View source for Evolution of sexual reproduction

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{{Evolutionary biology}}
{{Use dmy dates|date=October 2016}}
[[File:Ladybird-Coccinellidae-mating.jpg|thumb|[[Ladybird]]s mating]]
[[File:2012-04-03 16-43-53-amaryllis-sp.jpg|thumb|[[Pollen]] production is an essential step in sexual reproduction of [[seed plant]]s.]]
{{Unsolved|biology|What [[selection pressure]]s led to the evolution and maintenance of sexual reproduction?}}
[[Sexually reproducing]] [[animal]]s, [[plant]]s, [[fungi]] and [[protist]]s are thought to have [[evolved]] from a [[common ancestor]] that was a single-celled [[eukaryotic]] [[species]].<ref name="Letunic I and Bork P">
{{cite web |last1=Letunic |first1=I |last2=Bork |first2=P |year=2006 |title=Interactive Tree of Life |url=http://itol.embl.de/ |access-date=23 July 2011}}</ref><ref>m{{cite journal |last1=Letunic |first1=I |last2=Bork |first2=P |year=2007 |title=Interactive Tree of Life (iTOL): An online tool for phylogenetic tree display and annotation |url=http://itol.embl.de/help/17050570.pdf |journal=[[Bioinformatics (journal)|Bioinformatics]] |volume=23 |issue=1 |pages=127–8 |doi=10.1093/bioinformatics/btl529 |pmid=17050570 |doi-access=free}}</ref><ref>{{cite journal |last1=Letunic |first1=I |last2=Bork |first2=P |year=2011 |title=Interactive Tree of Life v2: Online annotation and display of phylogenetic trees made easy |url=http://itol.embl.de/help/gkr201.pdf |journal=[[Nucleic Acids Research]] |volume=39 |issue=Web Server issue |pages=W475–8 |doi=10.1093/nar/gkr201 |pmc=3125724 |pmid=21470960}}</ref> Sexual reproduction is widespread in eukaryotes, though a few eukaryotic species have secondarily lost the ability to reproduce sexually, such as [[Bdelloidea]], and some plants and animals routinely reproduce [[asexual reproduction|asexually]] (by [[apomixis]] and [[parthenogenesis]]) without entirely having lost [[sex]]. The evolution of sexual reproduction contains two related yet distinct themes: its ''origin'' and its ''maintenance.'' Bacteria and Archaea ([[Prokaryote|prokaryotes]]) have processes that can transfer DNA from one cell to another ([[Sexual conjugation|conjugation]], [[transformation (genetics)|transformation]], and [[transduction (genetics)|transduction]]<ref>{{Cite web |last=Otto |first=Sarah |date=2014 |title=Sexual Reproduction and the Evolution of Sex |url=https://www.nature.com/scitable/topicpage/sexual-reproduction-and-the-evolution-of-sex-824 |access-date=28 Feb 2019 |website=Scitable}}</ref>), but it is unclear if these processes are evolutionarily related to sexual reproduction in Eukaryotes.<ref>{{Cite journal |last=Redfield |first=Rosemary J. |date=August 2001 |title=Do bacteria have sex? |url=http://dx.doi.org/10.1038/35084593 |journal=Nature Reviews Genetics |volume=2 |issue=8 |pages=634–639 |doi=10.1038/35084593 |pmid=11483988 |s2cid=5465846}}</ref> In eukaryotes, true sexual reproduction by meiosis and cell fusion is thought to have arisen in the [[last eukaryotic common ancestor]], possibly via several processes of varying success, and then to have persisted.<ref>{{Cite journal |last1=Goodenough |first1=U. |last2=Heitman |first2=J. |date=2014-03-01 |title=Origins of Eukaryotic Sexual Reproduction |journal=Cold Spring Harbor Perspectives in Biology |volume=6 |issue=3 |pages=a016154 |doi=10.1101/cshperspect.a016154 |issn=1943-0264 |pmc=3949356 |pmid=24591519}}</ref>

Since hypotheses for the origin of sex are difficult to verify experimentally<ref>{{Cite journal |last=Hartfield |first=M |last2=Keightley |first2=PD |date=June 2012 |title=Current hypotheses for the evolution of sex and recombination |url=https://doi.org/10.1111/j.1749-4877.2012.00284.x |journal=Integrative Zoology |volume=7 |issue=2 |pages=192-209 |via=WILEY}}</ref> (outside of [[evolutionary computation]]), most current work has focused on the persistence of sexual reproduction over evolutionary time. The maintenance of sexual reproduction (specifically, of its [[dioecious]] form) by natural selection in a highly competitive world has long been one of the major mysteries of biology, since both other known mechanisms of reproduction – [[asexual reproduction]] and [[hermaphroditism]] – possess apparent advantages over it. Asexual reproduction can proceed by budding, fission, or spore formation and does not involve the union of gametes, which accordingly results in [[#xspeed|a much faster rate]] of reproduction compared to sexual reproduction, where 50% of offspring are males and unable to produce offspring themselves. In hermaphroditic reproduction, each of the two parent organisms required for the formation of a [[zygote]] can provide either the male or the female gamete, which leads to advantages in both size and genetic variance of a population.

Sexual reproduction therefore must offer significant [[fitness (biology)|fitness]] advantages because, despite the two-fold cost of sex (see below), it dominates among multicellular forms of life, implying that the fitness of offspring produced by sexual processes outweighs the costs. Sexual reproduction derives from [[genetic recombination|recombination]], where parent genotypes are reorganised and shared with the offspring. This stands in contrast to single-parent asexual [[Self-replication|replication]], where the offspring is always identical to the parents (barring mutation). Recombination supplies two [[fault-tolerance]] mechanisms at the molecular level: ''recombinational [[DNA repair]]'' (promoted during [[meiosis]] because [[homologous chromosome]]s pair at that time) and ''[[Complementation (genetics)|complementation]]'' (also known as [[heterosis]], hybrid vigour or masking of mutations).

==Historical perspective==
Reproduction, including modes of sexual reproduction, features in the writings of [[Aristotle]]; modern philosophical-scientific thinking on the problem dates from at least [[Erasmus Darwin]] (1731–1802) in the 18th century.<ref>{{cite book |last1=Darwin |first1=Erasmus |title=Phytologia … |date=1800 |publisher=P. Byrne |location=Dublin, Ireland |page=104 |url=https://books.google.com/books?id=YggpAAAAYAAJ&pg=PA104}}  From p. 104:   "As the progeny by lateral generation [i.e., vegetative (asexual) reproduction] so exactly resembles the parent stock, it follows, that though any new variety, or improvement, may be thus continued for a century or two, as in grafted  fruit-trees, yet that no new variety or improvements can be obtained by this mode of generation; … "  "But from the sexual, or amatorial, generation of plants new varieties, or improvements, are frequently obtained; as many of the young plants from seeds are dissimilar to the parent, and some of them supererior to the parent in the qualities we wish to possess; … " " … another advantage occurs from sexual generation, which is the production of new species of plants, or mules, … "</ref> [[August Weismann]] picked up the thread in 1885, arguing that sex serves to generate [[genetic variation]], as detailed in the majority of the explanations below.<ref>English translation: 
 {{cite book |last1=Weismann |first1=August |editor1-last=Poulton |editor1-first=Edward B. |editor2-last=Schönland |editor2-first=Selmar |editor3-last=Shipley |editor3-first=Arthur E. |title=Essays Upon Heredity and Kindred Biological Problems |date=1889 |publisher=Clarendon Press |location=Oxford, England |pages=252–332 |url=https://books.google.com/books?id=iGysxQEACAAJ&pg=PA252}}  Ch. 5:  The Significance of Sexual Reproduction in the Theory of Natural Selection (1886)
* Weismann, Aug. (1885) [https://www.biodiversitylibrary.org/item/182986#page/42/mode/1up "Die Bedeutung der sexuellen Fortpflanzung für die Selektions-Theorie"] [The significance of sexual reproduction in the theory of natural selection] Stilling, J. (ed.) ''Tageblatt der 58. Versammlung Deutscher Naturforscher und Aerzte in Strassburg'' [Daily News of the 58th Conference of German Natural Scientists and Physicians in Strassburg] (in German) Strassburg, Germany:  G. Fischbach pp. 42-56.
* Revised and expanded in:  {{cite book |last1=Weismann |first1=August |title=Die Bedeutung der sexuellen Fortpflanzung für die Selektions-Theorie |date=1886 |publisher=Gustav Fischer |location=Jena, Germany |url=https://www.biodiversitylibrary.org/item/18057#page/5/mode/1up |language=German}}</ref> On the other hand, [[Charles Darwin]] (1809–1882) concluded that the effect of [[Heterosis|hybrid vigor]] (complementation) "is amply sufficient to account for the … genesis of the two sexes".<ref>{{cite book |last1=Darwin |first1=Charles |title=The Effects of Cross and Self Fertilisation in the Vegetable Kingdom |date=1876 |publisher=John Murray |location=London, England |page=462 |url=https://www.biodiversitylibrary.org/item/194109#page/478/mode/1up}}</ref> This is consistent with the repair and complementation hypothesis, described below. Since the emergence of the [[modern evolutionary synthesis]] in the 20th century, numerous biologists including [[W. D. Hamilton]], [[Alexey Kondrashov]], [[George C. Williams (biologist)|George C. Williams]], Harris Bernstein, Carol Bernstein, Michael M. Cox, Frederic A. Hopf and Richard E. Michod – have suggested competing explanations for how a vast array of different living species maintain sexual reproduction.

