec A, Burt A, Godfray HC | title = The population genetics of using homing endonuclease genes in vector and pest management | journal = Genetics | volume = 179 | issue = 4 | pages = 2013–26 | date = August 2008 | pmid = 18660532 | pmc = 2516076 | doi = 10.1534/genetics.108.089037 }}</ref> An important component of modeling these processes in natural populations is to consider the genetic response in the target population. For one thing, any natural population will harbor standing genetic variation, and that variation might well include polymorphism in the sequences homologous to the guide RNAs, or the homology arms that are meant to direct the repair. In addition, different hosts and different constructs may have quite different rates of non-homologous end joining, the form of repair that results in broken or resistant alleles that no longer spread. Full accommodation of the host factors presents considerable challenge for getting a gene drive construct to go to fixation, and Unckless and colleagues<ref>{{cite journal | vauthors = Unckless RL, Clark AG, Messer PW | title = Evolution of Resistance Against CRISPR/Cas9 Gene Drive | journal = Genetics | volume = 205 | issue = 2 | pages = 827–841 | date = February 2017 | pmid = 27941126 | pmc = 5289854 | doi = 10.1534/genetics.116.197285}}</ref> show that in fact the current constructs are quite far from being able to attain even moderate frequencies in natural populations. This is another excellent example showing that just because an element appears to have a strong selfish transmission advantage, whether it can successfully spread may depend on subtle configurations of other parameters in the population.<ref name=":28" /> | ||
=== Transposable elements === | === Transposable elements === | ||
To model the dynamics of transposable elements (TEs) within a genome, one has to realize that the elements behave like a population within each genome, and they can jump from one haploid genome to another by horizontal transfer. The mathematics has to describe the rates and dependencies of these transfer events. It was observed early on that the rate of jumping of many TEs varies with copy number, and so the first models simply used an empirical function for the rate of transposition. This had the advantage that it could be measured by experiments in the lab, but it left open the question of why the rate differs among elements and differs with copy number. Stan Sawyer and Daniel L. Hartl<ref>Sawyer S, Hartl D |
To model the dynamics of transposable elements (TEs) within a genome, one has to realize that the elements behave like a population within each genome, and they can jump from one haploid genome to another by horizontal transfer. The mathematics has to describe the rates and dependencies of these transfer events. It was observed early on that the rate of jumping of many TEs varies with copy number, and so the first models simply used an empirical function for the rate of transposition. This had the advantage that it could be measured by experiments in the lab, but it left open the question of why the rate differs among elements and differs with copy number. Stan Sawyer and Daniel L. Hartl<ref>{{cite journal | vauthors = Sawyer S, Hartl D | title = Distribution of transposable elements in prokaryotes | journal = Theoretical Population Biology | volume = 30 | issue = 1 | pages = 1–16 | date = August 1986 | pmid = 3018953 | doi = 10.1016/0040-5809(86)90021-3}}</ref> fitted models of this sort to a variety of bacterial TEs, and obtained quite good fits between copy number and transmission rate and the population-wide incidence of the TEs. TEs in higher organisms, like ''Drosophila'', have a very different dynamics because of sex, and ], ], Charles Langley, John Brookfield and others<ref name=":13" /><ref>{{cite journal | vauthors = Brookfield JF, Badge RM | title = Population genetics models of transposable elements | journal = Genetica | volume = 100 | issue = 1–3 | pages = 281–94 | date = 1997 | pmid = 9440281 | doi = 10.1023/A:1018310418744| s2cid = 40644313 }}</ref><ref>{{cite journal | vauthors = Charlesworth B, Charlesworth D | title = The population dynamics of transposable elements. | journal = Genet. Res. | date = 1983 | volume = 42 | pages = 1–27 | doi = 10.1017/S0016672300021455 | doi-access = free }}</ref> modeled TE copy number evolution in ''Drosophila'' and other species. What is impressive about all these modeling efforts is how well they fitted empirical data, given that this was decades before discovery of the fact that the host fly has a powerful defense mechanism in the form of piRNAs. Incorporation of host defense along with TE dynamics into evolutionary models of TE regulation is still in its infancy.<ref>{{cite journal | vauthors = Lu J, Clark AG | title = Population dynamics of PIWI-interacting RNAs (piRNAs) and their targets in Drosophila | journal = Genome Research | volume = 20 | issue = 2 | pages = 212–27 | date = February 2010 | pmid = 19948818 | pmc = 2813477 | doi = 10.1101/gr.095406.109 }}</ref> | ||
== See also == | == See also == | ||
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== References == | == References == | ||
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{{Academic peer reviewed|journal=]|doi=10.1371/journal.pgen.1007700|review=http://topicpageswiki.plos.org/Talk:Selfish_Genetic_Elements|title=Selfish genetic elements|authors=Ågren A, Clark A|date=2018|volume=14|issue=11|pages=e1007700|pmid=|pmc=}}{{Reflist}} | |||
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== Further reading == | == Further reading == | ||
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*Burt |
* {{cite book | last1 = Burt | first1 = Austin | last2 = Trivers | first2 = Robert | name-list-style = vanc | date = 2006 | title = Genes in conflict: the biology of selfish genetic elements | publisher = Harvard University Press | isbn = 978-0-674-02722-0 }} | ||
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Latest revision as of 19:18, 29 October 2024
Genetic segments that can enhance their own transmission at the expense of other genesSelfish genetic elements (historically also referred to as selfish genes, ultra-selfish genes, selfish DNA, parasitic DNA and genomic outlaws) are genetic segments that can enhance their own transmission at the expense of other genes in the genome, even if this has no positive or a net negative effect on organismal fitness. Genomes have traditionally been viewed as cohesive units, with genes acting together to improve the fitness of the organism.