==Advantages of sex and sexual reproduction==
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The concept of sex includes two fundamental phenomena: the sexual process (fusion of genetic information of two individuals) and sexual differentiation (separation of this information into two parts). Depending on the presence or absence of these phenomena, all of the existing forms of reproduction can be classified as asexual, hermaphrodite or dioecious. The sexual process and sexual differentiation are different phenomena, and, in essence, are diametrically opposed. The first creates (increases) diversity of genotypes, and the second decreases it by half.

Reproductive advantages of the asexual forms are in quantity of the progeny, and the advantages of the hermaphrodite forms are in maximal diversity. Transition from the hermaphrodite to dioecious state leads to a loss of at least half of the diversity. So, the primary challenge is to explain the advantages given by sexual differentiation, i.e. the benefits of two separate sexes compared to hermaphrodites rather than to explain benefits of sexual forms (hermaphrodite + dioecious) over asexual ones. It has already been understood that since sexual reproduction is not associated with any clear reproductive advantages over asexual reproduction, there should be some important advantages in evolution.<ref>Crow J.F. (1994). Advantages of Sexual Reproduction, Dev. Gen., vol.15, pp. 205-213.</ref>{{Better source needed|date=August 2021|reason=Does the information in this source still hold up?}}

===Advantages due to genetic variation, DNA repair and genetic complementation===
{{more citations needed|section|date=April 2023}}{{See also|Hill–Robertson effect}}
For the advantage due to genetic variation, there are three possible reasons this might happen. First, sexual reproduction can combine the effects of two beneficial [[mutation]]s in the same individual (i.e. sex aids in the spread of advantageous traits) without the mutations having to have occurred one after another in a single line of descendants.<ref>
{{cite book
 |last=Goldstein
 |first=R N
 |year=2010
 |title=36 Arguments for the Existence of God: A Work of Fiction
 |publisher=[[Pantheon Books|Pantheon]]
 |isbn=978-0-307-37818-7
 |url=https://archive.org/details/36argumentsforex00gold
 }}</ref>{{unreliable source?|date=April 2012}} Second, sex acts to bring together currently deleterious mutations to create severely unfit individuals that are then eliminated from the population (i.e. sex aids in the removal of deleterious genes). However, in organisms containing only one set of chromosomes, deleterious mutations would be eliminated immediately, and therefore removal of harmful mutations is an unlikely benefit for sexual reproduction. Lastly, sex creates new gene combinations that may be more fit than previously existing ones, or may simply lead to reduced competition among relatives.

For the advantage due to [[DNA repair]], there is an immediate large benefit of removing DNA damage by recombinational DNA repair during [[meiosis]] (assuming the initial mutation rate is higher than optimal<ref>{{Cite journal |title=NCBI |date=2008 |pmc=2253642 |last1=Baer |first1=C. F. |journal=PLOS Biology |volume=6 |issue=2 |pages=e52 |doi=10.1371/journal.pbio.0060052 |doi-access=free |pmid=18303954 }}</ref>), since this removal allows greater survival of progeny with undamaged DNA. The advantage of [[Complementation (genetics)|complementation]] to each sexual partner is avoidance of the bad effects of their deleterious recessive genes in progeny by the masking effect of normal dominant genes contributed by the other partner.<ref name="Bernstein1985">Bernstein H, Byerly HC, Hopf FA, Michod RE (September 1985). "Genetic damage, mutation, and the evolution of sex". Science. 229 (4719): 1277–81 doi:10.1126/science.3898363. PMID 3898363</ref><ref name="Bernstein1986">Bernstein H, Hopf FA, Michod RE (1987). "The molecular basis of the evolution of sex". Adv Genet. 24: 323–70. doi:10.1016/s0065-2660(08)60012-7. PMID 3324702</ref>

The classes of hypotheses based on the creation of variation are further broken down below. Any number of these hypotheses may be true in any given species (they are not [[mutually exclusive events|mutually exclusive]]), and different hypotheses may apply in different species. However, a research framework based on creation of variation has yet to be found that allows one to determine whether the reason for sex is universal for all sexual species, and, if not, which mechanisms are acting in each species.

On the other hand, the maintenance of sex based on DNA repair and complementation applies widely to all sexual species.

===Protection from major genetic mutation===
In contrast to the view that sex promotes genetic variation, Heng,<ref>{{cite journal | author = Heng HH | year = 2007 | title = Elimination of altered karyotypes by sexual reproduction preserves species identity | journal = Genome | volume = 50 | issue = 5| pages = 517–524 | pmid = 17612621 | doi=10.1139/g07-039 | first2 = Henry H.Q.| last2 = Heng }}</ref> and Gorelick and Heng<ref name = Gorelick2011>{{cite journal | author = Gorelick R, Heng HH | year = 2011 | title = Sex reduces genetic variation: a multidisciplinary review | journal = Evolution | volume = 65 | issue = 4| pages = 1088–1098 | doi = 10.1111/j.1558-5646.2010.01173.x | pmid = 21091466 | last2 = Heng | doi-access =  | s2cid = 7714974 }}</ref> reviewed evidence that sex actually acts as a constraint on genetic variation. They consider that sex acts as a coarse filter, weeding out major genetic changes, such as chromosomal rearrangements, but permitting minor variation, such as changes at the nucleotide or gene level (that are often neutral) to pass through the sexual sieve.

===Novel genotypes===
{{more citations needed|section|date=April 2023}}

[[File:Evolsex-dia2a.svg|thumb|250px|This diagram illustrates how sex might create novel genotypes more rapidly. Two advantageous alleles ''A'' and ''B'' occur at random. The two alleles are recombined rapidly in a sexual population (top), but in an asexual population (bottom) the two alleles must independently arise because of [[clonal interference]].]]

Sex could be a method by which novel genotypes are created. Because sex combines genes from two individuals, sexually reproducing populations can more easily combine advantageous genes than can asexual populations. If, in a sexual population, two different advantageous [[alleles]] arise at different loci on a chromosome in different members of the population, a chromosome containing the two advantageous alleles can be produced within a few generations by [[Genetic recombination|recombination]]. However, should the same two alleles arise in different members of an asexual population, the only way that one chromosome can develop the other allele is to independently gain the same mutation, which would take much longer. Several studies have addressed counterarguments, and the question of whether this model is sufficiently robust to explain the predominance of sexual versus asexual reproduction remains.<ref name="Birdsell"/>{{rp|73–86}}<!--this is a scientific review of multiple theories, i.e. a high-quality source--><ref name = Gorelick2011/><ref>Gorelick R, Viillablanca, FX. Meiosis decreases recombination load: Mitosis increases recombination load. Ideas in Ecology and Evolution 11:19-28, 2018   doi:10.4033/iee.2018.11.3.n</ref>

[[Ronald Fisher]] suggested that sex might facilitate the spread of advantageous genes by allowing them to better escape their genetic surroundings, if they should arise on a chromosome with deleterious genes.

Supporters of these theories respond to the balance argument that the individuals produced by sexual and asexual reproduction may differ in other respects too – which may influence the persistence of sexuality. For example, in the [[Asexual reproduction#Alternation between sexual and asexual reproduction|heterogamous]] [[water flea]]s of the genus ''Cladocera'', sexual offspring form eggs which are better able to survive the winter versus those the fleas produce asexually.

===Increased resistance to parasites===
One of the most widely discussed theories to explain the persistence of sex is that it is maintained to assist sexual individuals in resisting [[parasite]]s, also known as the [[Red Queen Hypothesis]].<ref name="ridley">[[Matt Ridley]] 1995 ''The Red Queen: Sex and the Evolution of Human Nature'' 1995 Penguin.</ref><ref name=Birdsell>{{cite book | last1 = Birdsell | first1 = JA | last2 = Wills | first2 = C | title = Evolutionary Biology | chapter = The Evolutionary Origin and Maintenance of Sexual Recombination: A Review of Contemporary Models | year = 2003 | doi = 10.1007/978-1-4757-5190-1_2 | volume = 33 | pages = 27–137 | isbn = 978-1-4419-3385-0 }}</ref>{{rp|113–117}}<ref>MacIntyre, Ross J.; Clegg, Michael, T (Eds.), Springer. Hardcover {{ISBN|978-0306472619}}, {{ISBN|0306472619}} Softcover {{ISBN|978-1-4419-3385-0}}.</ref><ref name="red">{{cite journal | last1 = Van Valen | first1 = L. | year = 1973 | title = A New Evolutionary Law | journal = Evolutionary Theory | volume = 1 | pages = 1–30 }}</ref><ref name="parasite">{{cite journal | doi = 10.1073/pnas.87.9.3566 | last1 = Hamilton | first1 = W. D. | author-link = W. D. Hamilton | year = 1990 | title = Sexual reproduction as an adaptation to resist parasites |journal= [[Proceedings of the National Academy of Sciences]] | volume = 87 | issue = 9| pages = 3566–3573 | last2 = Axelrod | first2 = R. | last3 = Tanese | first3 = R. | pmid=2185476 | pmc=53943 | bibcode = 1990PNAS...87.3566H| doi-access = free }}</ref>

When an environment changes, previously neutral or deleterious alleles can become favourable. If the environment changed sufficiently rapidly (i.e. between generations), these changes in the environment can make sex advantageous for the individual. Such rapid changes in environment are caused by the co-evolution between hosts and parasites.

Imagine, for example that there is one gene in parasites with two alleles ''p'' and ''P'' conferring two types of parasitic ability, and one gene in hosts with two alleles ''h'' and ''H'', conferring two types of parasite resistance, such that parasites with allele ''p'' can attach themselves to hosts with the allele ''h'', and ''P'' to ''H''. Such a situation will lead to cyclic changes in allele frequency – as ''p'' increases in frequency, ''h'' will be disfavoured.