Early observations of selfish genetic elements were made almost a century ago, but the topic did not get widespread attention until several decades later. Inspired by the gene-centred views of evolution popularized by George Williams and Richard Dawkins, two papers were published back-to-back in Nature in 1980 – by Leslie Orgel and Francis Crick and by Ford Doolittle and Carmen Sapienza – introducing the concept of selfish genetic elements (at the time called "selfish DNA") to the wider scientific community. Both papers emphasized that genes can spread in a population regardless of their effect on organismal fitness as long as they have a transmission advantage.
Selfish genetic elements have now been described in most groups of organisms, and they demonstrate a remarkable diversity in the ways by which they promote their own transmission. Though long dismissed as genetic curiosities, with little relevance for evolution, they are now recognized to affect a wide swath of biological processes, ranging from genome size and architecture to speciation.
History
Early observations
Observations of what is now referred to as selfish genetic elements go back to the early days in the history of genetics. Already in 1928, Russian geneticist Sergey Gershenson reported the discovery of a driving X chromosome in Drosophila obscura. Crucially, he noted that the resulting female-biased sex ratio may drive a population extinct (see Species extinction). The earliest clear statement of how chromosomes may spread in a population not because of their positive fitness effects on the individual organism, but because of their own "parasitic" nature came from the Swedish botanist and cytogeneticist Gunnar Östergren in 1945. Discussing B chromosomes in plants he wrote:
In many cases these chromosomes have no useful function at all to the species carrying them, but that they often lead an exclusively parasitic existence ... need not be useful for the plants. They need only be useful to themselves.
Around the same time, several other examples of selfish genetic elements were reported. For example, the American maize geneticist Marcus Rhoades described how chromosomal knobs led to female meiotic drive in maize. Similarly, this was also when it was first suggested that an intragenomic conflict between uniparentally inherited mitochondrial genes and biparentally inherited nuclear genes could lead to cytoplasmic male sterility in plants. Then, in the early 1950s, Barbara McClintock published a series of papers describing the existence of transposable elements, which are now recognized to be among the most successful selfish genetic elements. The discovery of transposable elements led to her being awarded the Nobel Prize in Medicine or Physiology in 1983.
Conceptual developments
The empirical study of selfish genetic elements benefited greatly from the emergence of the so-called gene-centred view of evolution in the nineteen sixties and seventies. In contrast with Darwin's original formulation of the theory of evolution by natural selection that focused on individual organisms, the gene's-eye view takes the gene to be the central unit of selection in evolution. It conceives evolution by natural selection as a process involving two separate entities: replicators (entities that produce faithful copies of themselves, usually genes) and vehicles (or interactors; entities that interact with the ecological environment, usually organisms).
Since organisms are temporary occurrences, present in one generation and gone in the next, genes (replicators) are the only entity faithfully transmitted from parent to offspring. Viewing evolution as a struggle between competing replicators made it easier to recognize that not all genes in an organism would share the same evolutionary fate.