In reality, there will be several genes involved in the relationship between hosts and parasites. In an asexual population of hosts, offspring will only have the different parasitic resistance if a mutation arises. In a sexual population of hosts, however, offspring will have a new combination of parasitic resistance alleles.

In other words, like [[Lewis Carroll]]'s Red Queen, sexual hosts are continually "running" (adapting) to "stay in one place" (resist parasites).

Evidence for this explanation for the evolution of sex is provided by comparison of the rate of [[molecular evolution]] of genes for [[kinase]]s and [[immunoglobulin]]s in the [[immune system]] with genes coding other [[protein]]s. The genes coding for immune system proteins evolve considerably faster.<ref name="kuma">{{cite journal | last1 = Kuma | first1 = K. | last2 = Iwabe | first2 = N. | last3 = Miyata | first3 = T. | year = 1995 | title = Functional constraints against variations on molecules from the tissue-level - slowly evolving brain-specific genes demonstrated by protein-kinase and immunoglobulin supergene families | journal = Molecular Biology and Evolution | volume = 12 | issue = 1| pages = 123–130 | pmid = 7877487 | doi = 10.1093/oxfordjournals.molbev.a040181 | doi-access = free }}</ref><ref name="wolfe">{{cite journal | author = Wolfe KH, Sharp PM | year = 1993 | title = Mammalian gene evolution - nucleotide-sequence divergence between mouse and rat | journal = Journal of Molecular Evolution | volume = 37 | issue = 4| pages = 441–456 | doi = 10.1007/BF00178874 | pmid = 8308912 | last2 = Sharp | bibcode = 1993JMolE..37..441W | s2cid = 10437152 }}</ref>

Further evidence for the Red Queen hypothesis was provided by observing long-term dynamics and parasite coevolution in a "mixed" (sexual and asexual) population of snails (''[[Potamopyrgus antipodarum]]''). The number of sexuals, the number asexuals, and the rates of parasite infection for both were monitored. It was found that clones that were plentiful at the beginning of the study became more susceptible to parasites over time. As parasite infections increased, the once plentiful clones dwindled dramatically in number. Some clonal types disappeared entirely. Meanwhile, sexual snail populations remained much more stable over time.<ref>{{cite journal | doi = 10.1086/599080 | last1 = Jokela | first1 = Jukka | last2 = Dybdahl | first2 = Mark | last3 = Lively | first3 = Curtis | year = 2009 | title = The Maintenance of Sex, Clonal Dynamics, and Host-Parasite Coevolution in a Mixed Population of Sexual and Asexual Snails | jstor = 10.1086/599080| journal = The American Naturalist | volume = 174 | issue = s1 | pages = S43–53 | pmid=19441961| s2cid = 6797643 | url = https://www.dora.lib4ri.ch/eawag/islandora/object/eawag%3A6224/datastream/PDF/view }}</ref><ref>{{cite web | url = https://www.sciencedaily.com/releases/2009/07/090706171542.htm | title = Parasites May Have Had Role In Evolution Of Sex | date = 31 July 2009 | publisher = Science Daily | access-date= 19 September 2011}}</ref>

However, Hanley et al.<ref>{{cite journal |author1=Hanley KA |author2=Fisher RN |author3=Case TJ | year = 1995 | title = Lower mite infestations in an asexual gecko compared with its sexual ancestors | journal = Evolution | volume = 49 | issue = 3| pages = 418–426 | jstor=2410266 | doi = 10.2307/2410266|pmid=28565091 }}</ref> studied mite infestations of a [[parthenogenesis|parthenogenetic]] gecko species and its two related sexual ancestral species. Contrary to expectation based on the [[Red Queen hypothesis]], they found that the prevalence, abundance and mean intensity of mites in sexual geckos was significantly higher than in asexuals sharing the same habitat.

In 2011, researchers used the microscopic roundworm ''[[Caenorhabditis elegans]]'' as a host and the pathogenic bacteria ''[[Serratia marcescens]]'' to generate a host-parasite coevolutionary system in a controlled environment, allowing them to conduct more than 70 evolution experiments testing the Red Queen Hypothesis. They genetically manipulated the [[mating system]] of ''C. elegans'', causing populations to mate either sexually, by self-fertilization, or a mixture of both within the same population. Then they exposed those populations to the ''S. marcescens'' parasite. It was found that the self-fertilizing populations of ''C. elegans'' were rapidly driven extinct by the coevolving parasites while sex allowed populations to keep pace with their parasites, a result consistent with the Red Queen Hypothesis.<ref>{{cite journal | doi = 10.1126/science.1206360 | last1 = Morran | first1 = Levi T. | last2 = Schmidt | first2 = Olivia G. | last3 = Gelarden | first3 = Ian A. | last4 = Parrish Rc | first4 = Raymond C. | last5 = Lively | first5 = Curtis M. | year = 2011 | title = Running with the Red Queen: Host-Parasite Coevolution Selects for Biparental Sex | journal = Science | volume = 333 | issue = 6039 | pages = 216–218 | pmid = 21737739 | pmc = 3402160| bibcode = 2011Sci...333..216M }}</ref><ref>{{cite web | url = https://www.sciencedaily.com/releases/2011/07/110707141158.htm | title = Sex -- As We Know It -- Works Thanks to Ever-Evolving Host-Parasite Relationships, Biologists Find | date = 9 July 2011 | publisher = Science Daily | access-date=19 September 2011}}</ref> In natural populations of ''[[Caenorhabditis elegans|C. elegans]]'', self-fertilization is the predominant mode of reproduction, but infrequent out-crossing events occur at a rate of about 1%.<ref name="pmid16005289">{{cite journal |vauthors=Barrière A, Félix MA |title=High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations |journal=Curr. Biol. |volume=15 |issue=13 |pages=1176–84 |date=July 2005 |pmid=16005289 |doi=10.1016/j.cub.2005.06.022 |arxiv=q-bio/0508003 |bibcode=2005CBio...15.1176B |s2cid=2229622 }}</ref>

Critics of the Red Queen hypothesis question whether the constantly changing environment of hosts and parasites is sufficiently common to explain the evolution of sex. In particular, Otto and Nuismer <ref>{{cite journal | author = Otto SP, Nuismer SL | year = 2004 | title = Species interactions and the evolution of sex |journal=Science |volume=304 |issue=5673 |pages = 1018–1020 | pmid = 15143283 | doi=10.1126/science.1094072| last2 = Nuismer | bibcode = 2004Sci...304.1018O | s2cid = 8599387 }}</ref> presented results showing that species interactions (e.g. host vs parasite interactions) typically select against sex. They concluded that, although the Red Queen hypothesis favors sex under certain circumstances, it alone does not account for the ubiquity of sex. Otto and Gerstein <ref>{{cite journal | pmid = 16856849 | doi=10.1042/BST0340519 |volume=34 |issue=Pt 4 |title=Why have sex? The population genetics of sex and recombination |date=August 2006 | pages=519–22 | author=Otto SP, Gerstein AC |journal=Biochemical Society Transactions |last2=Gerstein}}</ref> further stated that "it seems doubtful to us that strong selection per gene is sufficiently commonplace for the Red Queen hypothesis to explain the ubiquity of sex". Parker<ref>{{cite journal | author = Parker MA | year = 1994 | title = Pathogens and sex in plants | journal = Evolutionary Ecology | volume = 8 | issue = 5| pages = 560–584 | doi = 10.1007/BF01238258| bibcode = 1994EvEco...8..560P | s2cid = 31756267 }}</ref> reviewed numerous genetic studies on plant disease resistance and failed to uncover a single example consistent with the assumptions of the Red Queen hypothesis.

==Disadvantages of sex and sexual reproduction==
The paradox of the existence of sexual reproduction is that though it is ubiquitous in multicellular organisms, there are ostensibly many inherent disadvantages to reproducing sexually when weighed against the relative advantages of alternative forms of reproduction, such as asexual reproduction. Thus, because sexual reproduction abounds in complex multicellular life, there must be some significant benefit(s) to sex and sexual reproduction that compensates for these fundamental disadvantages.

==={{anchor|Two-fold cost}}{{anchor|xspeed}}Population expansion cost of sex===
Among the most limiting disadvantages to the evolution of sexual reproduction by natural selection is that an asexual population can grow much more rapidly than a sexual one with each generation.

For example, assume that the entire population of a theoretical species has 100 total organisms consisting of two sexes (i.e. males and females), with 50:50 male-to-female representation, and that only the females of this species can bear offspring. If all capable members of this population procreated once, a total of 50 offspring would be produced (the ''F<sub>1</sub>'' generation). Contrast this outcome with an asexual species, in which each and every member of an equally sized 100-organism population is capable of bearing young. If all capable members of this asexual population procreated once, a total of 100 offspring would be produced – twice as many as produced by the sexual population in a single generation.

[[File:Evolsex-dia1a.svg|thumb|250px|This diagram illustrates the ''two-fold cost of sex''. If each individual were to contribute to the same number of offspring (two), ''(a)'' the sexual population remains the same size each generation, where the ''(b)'' asexual population doubles in size each generation.]]
This idea is sometimes referred to as the '''two-fold cost''' of sexual reproduction. It was first described mathematically by [[John Maynard Smith]].<ref name="maynard">{{cite book|author-link=John Maynard Smith|first = J. Maynard|last = Smith|title =The Evolution of Sex|date= 1978|publisher = Cambridge University Press|url =https://archive.org/details/evolutionofsex0000mayn|url-access=registration|isbn = 9780521293020}}</ref>{{Page needed|date=August 2021}} In his manuscript, Smith further speculated on the impact of an asexual mutant arising in a sexual population, which suppresses [[meiosis]] and allows eggs to develop into offspring genetically identical to the mother by mitotic division.<ref name="1946- 2005">{{Cite book|title=Evolution : an introduction|last=Stearns|first=S. C.|date=2005|publisher=Oxford University Press|others=Hoekstra, Rolf F.|isbn=978-0199255634|edition= 2nd|location=Oxford [England]|oclc=56964580}}</ref>{{Page needed|date=August 2021}} The mutant-asexual lineage would double its representation in the population each generation, all else being equal.