The gene's-eye view was a synthesis of the population genetic models of the modern synthesis, in particular the work of RA Fisher, and the social evolution models of W. D. Hamilton. The view was popularized by George Williams's Adaptation and Natural Selection and Richard Dawkins's best seller The Selfish Gene. Dawkins summarized a key benefit from the gene's-eye view as follows:
"If we allow ourselves the license of talking about genes as if they had conscious aims, always reassuring ourselves that we could translate our sloppy language back into respectable terms if we wanted to, we can ask the question, what is a single selfish gene trying to do?" — Richard Dawkins, The Selfish Gene
In 1980, two high-profile papers published back-to-back in Nature by Leslie Orgel and Francis Crick, and by Ford Doolittle and Carmen Sapienza, brought the study of selfish genetic elements to the centre of biological debate. The papers took their starting point in the contemporary debate of the so-called C-value paradox, the lack of correlation between genome size and perceived complexity of a species. Both papers attempted to counter the prevailing view of the time that the presence of differential amounts of non-coding DNA and transposable elements is best explained from the perspective of individual fitness, described as the "phenotypic paradigm" by Doolittle and Sapienza. Instead, the authors argued that much of the genetic material in eukaryotic genomes persists, not because of its phenotypic effects, but can be understood from a gene's-eye view, without invoking individual-level explanations. The two papers led to a series of exchanges in Nature.
Current views
If the selfish DNA papers marked the beginning of the serious study of selfish genetic elements, the subsequent decades have seen an explosion in theoretical advances and empirical discoveries. Leda Cosmides and John Tooby wrote a landmark review about the conflict between maternally inherited cytoplasmic genes and biparentally inherited nuclear genes. The paper also provided a comprehensive introduction to the logic of genomic conflicts, foreshadowing many themes that would later be subject of much research. Then in 1988 John H. Werren and colleagues wrote the first major empirical review of the topic. This paper achieved three things. First, it coined the term selfish genetic element, putting an end to a sometimes confusingly diverse terminology (selfish genes, ultra-selfish genes, selfish DNA, parasitic DNA, genomic outlaws). Second, it formally defined the concept of selfish genetic elements. Finally, it was the first paper to bring together all different kinds of selfish genetic elements known at the time (genomic imprinting, for example, was not covered).
In the late 1980s, most molecular biologists considered selfish genetic elements to be the exception, and that genomes were best thought of as highly integrated networks with a coherent effect on organismal fitness. In 2006, when Austin Burt and Robert Trivers published the first book-length treatment of the topic, the tide was changing. While their role in evolution long remained controversial, in a review published a century after their first discovery, William R. Rice concluded that "nothing in genetics makes sense except in the light of genomic conflicts".
Logic
Though selfish genetic elements show a remarkable diversity in the way they promote their own transmission, some generalizations about their biology can be made. In a classic 2001 review, Gregory D.D. Hurst and John H. Werren proposed two ‘rules' of selfish genetic elements.
Rule 1: Spread requires sex and outbreeding
Sexual reproduction involves the mixing of genes from two individuals. According to Mendel's Law of Segregation, alleles in a sexually reproducing organism have a 50% chance of being passed from parent to offspring. Meiosis is therefore sometimes referred to as "fair".
Highly self-fertilizing or asexual genomes are expected to experience less conflict between selfish genetic elements and the rest of the host genome than outcrossing sexual genomes. There are several reasons for this. First, sex and outcrossing put selfish genetic elements into new genetic lineages. In contrast, in a highly selfing or asexual lineage, any selfish genetic element is essentially stuck in that lineage, which should increase variation in fitness among individuals. The increased variation should result in stronger purifying selection in selfers/asexuals, as a lineage without the selfish genetic elements should out-compete a lineage with the selfish genetic element. Second, the increased homozygosity in selfers removes the opportunity for competition among homologous alleles. Third, theoretical work has shown that the greater linkage disequilibrium in selfing compared to outcrossing genomes may in some, albeit rather limited, cases cause selection for reduced transposition rates. Overall, this reasoning leads to the prediction that asexuals/selfers should experience a lower load of selfish genetic elements. One caveat to this is that the evolution of selfing is associated with a reduction in the effective population size. A reduction in the effective population size should reduce the efficacy of selection and therefore leads to the opposite prediction: higher accumulation of selfish genetic elements in selfers relative to outcrossers.
Empirical evidence for the importance of sex and outcrossing comes from a variety of selfish genetic elements, including transposable elements, self-promoting plasmids, and B chromosomes.
Rule 2: Presence is often revealed in hybrids
The presence of selfish genetic elements can be difficult to detect in natural populations. Instead, their phenotypic consequences often become apparent in hybrids. The first reason for this is that some selfish genetic elements rapidly sweep to fixation, and the phenotypic effects will therefore not be segregating in the population. Hybridization events, however, will produce offspring with and without the selfish genetic elements and so reveal their presence. The second reason is that host genomes have evolved mechanisms to suppress the activity of the selfish genetic elements, for example the small RNA administered silencing of transposable elements. The co-evolution between selfish genetic elements and their suppressors can be rapid, and follow a Red Queen dynamics, which may mask the presence of selfish genetic elements in a population. Hybrid offspring, on the other hand, may inherit a given selfish genetic element, but not the corresponding suppressor and so reveal the phenotypic effect of the selfish genetic element.
Examples
Segregation distorters
Some selfish genetic elements manipulate the genetic transmission process to their own advantage, and so end up being overrepresented in the gametes. Such distortion can occur in various ways, and the umbrella term that encompasses all of them is segregation distortion. Some elements can preferentially be transmitted in egg cells as opposed to polar bodies during meiosis, where only the former will be fertilized and transmitted to the next generation. Any gene that can manipulate the odds of ending up in the egg rather than the polar body will have a transmission advantage, and will increase in frequency in a population.
Segregation distortion can happen in several ways. When this process occurs during meiosis it is referred to as meiotic drive. Many forms of segregation distortion occur in male gamete formation, where there is differential mortality of spermatids during the process of sperm maturation or spermiogenesis. The segregation distorter (SD) in Drosophila melanogaster is the best studied example, and it involves a nuclear envelope protein Ran-GAP and the X-linked repeat array called Responder (Rsp), where the SD allele of Ran-GAP favors its own transmission only in the presence of a Rsp allele on the homologous chromosome. SD acts to kill RSP sperm, in a post-meiotic process (hence it is not strictly speaking meiotic drive). Systems like this can have interesting rock-paper-scissors dynamics, oscillating between the SD-RSP, SD+-RSP and SD+-RSP haplotypes. The SD-RSP haplotype is not seen because it essentially commits suicide.
When segregation distortion acts on sex chromosomes, they can skew the sex ratio. The SR system in Drosophila pseudoobscura, for example, is on the X chromosome, and XSR/Y males produce only daughters, whereas females undergo normal meiosis with Mendelian proportions of gametes. Segregation distortion systems would drive the favored allele to fixation, except that most of the cases where these systems have been identified have the driven allele opposed by some other selective force. One example is the lethality of the t-haplotype in mice, another is the effect on male fertility of the Sex Ratio system in D. pseudoobscura.
Homing endonucleases
A phenomenon closely related to segregation distortion is homing endonucleases. These are enzymes that cut DNA in a sequence-specific way, and those cuts, generally double-strand breaks, are then "healed" by the regular DNA repair machinery. Homing endonucleases insert themselves into the genome at the site homologous to the first insertion site, resulting in a conversion of a heterozygote into a homozygote bearing a copy of the homing endonuclease on both homologous chromosomes. This gives homing endonucleases an allele frequency dynamics rather similar to a segregation distortion system, and generally unless opposed by strong countervailing selection, they are expected to go to fixation in a population. CRISPR-Cas9 technology allows the artificial construction of homing endonuclease systems. These so-called "gene drive" systems pose a combination of great promise for biocontrol but also potential risk.
Transposable elements
Transposable elements (TEs) include a wide variety of DNA sequences that all have the ability to move to new locations in the genome of their host. Transposons do this by a direct cut-and-paste mechanism, whereas retrotransposons need to produce an RNA intermediate to move. TEs were first discovered in maize by Barbara McClintock in the 1940s and their ability to occur in both active and quiescent states in the genome was also first elucidated by McClintock. TEs have been referred to as selfish genetic elements because they have some control over their own propagation in the genome. Most random insertions into the genome appear to be relatively innocuous, but they can disrupt critical gene functions with devastating results. For example, TEs have been linked to a variety of human diseases, ranging from cancer to haemophilia. TEs that tend to avoid disrupting vital functions in the genome tend to remain in the genome longer, and hence they are more likely to be found in innocuous locations.