Technically the problem above is not one of sexual reproduction but of having a subset of organisms incapable of bearing offspring. Indeed, some multicellular organisms ([[isogamy|isogamous]]) engage in sexual reproduction but all members of the species are capable of bearing offspring.<ref name="Hoekstra">{{cite book|author-link=Rolf Hoekstra|first=Rolf F.|last = Hoekstra|date= 1987|title= The Evolution of Sex and its Consequences|publisher=Springer Basel AG|editor-first=Stephen C.|editor-last=Stearns|chapter = The Evolution of Sexes|chapter-url = https://books.google.com/books?id=1cQACAAAQBAJ&pg=PA59|isbn = 9783034862738}}</ref>{{Page needed|date=August 2021}} The two-fold reproductive disadvantage assumes that males contribute only genes to their offspring and sexual females spend half their reproductive potential on sons.<ref name="1946- 2005"/>{{Page needed|date=August 2021}} Thus, in this formulation, the principal cost of sex is that males and females must successfully [[copulation (zoology)|copulate]], which almost always involves expending energy to come together through time and space. Asexual organisms need not expend the energy necessary to find a mate.

===Selfish cytoplasmic genes===
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| date = August 2021
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Sexual reproduction implies that chromosomes and alleles segregate and recombine in every generation, but not all genes are transmitted together to the offspring.<ref name="1946- 2005" />{{Page needed|date=August 2021}} There is a chance of spreading mutants that cause unfair transmission at the expense of their non-mutant colleagues. These mutations are referred to as "selfish" because they promote their own spread at the cost of alternative alleles or of the host organism; they include nuclear meiotic drivers and selfish cytoplasmic genes.<ref name="1946- 2005" />{{Page needed|date=August 2021}} [[Meiotic drive]]rs are genes that distort meiosis to produce gametes containing themselves more than the 50% of the time expected by chance. A selfish cytoplasmic gene is a gene located in an organelle, plasmid or intracellular parasite that modifies reproduction to cause its own increase at the expense of the cell or organism that carries it.<ref name="1946- 2005" />{{Page needed|date=August 2021}}

===Genetic heritability cost of sex===
A sexually reproducing organism only passes on ~50% of its own genetic material to each L2 offspring. This is a consequence of the fact that gametes from sexually reproducing species are [[haploid]]. Again, however, this is not applicable to all sexual organisms. There are numerous species which are sexual but do not have a genetic-loss problem because they do not produce males or females. Yeast, for example, are [[isogamy|isogamous]] sexual organisms which have two [[mating type]]s which fuse and recombine their haploid genomes. Both sexes reproduce during the haploid and diploid stages of their life cycle and have a 100% chance of passing their genes into their offspring.<ref name="Hoekstra" />{{Page needed|date=August 2021}}

Some species avoid the 50% cost of sexual reproduction, although they have "sex" (in the sense of [[genetic recombination]]). In these species (e.g., [[bacteria]], [[ciliates]], [[dinoflagellate]]s and [[diatom]]s), "sex" and reproduction occur separately.<ref name="Ridley M 2004 p. 314"/><ref>Beukeboom, L. & Perrin, N. (2014). ''The Evolution of Sex Determination''. Oxford University Press, p. 5–6 [https://books.google.com/books?id=d4cLBAAAQBAJ&pg=PA5]. Online resources, [http://www.oup.co.uk/companion/beukeboom].</ref>

==DNA repair and complementation==
As discussed in the earlier part of this article, sexual reproduction is conventionally explained as an adaptation for producing genetic variation through allelic recombination. As acknowledged above, however, serious problems with this explanation have led many biologists to conclude that the benefit of sex is a major unsolved problem in evolutionary biology.

An alternative "[[information theory|informational]]" approach to this problem has led to the view that the two fundamental aspects of sex, [[genetic recombination]] and [[outcrossing]], are adaptive responses to the two major sources of "noise" in transmitting genetic information. Genetic noise can occur as either physical damage to the genome (e.g. chemically altered bases of DNA or breaks in the chromosome) or replication errors (mutations).<ref name="dna-repair">{{cite journal |author1=Bernstein H |author2=Byerly HC |author3=Hopf FA |author4=Michod RE |title=Origin of sex |journal=J. Theor. Biol. |volume=110 |issue=3 |pages=323–51 |year=1984 |pmid=6209512 |doi=10.1016/S0022-5193(84)80178-2|bibcode=1984JThBi.110..323B }}</ref><ref name = Bernstein1985>Bernstein H, Byerly HC, Hopf FA, Michod RE (September 1985). "Genetic damage, mutation, and the evolution of sex". Science. 229 (4719): 1277–81 doi:10.1126/science.3898363. PMID 3898363</ref><ref name = Bernstein1986>Bernstein H, Hopf FA, Michod RE (1987). "The molecular basis of the evolution of sex". Adv Genet. 24: 323–70. doi:10.1016/s0065-2660(08)60012-7. PMID 3324702</ref> This alternative view is referred to as the repair and complementation hypothesis, to distinguish it from the traditional variation hypothesis.

The repair and complementation hypothesis assumes that [[genetic recombination]] is fundamentally a DNA repair process, and that when it occurs during [[meiosis]] it is an adaptation for repairing the genomic DNA which is passed on to progeny. Recombinational repair is the only repair process known which can accurately remove double-strand damages in DNA, and such damages are both common in nature and ordinarily lethal if not repaired. For instance, double-strand breaks in DNA occur about 50 times per cell cycle in human cells (see [[DNA damage (naturally occurring)|naturally occurring DNA damage]]). Recombinational repair is prevalent from the simplest viruses to the most complex multicellular eukaryotes. It is effective against many different types of genomic damage, and in particular is highly efficient at overcoming double-strand damages. Studies of the mechanism of meiotic recombination indicate that meiosis is an adaptation for repairing DNA.<ref name="replication-help">{{cite journal |author1=Cox MM |title=Historical overview: searching for replication help in all of the rec places |journal=Proc. Natl. Acad. Sci. U.S.A. |volume=98 |issue=15 |pages=8173–80 |year=2001 |pmid=11459950 |doi=10.1073/pnas.131004998 |pmc=37418|bibcode=2001PNAS...98.8173C |doi-access=free }}</ref>  These considerations form the basis for the first part of the repair and complementation hypothesis.

In some lines of descent from the earliest organisms, the [[Ploidy|diploid]] stage of the sexual cycle, which was at first transient, became the predominant stage, because it allowed [[Complementation (genetics)|complementation]] — the masking of deleterious recessive mutations (i.e. [[Heterosis|hybrid vigor or heterosis]]). [[Outcrossing]], the second fundamental aspect of sex, is maintained by the advantage of masking mutations and the disadvantage of [[inbreeding]] (mating with a close relative) which allows expression of recessive mutations (commonly observed as [[inbreeding depression]]). This is in accord with [[Charles Darwin]],<ref>Darwin CR (1876). The effects of cross and self fertilisation in the vegetable kingdom. London: John Murray. [http://darwin-online.org.uk/converted/published/1881_Worms_F1357/1876_CrossandSelfFertilisation_F1249/1876_CrossandSelfFertilisation_F1249.html] {{Webarchive|url=https://web.archive.org/web/20160219083546/http://darwin-online.org.uk/converted/published/1881_Worms_F1357/1876_CrossandSelfFertilisation_F1249/1876_CrossandSelfFertilisation_F1249.html|date=19 February 2016}} see page 462</ref> who concluded that the adaptive advantage of sex is hybrid vigor; or as he put it, "the offspring of two individuals, especially if their progenitors have been subjected to very different conditions, have a great advantage in height, weight, constitutional vigor and fertility over the self fertilised offspring from either one of the same parents."

However, outcrossing may be abandoned in favor of parthenogenesis or selfing (which retain the advantage of meiotic recombinational repair) under conditions in which the costs of mating are very high. For instance, costs of mating are high when individuals are rare in a geographic area, such as when there has been a forest fire and the individuals entering the burned area are the initial ones to arrive. At such times mates are hard to find, and this favors parthenogenic species.

In the view of the repair and complementation hypothesis, the removal of DNA damage by recombinational repair produces a new, less deleterious form of informational noise, allelic recombination, as a by-product. This lesser informational noise generates genetic variation, viewed by some as the major effect of sex, as discussed in the earlier parts of this article.

==Deleterious mutation clearance==
[[Mutation]]s can have many different effects upon an organism. It is generally believed that the majority of non-neutral mutations are deleterious, which means that they will cause a decrease in the organism's overall fitness.<ref name="Griffiths">Griffiths ''et al.'' 1999. Gene mutations, p197-234, ''in'' Modern Genetic Analysis, New York, W.H. Freeman and Company.</ref>{{Page range too broad|date=August 2021}} If a mutation has a deleterious effect, it will then usually be removed from the population by the process of [[natural selection]]. Sexual reproduction is believed to be more efficient than asexual reproduction in removing those mutations from the genome.<ref name="kondrashov">{{cite journal | doi = 10.1038/336435a0 | last1 = Kondrashov | first1 = A. S. | author-link = Alexey Kondrashov | year = 1988| title = Deleterious mutations and the evolution of sexual reproduction | journal = [[Nature (journal)|Nature]] | volume = 336 | issue = 6198| pages = 435–440 | pmid=3057385| bibcode = 1988Natur.336..435K | s2cid = 4233528 }}</ref>

There are two main hypotheses which explain how sex may act to remove deleterious [[gene]]s from the genome.