Both plant and animal hosts have evolved means for reducing the fitness impact of TEs, both by directly silencing them and by reducing their ability to transpose in the genome. It would appear that hosts in general are fairly tolerant of TEs in their genomes, since a sizable portion (30-80%) of the genome of many animals and plants is TEs. When the host is able to stop their movement, TEs can simply be frozen in place, and it then can take millions of years for them to mutate away. The fitness of a TE is a combination of its ability to expand in numbers within a genome, to evade host defenses, but also to avoid eroding host fitness too drastically. The effect of TEs in the genome is not entirely selfish. Because their insertion into the genome can disrupt gene function, sometimes those disruptions can have positive fitness value for the host. Many adaptive changes in Drosophila and dogs for example, are associated with TE insertions.
B chromosomes
B chromosomes refer to chromosomes that are not required for the viability or fertility of the organism, but exist in addition to the normal (A) set. They persist in the population and accumulate because they have the ability to propagate their own transmission independently of the A chromosomes. They often vary in copy number between individuals of the same species.
B chromosomes were first detected over a century ago. Though typically smaller than normal chromosomes, their gene poor, heterochromatin-rich structure made them visible to early cytogenetic techniques. B chromosomes have been thoroughly studied and are estimated to occur in 15% of all eukaryotic species. In general, they appear to be particularly common among eudicot plants, rare in mammals, and absent in birds. In 1945, they were the subject of Gunnar Östergren's classic paper "Parasitic nature of extra fragment chromosomes", where he argues that the variation in abundance of B chromosomes between and within species is because of the parasitic properties of the Bs. This was the first time genetic material was referred to as "parasitic" or "selfish". B chromosome number correlates positively with genome size and has also been linked to a decrease in egg production in the grasshopper Eyprepocnemis plorans.
Selfish mitochondria
Genomic conflicts often arise because not all genes are inherited in the same way. Probably the best example of this is the conflict between uniparentally (usually but not always, maternally) inherited mitochondrial and biparentally inherited nuclear genes. Indeed, one of the earliest clear statements about the possibility of genomic conflict was made by the English botanist Dan Lewis in reference to the conflict between maternally inherited mitochondrial and biparentally inherited nuclear genes over sex allocation in hermaphroditic plants.
A single cell typically contains multiple mitochondria, creating a situation for competition over transmission. Uniparental inheritance has been suggested to be a way to reduce the opportunity for selfish mitochondria to spread, as it ensures all mitochondria share the same genome, thus removing the opportunity for competition. This view remains widely held, but has been challenged. Why inheritance ended up being maternal, rather than paternal, is also much debated, but one key hypothesis is that the mutation rate is lower in female compared to male gametes.
The conflict between mitochondrial and nuclear genes is especially easy to study in flowering plants. Flowering plants are typically hermaphrodites, and the conflict thus occurs within a single individual. Mitochondrial genes are typically only transmitted through female gametes, and therefore from their point of view the production of pollen leads to an evolutionary dead end. Any mitochondrial mutation that can affect the amount of resources the plant invests in the female reproductive functions at the expense of the male reproductive functions improves its own chance of transmission. Cytoplasmic male sterility is the loss of male fertility, typically through loss of functional pollen production, resulting from a mitochondrial mutation. In many species where cytoplasmic male sterility occurs, the nuclear genome has evolved so-called restorer genes, which repress the effects of the cytoplasmic male sterility genes and restore the male function, making the plant a hermaphrodite again.
The co-evolutionary arms race between selfish mitochondrial genes and nuclear compensatory alleles can often be detected by crossing individuals from different species that have different combinations of male sterility genes and nuclear restorers, resulting in hybrids with a mismatch.
Another consequence of the maternal inheritance of the mitochondrial genome is the so-called Mother's Curse. Because genes in the mitochondrial genome are strictly maternally inherited, mutations that are beneficial in females can spread in a population even if they are deleterious in males. Explicit screens in fruit flies have successfully identified such female-neutral but male-harming mtDNA mutations. Furthermore, a 2017 paper showed how a mitochondrial mutation causing Leber's hereditary optic neuropathy, a male-biased eye disease, was brought over by one of the Filles du roi that arrived in Quebec, Canada, in the 17th century and subsequently spread among many descendants.
Genomic imprinting
Another sort of conflict that genomes face is that between the mother and father competing for control of gene expression in the offspring, including the complete silencing of one parental allele. Due to differences in methylation status of gametes, there is an inherent asymmetry to the maternal and paternal genomes that can be used to drive a differential parent-of-origin expression. This results in a violation of Mendel's rules at the level of expression, not transmission, but if the gene expression affects fitness, it can amount to a similar result.
Imprinting seems like a maladaptive phenomenon, since it essentially means giving up diploidy, and heterozygotes for one defective allele are in trouble if the active allele is the one that is silenced. Several human diseases, such as Prader-Willi and Angelman syndromes, are associated with defects in imprinted genes. The asymmetry of maternal and paternal expression suggests that some kind of conflict between these two genomes might be driving the evolution of imprinting. In particular, several genes in placental mammals display expression of paternal genes that maximize offspring growth, and maternal genes that tend to keep that growth in check. Many other conflict-based theories about the evolution of genomic imprinting have been put forward.
At the same time, genomic or sexual conflict are not the only possible mechanisms whereby imprinting can evolve. Several molecular mechanisms for genomic imprinting have been described, and all have the aspect that maternally and paternally derived alleles are made to have distinct epigenetic marks, in particular the degree of methylation of cytosines. An important point to note regarding genomic imprinting is that it is quite heterogeneous, with different mechanisms and different consequences of having single parent-of-origin expression. For example, examining the imprinting status of closely related species allows one to see that a gene that is moved by an inversion into close proximity of imprinted genes may itself acquire an imprinted status, even if there is no particular fitness consequence of the imprinting.
Greenbeards
A greenbeard gene is a gene that has the ability to recognize copies of itself in other individuals and then make its carrier act preferentially toward such individuals. The name itself comes from thought-experiment first presented by William Hamilton and then it was developed and given its current name by Richard Dawkins in The Selfish Gene. The point of the thought experiment was to highlight that from a gene's-eye view, it is not the genome-wide relatedness that matters (which is usually how kin selection operates, i.e. cooperative behavior is directed towards relatives), but the relatedness at the particular locus that underlies the social behavior.
Following Dawkins, a greenbeard is usually defined as a gene, or set of closely linked genes, that has three effects:
- It gives carriers of the gene a phenotypic label, such as a greenbeard.
- The carrier is able to recognize other individuals with the same label.
- The carrier then behaves altruistically towards individuals with the same label.
Greenbeards were long thought to be a fun theoretical idea, with limited possibility of them actually existing in nature. However, since its conception, several examples have been identified, including in yeast, slime moulds, and fire ants.
There has been some debate whether greenbeard genes should be considered selfish genetic elements. Conflict between a greenbeard locus and the rest of the genome can arise because during a given social interaction between two individuals, the relatedness at the greenbeard locus can be higher than at other loci in the genome. As a consequence, it may in the interest of the greenbeard locus to perform a costly social act, but not in the interest of the rest of the genome.
In conjunction with selfish genetic elements, greenbeard selection has also been used as a theoretical explanation for suicide.
Consequences to the host
Species extinction
Perhaps one of the clearest ways to see that the process of natural selection does not always have organismal fitness as the sole driver is when selfish genetic elements have their way without restriction. In such cases, selfish elements can, in principle, result in species extinction. This possibility was pointed out already in 1928 by Sergey Gershenson and then in 1967, Bill Hamilton developed a formal population genetic model for a case of segregation distortion of sex chromosomes driving a population to extinction. In particular, if a selfish element should be able to direct the production of sperm, such that males bearing the element on the Y chromosome would produce an excess of Y-bearing sperm, then in the absence of any countervailing force, this would ultimately result in the Y chromosome going to fixation in the population, producing an extremely male-biased sex ratio. In ecologically challenged species, such biased sex ratios imply that the conversion of resources to offspring becomes very inefficient, to the point of risking extinction.
Speciation
Selfish genetic elements have been shown to play a role in speciation. This could happen because the presence of selfish genetic elements can result in changes in morphology and/or life history, but ways by which the co-evolution between selfish genetic elements and their suppressors can cause reproductive isolation through so-called Bateson–Dobzhansky–Muller incompatibilities has received particular attention.
An early striking example of hybrid dysgenesis induced by a selfish genetic element was the P element in Drosophila. If males carrying the P element were crossed to females lacking it, the resulting offspring suffered from reduced fitness. However, offspring of the reciprocal cross were normal, as would be expected since piRNAs are maternally inherited. The P element is typically present only in wild strains, and not in lab strains of D. melanogaster, as the latter were collected before the P elements were introduced into the species, probably from a closely related Drosophila species. The P element story is also a good example of how the rapid co-evolution between selfish genetic elements and their silencers can lead to incompatibilities on short evolutionary time scales, as little as within a few decades.