===Evading harmful mutation build-up===
{{Main|Muller's ratchet}}
While [[DNA]] is able to recombine to modify [[alleles]], DNA is also susceptible to mutations within the sequence that can affect an organism in a negative manner. Asexual organisms do not have the ability to recombine their genetic information to form new and differing alleles. Once a [[mutation]] occurs in the DNA or other genetic carrying sequence, there is no way for the mutation to be removed from the population until another mutation occurs that ultimately deletes the primary mutation. This is rare among organisms.

[[Hermann Joseph Muller]] introduced the idea that mutations build up in asexual reproducing organisms. Muller described this occurrence by comparing the mutations that accumulate as a [[Muller's ratchet|ratchet]]. Each mutation that arises in asexually reproducing organisms turns the ratchet once. The ratchet is unable to be rotated backwards, only forwards. The next mutation that occurs turns the ratchet once more. Additional mutations in a population continually turn the ratchet and the mutations, mostly deleterious, continually accumulate without recombination.<ref>{{cite journal | last1 = Muller | first1 = H.J. | year = 1964 | title = The Relation of Recombination to Mutational Advance | journal = Mutation Research | volume = 1 | issue = 1 | pages = 2–9 | doi=10.1016/0027-5107(64)90047-8| pmid = 14195748 | bibcode = 1964MRFMM...1....2M }}</ref> These mutations are passed onto the next generation because the offspring are exact genetic [[cloning|clones]] of their parents. The genetic load of organisms and their populations will increase due to the addition of multiple deleterious mutations and decrease the overall reproductive success and fitness.

For sexually reproducing populations, studies have shown that single-celled bottlenecks are beneficial for resisting mutation build-up{{Citation needed|date=January 2022}}. Passaging a population through a single-celled bottleneck involves the fertilization event occurring with [[haploid]] sets of DNA, forming one fertilized cell. For example, humans undergo a single-celled bottleneck in that the haploid sperm fertilizes the haploid egg, forming the diploid [[zygote]], which is unicellular. This passage through a single cell is beneficial in that it lowers the chance of mutations from being passed on through multiple individuals. Instead, the mutation is only passed onto one individual.<ref>{{Cite journal|last=Niklas|first=Karl J.|date=2014-01-01|title=The evolutionary-developmental origins of multicellularity|journal=American Journal of Botany|language=en|volume=101|issue=1|pages=6–25|doi=10.3732/ajb.1300314|issn=0002-9122|pmid=24363320}}</ref> Further studies using ''[[Dictyostelium discoideum]]'' suggest that this unicellular initial stage is important for resisting mutations due to the importance of high relatedness. Highly related individuals are more closely related, and more clonal, whereas less related individuals are less so, increasing the likelihood that an individual in a population of low relatedness may have a detrimental mutation. Highly related populations also tend to thrive better than lowly related because the cost of sacrificing an individual is greatly offset by the benefit gained by its relatives and in turn, its genes, according to [[kin selection]]. The studies with ''D. discoideum'' showed that conditions of high relatedness resisted mutant individuals more effectively than those of low relatedness, suggesting the importance of high relatedness to resist mutations from proliferating.<ref>{{Cite journal|last1=Kuzdzal-Fick|first1=Jennie J.|last2=Fox|first2=Sara A.|last3=Strassmann|first3=Joan E.|last4=Queller|first4=David C.|date=2011-12-16|title=High Relatedness Is Necessary and Sufficient to Maintain Multicellularity in Dictyostelium|journal=Science|language=en|volume=334|issue=6062|pages=1548–1551|doi=10.1126/science.1213272|issn=0036-8075|pmid=22174251|bibcode=2011Sci...334.1548K|s2cid=206537272}}</ref>

===Removal of deleterious genes===
[[File:Synergistic versus antagonistic epistasis.svg|thumb|200px|Diagram illustrating different relationships between numbers of mutations and fitness. Kondrashov's model requires ''synergistic epistasis'', which is represented by the red line<ref>Ridley M (2004) ''Evolution'', 3rd edition. Blackwell Publishing.</ref><ref>Charlesworth B, Charlesworth D (2010) ''Elements of Evolutionary Genetics''. Roberts and Company Publishers.</ref> – each subsequent mutation has a disproportionately large effect on the organism's fitness.]]
This hypothesis was proposed by [[Alexey Kondrashov]], and is sometimes known as the ''deterministic mutation hypothesis''.<ref name="kondrashov"/> It assumes that the majority of deleterious mutations are only slightly deleterious, and affect the individual such that the introduction of each additional mutation has an increasingly large effect on the fitness of the organism. This relationship between number of mutations and fitness is known as [[epistasis|''synergistic epistasis'']].

By way of [[analogy]], think of a [[Automobile|car]] with several minor faults. Each is not sufficient alone to prevent the car from running, but in combination, the faults combine to prevent the car from functioning.

Similarly, an organism may be able to cope with a few defects, but the presence of many mutations could overwhelm its backup mechanisms.

Kondrashov argues that the slightly deleterious nature of mutations means that the population will tend to be composed of individuals with a small number of mutations. Sex will act to [[Genetic recombination|recombine]] these genotypes, creating some individuals with fewer deleterious mutations, and some with more. Because there is a major selective disadvantage to individuals with more mutations, these individuals die out. In essence, sex compartmentalises the deleterious mutations.

There has been much criticism of Kondrashov's theory, since it relies on two key restrictive conditions. The first requires that the rate of deleterious mutation should exceed one per genome per generation in order to provide a substantial advantage for sex. While there is some empirical evidence for it (for example in [[Drosophila]]<ref name="Drosophila">{{cite journal | last1 = Whitlock | first1 = M. C. | last2 = Bourguet | first2 = D. | year = 2000 | title = Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components | url = https://hal.archives-ouvertes.fr/hal-02914167/file/Whitlock%20and%20Bourguet%20Evolution%202000.pdf| journal = Evolution | volume = 54 | issue = 5| pages = 1654–1660 | pmid = 11108592 | doi=10.1554/0014-3820(2000)054[1654:fatgli]2.0.co;2| s2cid = 198153635 }}</ref> and [[E. coli]]<ref name="E. coli">{{cite journal | doi = 10.1038/37108 | last1 = Elena | first1 = S. F. | last2 = Lenski | first2 = R. E. | year = 1997 | title = Test of synergistic interactions among deleterious mutations in bacteria | journal = Nature | volume = 390 | issue = 6658| pages = 395–398 | pmid = 9389477 | bibcode = 1997Natur.390..395E | s2cid = 205025450 }}</ref>), there is also strong evidence against it. Thus, for instance, for the sexual species ''Saccharomyces cerevisiae'' (yeast) and ''Neurospora crassa'' (fungus), the mutation rate per genome per replication are 0.0027 and 0.0030 respectively. For the nematode worm ''Caenorhabditis elegans'', the mutation rate per effective genome per sexual generation is 0.036.<ref>{{cite journal | pmid = 9560386 | volume=148 | issue=4 | title=Rates of spontaneous mutation | pmc=1460098 |date=April 1998 | pages=1667–86 |author1=Drake JW |author2=Charlesworth B |author3=Charlesworth D |author4=Crow JF | journal = Genetics| doi=10.1093/genetics/148.4.1667 }}</ref> Secondly, there should be strong interactions among loci (synergistic epistasis), a mutation-fitness relation for which there is only limited evidence.<ref>{{cite journal | pmid = 28473589 | pmc=6200135 | title=Negative selection in humans and fruit flies involves synergistic epistasis | journal = Science | doi=10.1126/science.aah5238 | volume=356 | issue=6337 | pages=539–542 | last1 = Sohail | first1 = M | last2 = Vakhrusheva | first2 = OA | last3 = Sul | first3 = JH | last4 = Pulit | first4 = SL | last5 = Francioli | first5 = LC | last6 = van den Berg | first6 = LH | last7 = Veldink | first7 = JH | last8 = de Bakker | first8 = PIW | last9 = Bazykin | first9 = GA | last10 = Kondrashov | first10 = AS | last11 = Sunyaev | first11 = SR | year=2017| bibcode=2017Sci...356..539S }}</ref><ref>{{cite journal |last1=Matheson |first1=Joseph |last2=Masel |first2=Joanna |title=Background Selection From Unlinked Sites Causes Nonindependent Evolution of Deleterious Mutations |journal=Genome Biology and Evolution |date=2 March 2024 |volume=16 |issue=3 |pages=evae050 |doi=10.1093/gbe/evae050 |pmid=38482769 |language=en |issn=1759-6653|pmc=10972689 }}</ref> Conversely, there is also the same amount of evidence that mutations show no epistasis (purely additive model) or antagonistic interactions (each additional mutation has a disproportionally ''small'' effect).

==Other explanations==
===Geodakyan's evolutionary theory of sex===
Geodakyan suggested that sexual dimorphism provides a partitioning of a species' phenotypes into at least two functional partitions: a female partition that secures beneficial features of the species and a male partition that emerged in species with more variable and unpredictable environments. The male partition is suggested to be an "experimental" part of the species that allows the species to expand their ecological niche, and to have alternative configurations. This theory underlines the higher variability and higher mortality in males, in comparison to females. This functional partitioning also explains the higher susceptibility to disease in males, in comparison to females and therefore includes the idea of "protection against parasites" as another functionality of male sex. Geodakyan's evolutionary theory of sex was developed in Russia in 1960–1980 and was not known to the West till the era of the Internet. Trofimova, who analysed psychological sex differences, hypothesised that the male sex might also provide a "redundancy pruning" function.<ref name=Trofimova>{{cite journal|last1=Trofimova |first1=I.|year=2015| title= Do psychological sex differences reflect evolutionary bi-sexual partitioning? |journal =American Journal of Psychology|volume=128|issue=4 |pages=485–514|doi= 10.5406/amerjpsyc.128.4.0485| pmid=26721176}}</ref>

===Speed of evolution===
Ilan Eshel suggested that sex prevents rapid evolution. He suggests that [[Genetic recombination|recombination]] breaks up favourable gene combinations more often than it creates them, and sex is maintained because it ensures selection is longer-term than in asexual populations – so the population is less affected by short-term changes.<ref name=Birdsell />{{rp|85–86}}<ref>{{cite journal | pmid = 5527627 | volume=1 | issue=1 | title=On the evolutionary effect of recombination |date=May 1970 | pages=88–100 | author1=Eshel, I. | author2=Feldman, MW | journal = Theoretical Population Biology | doi=10.1016/0040-5809(70)90043-2 | bibcode=1970TPBio...1...88E }}</ref> This explanation is not widely accepted, as its assumptions are very restrictive.

It has recently been shown in experiments with ''[[Chlamydomonas]]'' algae that sex can remove the speed limit{{clarify|date=July 2013}} on evolution.<ref name="speed">{{cite journal | last1 = Colegrave | first1 = N. | year = 2002 | pmid = 12478292 | title = Sex releases the speed limit on evolution | doi = 10.1038/nature01191 | journal = Nature | volume = 420 | issue = 6916| pages = 664–666 | bibcode = 2002Natur.420..664C | hdl = 1842/692 | s2cid = 4382757 | hdl-access = free }}</ref>

An information theoretic analysis using a simplified but useful model shows that in asexual reproduction, the information gain per generation of a species is limited to 1 bit per generation, while in sexual reproduction, the information gain is bounded by {{nowrap|<math>\sqrt G</math>,}} where <math>G</math> is the size of the genome in bits.<ref>{{cite book | author=David MacKay | title=Information Theory, Inference, and Learning Algorithms | publisher=Cambridge University Press |location=Cambridge |date=2003 | pages=269–280 | url=http://www.inference.phy.cam.ac.uk/itprnn/book.pdf }}</ref>

===Libertine bubble theory===
The evolution of sex can alternatively be described as a kind of [[gene]] exchange that is independent from reproduction.<ref>{{cite journal | author = Lesbarrères D | year = 2011 | title = Sex or no sex, reproduction is not the question | journal = BioEssays | volume = 33 | issue = 11| page = 818 | doi = 10.1002/bies.201100105 | pmid = 22009640 | s2cid = 46112804 }}</ref> According to the [[Thierry Lodé]]'s "libertine bubble theory", sex originated from an archaic gene transfer process among [[Prebiotic (chemistry)|prebiotic]] bubbles.<ref name=sexisnot>{{cite journal | author = Lodé, T | year = 2011 | title = Sex is not a solution for reproduction: the libertine bubble theory | doi=10.1002/bies.201000125 | journal = BioEssays | volume = 33 | issue = 6| pages = 419–422 | pmid = 21472739 | doi-access = free }}</ref><ref>{{cite journal | author = Lodé, T | year = 2011 | title = The origin of sex was interaction, not reproduction (what's sex really all about), Big Idea | url = http://www.pagepress.org/journals/index.php/eb/article/view/eb.2012.e1 | journal = New Scientist | volume = 212 | issue = 2837| pages = 30–31 | doi = 10.1016/S0262-4079(11)62719-X }}</ref> The contact among the pre-biotic bubbles could, through simple food or parasitic reactions, promote the transfer of genetic material from one bubble to another. That interactions between two organisms be in balance appear to be a sufficient condition to make these interactions evolutionarily efficient, i.e. to select bubbles that tolerate these interactions ("libertine" bubbles) through a blind evolutionary process of self-reinforcing gene correlations and compatibility.<ref name="LODÉ T 2012">{{cite journal | author = Lodé, T | year = 2012 | title = Sex and the origin of genetic exchanges | journal = Trends Evol Biol | volume = 4 | page = e1 | doi = 10.4081/eb.2012.e1 | doi-access = free }}</ref>

The "libertine bubble theory" proposes that [[meiosis|meiotic]] sex evolved in proto-[[eukaryotes]] to solve a problem that bacteria did not have, namely a large amount of [[DNA]] material, occurring in an archaic step of [[proto-cell]] formation and genetic exchanges. So that, rather than providing selective advantages through reproduction, sex could be thought of as a series of separate events which combines step-by-step some very weak benefits of [[Genetic recombination|recombination]], meiosis, gametogenesis and [[syngamy]].<ref name="ReferenceA">{{cite journal | last1 = Lodé | first1 = T | year = 2012 | title = Have sex or not ? Lessons from bacteria | journal = Sexual Dev | volume = 6 | issue = 6| pages = 325–328 | doi=10.1159/000342879 | pmid=22986519| doi-access = free }}</ref> Therefore, current sexual species could be descendants of primitive organisms that practiced more stable exchanges in the long term, while asexual species have emerged, much more recently in evolutionary history, from the conflict of interest resulting from [[anisogamy]].{{clarify|reason=how?|date=December 2016}}

'''<big>Parasites and Muller's ratchet</big>'''

{{Unreferenced section|date=August 2021}}

R. Stephen Howard and [[Curtis Lively]] were the first to suggest that the combined effects of parasitism and [[mutation]] accumulation can lead to an increased advantage to sex under conditions not otherwise predicted (Nature, 1994).  Using computer simulations, they showed that when the two mechanisms act simultaneously the advantage to sex over [[asexual reproduction]] is larger than for either factor operating alone.

==Origin of sexual reproduction==
{{Life timeline}}
Many [[protist]]s reproduce sexually, as do many multicellular [[plant]]s, [[animal]]s, and [[fungi]]. In the eukaryotic fossil record, sexual reproduction first appeared about 2.0 billion years ago in the [[Proterozoic|Proterozoic Eon]],<ref name="NAT-2008">{{cite journal |last=Otto |first=Sarah P. |title=Sexual Reproduction and the Evolution of Sex |url=https://www.nature.com/scitable/topicpage/sexual-reproduction-and-the-evolution-of-sex-824/ |date=2008 |journal=[[Nature (journal)|Nature]] |accessdate=1 October 2021 }}</ref><ref name="SCI-20090605">{{cite journal |last=Zimmer |first=Carl |authorlink=Carl Zimmer |title=On The Origin Of Sexual Reproduction |url=https://www.science.org/lookup/doi/10.1126/science.324_1254 |date=5 June 2009 |journal=[[Science (journal)|Science]] |volume=324 |issue=5932 |pages=1254–1256 |doi=10.1126/science.324_1254 |pmid=19498143 |s2cid=39987391 |accessdate=1 October 2021 }}</ref> although a later date, 1.2 billion years ago, has also been presented.<ref name="PB-2000">{{cite journal |last=Butterfield |first=Nicholas J. |title=Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes |url=http://mr.crossref.org/iPage?doi=10.1666%2F0094-8373%282000%29026%3C0386%3ABPNGNS%3E2.0.CO%3B2 |date=2000 |journal=[[Paleobiology (journal)|Paleobiology]] |volume=26 |issue=3 |page=386 |doi=10.1666/0094-8373(2000)026<0386:BPNGNS>2.0.CO;2 |bibcode=2000Pbio...26..386B |s2cid=36648568 |accessdate=12 April 2021 }}</ref><ref name="BBC-20160704">{{cite news |last=Cumming |first=Vivian |title=The Real Reasons Why We Have Sex |url=http://www.bbc.com/earth/story/20160704-the-real-reasons-why-we-have-sex |date=4 July 2016 |work=[[BBC News]] |accessdate=12 April 2021 }}</ref> Nonetheless, all sexually reproducing [[eukaryotic]] organisms likely derive from a single-celled common ancestor.<ref name="Letunic I and Bork P"/><ref name=Bernstein2010>{{cite journal | author = Bernstein H, Bernstein C | year = 2010 | title = Evolutionary origin of recombination during meiosis | journal = BioScience | volume = 60 | issue = 7| pages = 498–505 | doi = 10.1525/bio.2010.60.7.5| s2cid = 86663600 }}</ref><ref name=sexisnot/> It is probable that the evolution of sex was an integral part of the evolution of the first eukaryotic cell.<ref name="Ploompuu1999">{{cite book |author=Ploompuu, T. |title=Biosüsteemide mälu teooria |journal=Schola Biotheoretica |publisher=Sulemees |year=1999 |isbn=978-9985908150 |volume=XXV |location=Tartu |pages=51–56 |language=et |trans-title=Why the eukaryotic cell memory was needed}} Abstract in English available online: [http://www.tlu.ee/~toenu/ingl/euk_rakk.htm]</ref><ref name="pmid29436502">{{cite journal |vauthors=Hörandl E, Speijer D |title=How oxygen gave rise to eukaryotic sex |journal=Proc. Biol. Sci. |volume=285 |issue=1872 |page= 20172706|date=February 2018 |pmid=29436502 |doi=10.1098/rspb.2017.2706 |pmc=5829205}}</ref>  There are a few species which have secondarily lost this feature, such as [[Bdelloidea]] and some [[parthenocarpic]] plants.