Several other examples of selfish genetic elements causing reproductive isolation have since been demonstrated. Crossing different species of Arabidopsis results in both higher activity of transposable elements and disruption in imprinting, both of which have been linked to fitness reduction in the resulting hybrids. Hybrid dysgenesis has also been shown to be caused by centromeric drive in barley and in several species of angiosperms by mito-nuclear conflict.
Genome-size variation
Attempts to understand the extraordinary variation in genome size (C-value)—animals vary 7,000 fold and land plants some 2,400-fold—has a long history in biology. However, this variation is poorly correlated with gene number or any measure of organismal complexity, which led CA Thomas to coin the term C-value paradox in 1971. The discovery of non-coding DNA resolved some of the paradox, and most current researchers now use the term "C-value enigma".
Two kinds of selfish genetic elements in particular have been shown to contribute to genome-size variation: B chromosomes and transposable elements. The contribution of transposable elements to the genome is especially well studied in plants. A striking example is how the genome of the model organism Arabidopsis thaliana contains the same number of genes as that of the Norwegian spruce (Picea abies), around 30,000, but accumulation of transposons means that the genome of the latter is some 100 times larger. Transposable element abundance has also been shown to cause the unusually large genomes found in salamanders.
The presence of an abundance of transposable elements in many eukaryotic genomes was a central theme of the original selfish DNA papers mentioned above (See Conceptual developments). Most people quickly accepted the central message of those papers, that the existence of transposable elements can be explained by selfish selection at the gene level and there is no need to invoke individual level selection. However, the idea that organisms keep transposable elements around as genetic reservoir to "speed up evolution" or for other regulatory functions persists in some quarters. In 2012, when the ENCODE Project published a paper claiming that 80% of the human genome can be assigned a function, a claim interpreted by many as the death of the idea of junk DNA, this debate was reignited.
Applications in agriculture and biotechnology
Cytoplasmic male sterility in plant breeding
A common problem for plant breeders is unwanted self-fertilization. This is particularly a problem when breeders try to cross two different strains to create a new hybrid strain. One way to avoid this is manual emasculation, i.e. physically removing anthers to render the individual male sterile. Cytoplasmic male sterility offers an alternative to this laborious exercise. Breeders cross a strain that carries a cytoplasmic male sterility mutation with a strain that does not, the latter acting as the pollen donor. If the hybrid offspring are to be harvested for their seed (like maize), and therefore needs to be male fertile, the parental strains need to be homozygous for the restorer allele. In contrast, in species that harvested for their vegetable parts, like onions, this is not an issue. This technique has been used in a wide variety of crops, including rice, maize, sunflower, wheat, and cotton.
PiggyBac vectors
While many transposable elements seem to do no good for the host, some transposable elements have been "tamed" by molecular biologists so that the elements can be made to insert and excise at the will of the scientist. Such elements are especially useful for doing genetic manipulations, like inserting foreign DNA into the genomes of a variety of organisms.
One excellent example of this is PiggyBac, a transposable element that can efficiently move between cloning vectors and chromosomes using a "cut and paste" mechanism. The investigator constructs a PiggyBac element with the desired payload spliced in, and a second element (the PiggyBac transposase), located on another plasmid vector, can be co-transfected into the target cell. The PiggyBac transposase cuts at the inverted terminal repeat sequences located on both ends of the PiggyBac vector and efficiently moves the contents from the original sites and integrates them into chromosomal positions where the sequence TTAA is found. The three things that make PiggyBac so useful are the remarkably high efficiency of this cut-and-paste operation, its ability to take payloads up to 200 kb in size, and its ability to leave a perfectly seamless cut from a genomic site, leaving no sequences or mutations behind.
CRISPR gene drive and homing endonuclease systems
CRISPR allows the construction of artificial homing endonucleases, where the construct produces guide RNAs that cut the target gene, and homologous flanking sequences then allow insertion of the same construct harboring the Cas9 gene and the guide RNAs. Such gene drives ought to have the ability to rapidly spread in a population (see Gene-drive systems), and one practical application of such a system that has been proposed is to apply it to a pest population, greatly reducing its numbers or even driving it extinct. This has not yet been attempted in the field, but gene drive constructs have been tested in the lab, and the ability to insert into the wild-type homologous allele in heterozygotes for the gene drive has been demonstrated. Unfortunately, the double-strand break that is introduced by Cas9 can be corrected by homology directed repair, which would make a perfect copy of the drive, or by non-homologous end joining, which would produce "resistant" alleles unable to further propagate themselves. When Cas9 is expressed outside of meiosis, it seems like non-homologous end joining predominates, making this the biggest hurdle to practical application of gene drives.
Mathematical theory
Much of the confusion regarding ideas about selfish genetic elements center on the use of language and the way the elements and their evolutionary dynamics are described. Mathematical models allow the assumptions and the rules to be given a priori for establishing mathematical statements about the expected dynamics of the elements in populations. The consequences of having such elements in genomes can then be explored objectively. The mathematics can define very crisply the different classes of elements by their precise behavior within a population, sidestepping any distracting verbiage about the inner hopes and desires of greedy selfish genes. There are many good examples of this approach, and this article focuses on segregation distorters, gene drive systems and transposable elements.
Segregation distorters
The mouse t-allele is a classic example of a segregation distorter system that has been modeled in great detail. Heterozygotes for a t-haplotype produce >90% of their gametes bearing the t (see Segregation distorters), and homozygotes for a t-haplotype die as embryos. This can result in a stable polymorphism, with an equilibrium frequency that depends on the drive strength and direct fitness impacts of t-haplotypes. This is a common theme in the mathematics of segregation distorters:virtually every example we know entails a countervailing selective effect, without which the allele with biased transmission would go to fixation and the segregation distortion would no longer be manifested. Whenever sex chromosomes undergo segregation distortion, the population sex ratio is altered, making these systems particularly interesting. Two classic examples of segregation distortion involving sex chromosomes include the "Sex Ratio" X chromosomes of Drosophila pseudoobscura and Y chromosome drive suppressors of Drosophila mediopunctata. A crucial point about the theory of segregation distorters is that just because there are fitness effects acting against the distorter, this does not guarantee that there will be a stable polymorphism. In fact, some sex chromosome drivers can produce frequency dynamics with wild oscillations and cycles.
Gene-drive systems
The idea of spreading a gene into a population as a means of population control is actually quite old, and models for the dynamics of introduced compound chromosomes date back to the 1970s. Subsequently, the population genetics theory for homing endonucleases and CRISPR-based gene drives has become much more advanced. An important component of modeling these processes in natural populations is to consider the genetic response in the target population. For one thing, any natural population will harbor standing genetic variation, and that variation might well include polymorphism in the sequences homologous to the guide RNAs, or the homology arms that are meant to direct the repair. In addition, different hosts and different constructs may have quite different rates of non-homologous end joining, the form of repair that results in broken or resistant alleles that no longer spread. Full accommodation of the host factors presents considerable challenge for getting a gene drive construct to go to fixation, and Unckless and colleagues show that in fact the current constructs are quite far from being able to attain even moderate frequencies in natural populations. This is another excellent example showing that just because an element appears to have a strong selfish transmission advantage, whether it can successfully spread may depend on subtle configurations of other parameters in the population.
Transposable elements
To model the dynamics of transposable elements (TEs) within a genome, one has to realize that the elements behave like a population within each genome, and they can jump from one haploid genome to another by horizontal transfer. The mathematics has to describe the rates and dependencies of these transfer events. It was observed early on that the rate of jumping of many TEs varies with copy number, and so the first models simply used an empirical function for the rate of transposition. This had the advantage that it could be measured by experiments in the lab, but it left open the question of why the rate differs among elements and differs with copy number. Stan Sawyer and Daniel L. Hartl fitted models of this sort to a variety of bacterial TEs, and obtained quite good fits between copy number and transmission rate and the population-wide incidence of the TEs. TEs in higher organisms, like Drosophila, have a very different dynamics because of sex, and Brian Charlesworth, Deborah Charlesworth, Charles Langley, John Brookfield and others modeled TE copy number evolution in Drosophila and other species. What is impressive about all these modeling efforts is how well they fitted empirical data, given that this was decades before discovery of the fact that the host fly has a powerful defense mechanism in the form of piRNAs. Incorporation of host defense along with TE dynamics into evolutionary models of TE regulation is still in its infancy.
See also
- C-value enigma
- Endogenous retrovirus
- Gene-centered view of evolution
- Genome size
- Intragenomic conflict
- Introns: introns as mobile genetic elements
- Junk DNA
- Mobile genetic elements
- Mutation
- Noncoding DNA
- Retrotransposon
- Transposable element
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Further reading
- Burt A, Trivers R (2006). Genes in conflict: the biology of selfish genetic elements. Harvard University Press. ISBN 978-0-674-02722-0.