===Diploidy===
Organisms need to replicate their genetic material in an efficient and reliable manner. The necessity to repair genetic damage is one of the leading theories explaining the origin of sexual reproduction. [[Diploid]] individuals can repair a damaged section of their DNA via [[homologous recombination]], since there are two copies of the gene in the cell and if one copy is [[DNA damage (naturally occurring)|damaged]], the other copy is unlikely to be damaged at the same site.

A harmful damage in a [[haploid]] individual, on the other hand, is more likely to become fixed (i.e. permanent), since any [[DNA repair]] mechanism would have no source from which to recover the original undamaged sequence.<ref name="dna-repair" /> The most primitive form of sex may have been one organism with damaged DNA replicating an undamaged strand from a similar organism in order to repair itself.<!--
 --><ref name="tatiana">{{cite book | author = Olivia Judson | title = Dr. Tatiana's sex advice to all creation | publisher = Metropolitan Books | location = New York | year = 2002 | isbn = 978-0-8050-6331-8 | pages = [https://archive.org/details/drtatianassexadv00juds/page/233 233–4] | url = https://archive.org/details/drtatianassexadv00juds/page/233 }}</ref>

===Meiosis===

Sexual reproduction appears to have arisen very early in [[eukaryote|eukaryotic]] evolution, implying that the essential features of [[meiosis]] were already present in the [[last eukaryotic common ancestor]].<ref>{{cite journal | vauthors=Dacks J, Roger AJ | s2cid=9441768 | title=The first sexual lineage and the relevance of facultative sex | journal=Journal of Molecular Evolution | volume=48 | issue=6 | pages=779–783 | date=June 1999 | pmid=10229582 | doi=10.1007/PL00013156 | bibcode=1999JMolE..48..779D }}</ref><ref name =Bernstein2010 /><ref name=BernsteinIntech/> In extant organisms, proteins with central functions in meiosis are similar to key proteins in [[transformation (genetics)|natural transformation]] in bacteria and DNA transfer in [[archaea]].<ref name=BernsteinIntech>Bernstein, H., Bernstein, C. Evolutionary origin and adaptive function of meiosis. In "Meiosis", Intech Publ (Carol Bernstein and Harris Bernstein editors), Chapter 3: 41-75 (2013).</ref><ref name=Bernsteinarchaea>{{cite book |last1=Bernstein |first1=H |chapter=Sexual communication in archaea, the precursor to meiosis |editor1-last=Witzany |editor1-first=Guenther |doi=10.1007/978-3-319-65536-9 |title=Biocommunication of Archaea |year=2017 |isbn=978-3-319-65535-2 |s2cid=26593032 |pages=103–117}}</ref> For example, [[recA]] recombinase, that catalyses the key functions of DNA [[homology (biology)|homology]] search and strand exchange in the bacterial sexual process of transformation, has [[orthologs]] in eukaryotes that perform similar functions in meiotic recombination<ref name=BernsteinIntech/>

Natural transformation in bacteria, DNA transfer in [[archaea]], and [[meiosis]] in eukaryotic microorganisms are induced by stressful circumstances such as overcrowding, resource depletion, and DNA damaging conditions.<ref name="LODÉ T 2012"/><ref name=BernsteinIntech /><ref name=Bernsteinarchaea /> This suggests that these sexual processes are adaptations for dealing with stress, particularly stress that causes DNA damage. In bacteria, these stresses induce an altered physiologic state, termed competence, that allows active take-up of DNA from a donor bacterium and the integration of this DNA into the recipient genome (see [[Natural competence]]) allowing recombinational repair of the recipients' damaged DNA.<ref>{{cite journal |vauthors=Michod RE, Wojciechowski MF, Hoelzer MA |year=1988 |title=DNA repair and the evolution of transformation in the bacterium Bacillus subtilis |journal=Genetics |volume=118 |issue=1 |pages=31–39 |doi=10.1093/genetics/118.1.31 |pmid=8608929 |pmc=1203263}}</ref>

If environmental stresses leading to DNA damage were a persistent challenge to the survival of early microorganisms, then selection would likely have been continuous through the prokaryote to eukaryote transition,<ref name="ReferenceA"/><ref name=BernsteinIntech /> and adaptative adjustments would have followed a course in which bacterial transformation or archaeal DNA transfer naturally gave rise to sexual reproduction in eukaryotes.

===Virus-like RNA-based origin===
Sex might also have been present even earlier, in the hypothesized [[RNA world]] that preceded DNA cellular life forms.<ref>{{cite journal |pmid=6164094 |volume=244 |issue=4 |title=The origin of genetic information |date=April 1981 |pages=88–92, 96, et passim |vauthors=[[Manfred Eigen|Eigen M]], Gardiner W, [[Peter Schuster|Schuster P]], [[Ruthild Winkler|Winkler-Oswatitsch R]] |journal=Scientific American |doi=10.1038/scientificamerican0481-88|bibcode=1981SciAm.244d..88E }}</ref> One proposed origin of sex in the RNA world was based on the type of sexual interaction that is known to occur in extant single-stranded segmented RNA viruses, such as influenza virus, and in extant double-stranded segmented RNA viruses such as reovirus.<ref>{{cite journal |pmid=6209512 |doi=10.1016/S0022-5193(84)80178-2 |volume=110 |issue=3 |title=Origin of sex |date=October 1984 |pages=323–351 |vauthors=Bernstein H, Byerly HC, Hopf FA, Michod RE |journal=Journal of Theoretical Biology|bibcode=1984JThBi.110..323B }}</ref>

Exposure to conditions that cause RNA damage could have led to blockage of replication and death of these early RNA life forms. Sex would have allowed re-assortment of segments between two individuals with damaged RNA, permitting undamaged combinations of RNA segments to come together, thus allowing survival. Such a regeneration phenomenon, known as multiplicity reactivation, occurs in the influenza virus<ref>{{cite journal |author=Barry RD |year=1961 |title=The multiplication of influenza virus. II. Multiplicity reactivation of ultraviolet irradiated virus |journal=Virology |volume=14 |issue=4 |pages=398–405 |pmid=13687359 |doi=10.1016/0042-6822(61)90330-0 |hdl=1885/109240 |hdl-access=free }}</ref> and reovirus.<ref>{{cite journal |vauthors=McClain ME, Spendlove RS |year=1966 |title=Multiplicity reactivation of reovirus particles after exposure to ultraviolet light |journal=J Bacteriol |volume=92 |issue=5 |pages=1422–1429 |doi=10.1128/JB.92.5.1422-1429.1966 |pmid=5924273 |pmc=276440}}</ref>

===Parasitic DNA elements===
Another theory is that sexual reproduction originated from [[Selfish DNA|selfish parasitic genetic elements]] that exchange genetic material (that is: copies of their own genome) for their transmission and propagation. In some organisms, sexual reproduction has been shown to enhance the spread of parasitic genetic elements (e.g. yeast, filamentous fungi).<ref name="hickey">{{cite journal |author=Hickey D |title=Selfish DNA: a sexually-transmitted nuclear parasite |journal=Genetics |volume=101 |issue=3–4 |pages=519–531 |year=1982 |doi=10.1093/genetics/101.3-4.519 |pmid=6293914 |pmc=1201875}}</ref>

[[Bacterial conjugation]] is a form of genetic exchange that some sources describe as "sex", but technically is not a form of reproduction, even though it is a form of [[horizontal gene transfer]]. However, it does support the "selfish gene" part theory, since the gene itself is propagated through the [[F-plasmid]].<ref name="tatiana" />

A similar origin of sexual reproduction is proposed to have evolved in ancient [[haloarchaea]] as a combination of two independent processes: [[jumping genes]] and [[plasmid]] swapping.<ref>{{cite journal |title=Extreme Microbes |first=Shiladitya |last=DasSarma |year=2007 |volume=95 |issue=3 |pages=224–231 |doi=10.1511/2007.65.224 |journal=American Scientist}}</ref>

===Partial predation===
A third theory is that sex evolved as a form of [[cannibalism]]: One primitive organism ate another one, but instead of completely digesting it, some of the eaten organism's DNA was incorporated into the DNA of the eater.<ref name="tatiana" /><ref name=Ploompuu1999/>

===Vaccination-like process===
{{One source section
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Sex may also be derived from another prokaryotic process. A comprehensive theory called "origin of sex as vaccination" proposes that eukaryan sex-as-[[fertilisation|syngamy]] (fusion sex) arose from prokaryan unilateral sex-as-infection, when infected hosts began swapping nuclearised genomes containing coevolved, vertically transmitted symbionts that provided protection against horizontal superinfection by other, more virulent symbionts.

Consequently, sex-as-meiosis (fission sex) would evolve as a host strategy for uncoupling from (and thereby render impotent) the acquired symbiotic/parasitic genes.<ref name="sterrer">{{cite journal |author=Sterrer W |title=On the origin of sex as vaccination |journal=Journal of Theoretical Biology |volume=216 |issue=4 |pages=387–396 |year=2002 |doi=10.1006/jtbi.2002.3008 |pmid=12151256|bibcode=2002JThBi.216..387S }}</ref>

==Mechanistic origin of sexual reproduction==
While theories positing fitness benefits that led to the origin of sex are often problematic,{{Citation needed|date=July 2018}} several theories addressing the emergence of the mechanisms of sexual reproduction have been proposed.

===Viral eukaryogenesis===
{{main| Viral eukaryogenesis}}
The viral eukaryogenesis (VE) theory proposes that eukaryotic cells arose from a combination of a [[lysogenic]] virus, an [[archaea]]n, and a [[bacterium]]. This model suggests that the nucleus originated when the lysogenic virus incorporated genetic material from the archaean and the bacterium and took over the role of information storage for the amalgam. The archaeal host transferred much of its functional genome to the virus during the evolution of cytoplasm, but retained the function of gene translation and general metabolism. The bacterium transferred most of its functional genome to the virus as it transitioned into a [[mitochondria|mitochondrion]].<ref name="bell-2001">{{cite journal |author=Bell, PJ |title=Viral eukaryogenesis: Was the ancestor of the nucleus a complex DNA virus? |journal=Journal of Molecular Biology |volume=53 |issue=3 |pages=251–256 |year=2001 |doi=10.1007/s002390010215 |pmid=11523012|bibcode=2001JMolE..53..251L |s2cid=20542871 |doi-access=free }}</ref>

For these transformations to lead to the eukaryotic cell cycle, the VE hypothesis specifies a pox-like virus as the lysogenic virus. A pox-like virus is a likely ancestor because of its fundamental similarities with eukaryotic nuclei. These include a double stranded DNA genome, a linear chromosome with short [[telomere|telomeric]] repeats, a complex membrane bound capsid, the ability to produce capped mRNA, and the ability to export the capped mRNA across the viral membrane into the [[cytoplasm]]. The presence of a lysogenic pox-like virus ancestor explains the development of meiotic division, an essential component of sexual reproduction.<ref name="bell-2006">{{cite journal |author=Bell, PJ |title=Sex and the eukaryotic cell cycle is consistent with a viral ancestry for the eukaryotic nucleus |journal=Journal of Theoretical Biology |volume=243 |issue=1 |pages=54–63 |year=2006 |doi=10.1016/j.jtbi.2006.05.015 |pmid=16846615 |bibcode=2006JThBi.243...54B }}</ref>

[[Meiotic]] division in the VE hypothesis arose because of the evolutionary pressures placed on the lysogenic virus as a result of its inability to enter into the [[lytic cycle]]. This selective pressure resulted in the development of processes allowing the viruses to spread horizontally throughout the population. The outcome of this selection was cell-to-cell fusion. (This is distinct from the conjugation methods used by bacterial plasmids under evolutionary pressure, with important consequences.)<ref name="bell-2001" /> The possibility of this kind of fusion is supported by the presence of fusion proteins in the envelopes of the pox viruses that allow them to fuse with host membranes. These proteins could have been transferred to the cell membrane during viral reproduction, enabling cell-to-cell fusion between the virus host and an uninfected cell. The theory proposes meiosis originated from the fusion between two cells infected with related but different viruses which recognised each other as uninfected. After the fusion of the two cells, incompatibilities between the two viruses result in a meiotic-like cell division.<ref name="bell-2006" />

The two viruses established in the cell would initiate replication in response to signals from the host cell. A mitosis-like cell cycle would proceed until the viral membranes dissolved, at which point linear chromosomes would be bound together with centromeres. The homologous nature of the two viral centromeres would incite the grouping of both sets into tetrads. It is speculated that this grouping may be the origin of crossing over, characteristic of the first division in modern meiosis. The partitioning apparatus of the mitotic-like cell cycle the cells used to replicate independently would then pull each set of chromosomes to one side of the cell, still bound by centromeres. These centromeres would prevent their replication in subsequent division, resulting in four daughter cells with one copy of one of the two original pox-like viruses. The process resulting from combination of two similar pox viruses within the same host closely mimics meiosis.<ref name="bell-2006" />

===Neomuran revolution===
An alternative theory, proposed by [[Thomas Cavalier-Smith]], was labeled the [[Neomura|Neomuran revolution]]. The designation "Neomuran revolution" refers to the appearances of the common ancestors of eukaryotes and archaea. Cavalier-Smith proposes that the first neomurans emerged 850 million years ago. Other molecular biologists assume that this group appeared much earlier, but Cavalier-Smith dismisses these claims because they are based on the "theoretically and empirically" unsound model of [[molecular clock]]s. Cavalier-Smith's theory of the Neomuran revolution has implications for the evolutionary history of the cellular machinery for recombination and sex. It suggests that this machinery evolved in two distinct bouts separated by a long period of stasis; first the appearance of recombination machinery in a bacterial ancestor which was maintained for 3 Gy(billion years), until the neomuran revolution when the mechanics were adapted to the presence of [[nucleosome]]s. The archaeal products of the revolution maintained recombination machinery that was essentially bacterial, whereas the eukaryotic products broke with this bacterial continuity. They introduced cell fusion and ploidy cycles into cell life histories. Cavalier-Smith argues that both bouts of mechanical evolution were motivated by similar selective forces: the need for accurate DNA replication without loss of viability.<ref name="TCSmith">{{cite journal |author=Cavalier-Smith, Thomas |title=Cell evolution and Earth history: Stasis and revolution |journal=Philosophical Transactions of the Royal Society B: Biological Sciences |volume=361 |issue=1470 |pages=969–1006 |year=2006 |doi=10.1098/rstb.2006.1842 |pmid=16754610 |pmc=1578732 }}</ref>

{{clear}}

==Questions==
Some questions biologists have attempted to answer include:
* Why does sexual reproduction exist, if in many organisms it has a 50% cost (fitness disadvantage) in relation to asexual reproduction?<ref name="Ridley M 2004 p. 314">{{cite book|last =Ridley|first= Mark|date= 2003 |title =Evolution|edition = 3rd |publisher = Wiley|page = 314|isbn = 9781405103459}}</ref>
* Did [[mating type]]s (types of gametes, according to their compatibility) arise as a result of [[anisogamy]] (gamete dimorphism), or did mating types evolve before anisogamy?<ref>T. Togashi, P. Cox (Eds.) ''The Evolution of Anisogamy''. Cambridge University Press, Cambridge; 2011, p. 22-29.</ref><ref>Beukeboom, L. & Perrin, N. (2014). ''The Evolution of Sex Determination''. Oxford University Press, p. 25 [https://books.google.com/books?id=d4cLBAAAQBAJ&pg=PA25]. Online resources, [http://www.oup.co.uk/companion/beukeboom].</ref>
* Why do most sexual organisms use a binary [[mating system]]? Grouping itself offers a survival advantage. A binary recognition based system is the most simple and effective method in maintaining species grouping.<ref>{{cite journal | last1 = Czárán | first1 = T.L. | last2 = Hoekstra | first2 = R.F. | year = 2006 | title = Evolution of sexual asymmetry | journal = BMC Evolutionary Biology | volume = 4 | pages = 34–46 |doi=10.1186/1471-2148-4-34 | pmid = 15383154 | pmc = 524165 | doi-access = free }}</ref> 
* Why do some organisms have gamete dimorphism?

==References==
{{Reflist|30em}}

==Further reading==
* {{Cite book |last=Bell |first=Graham |author-link=Graham Bell (biologist) |title=The masterpiece of nature: the evolution and genetics of sexuality |publisher=University of California Press |location=Berkeley |year=1982 |isbn=978-0-520-04583-5}}
* {{Cite book |last=Bernstein |first=Carol |author2=Harris Bernstein |title=Aging, sex, and DNA repair |publisher=Academic Press |location=Boston |year=1991 |isbn=978-0-12-092860-6 }}
* {{Cite journal | last = Hurst | first = L.D. |author2=J.R. Peck | title = Recent advances in the understanding of the evolution and maintenance of sex | journal = [[Trends in Ecology and Evolution]] | volume = 11 | pages = 46–52 | year = 1996 | doi = 10.1016/0169-5347(96)81041-X | issue = 2 | pmid=21237760| bibcode = 1996TEcoE..11...46H }}
* {{Cite book |last=Levin |first=Bruce R. |author2=Richard E. Michod |title=The Evolution of sex: an examination of current ideas |publisher=Sinauer Associates |location=Sunderland, Mass |year=1988 |isbn=978-0-87893-459-1 |url-access=registration |url=https://archive.org/details/evolutionofsexex0000unse }}
* {{Cite book |last=Maynard Smith |first=John |author-link=John Maynard Smith |title=The evolution of sex |publisher=Cambridge University Press |location=Cambridge, UK |year=1978 |isbn=978-0-521-21887-0 |url=https://archive.org/details/evolutionofsex0000mayn }}
* {{Cite book |last=Michod |first=Richard E. |title=Eros and evolution: a natural philosophy of sex |publisher=Addison-Wesley Pub. Co |location=Reading, Mass |year=1995 |isbn=978-0-201-40754-9 |url=https://archive.org/details/erosevolutionnat0000mich }}
*{{Cite news|url=http://www.nbcnews.com/id/27927661|archive-url=https://web.archive.org/web/20151219170335/http://www.nbcnews.com/id/27927661/|url-status=dead|archive-date=19 December 2015|title=Scientists put sex origin mystery to bed, Wild strawberry research provides evidence on when gender emerges|access-date=25 November 2008 |work=[[NBC News]]}}
* {{Cite book |last=Ridley |first=Mark |author-link=Mark Ridley (zoologist) |title=Evolution |publisher=Blackwell Scientific |location=Oxford |year=1993 |isbn=978-0-632-03481-9}}
* {{Cite book |last=Ridley |first=Mark |author-link=Mark Ridley (zoologist) |title=Mendel's demon: gene justice and the complexity of life |publisher=Weidenfeld & Nicolson |location=London |year=2000 |isbn=978-0-297-64634-1}}
* {{Cite book |last=Ridley |first=Matt |author-link=Matt Ridley |title=The Red Queen: sex and the evolution of human nature |publisher=Penguin Books |location=New York |year=1995 |isbn=978-0-14-024548-6}}
* {{Cite book |last=Szathmáry |first=Eörs |author2=John Maynard Smith |author-link=Eörs Szathmáry |title=The Major Transitions in Evolution |publisher=W.H. Freeman Spektrum |location=Oxford |year=1995 |isbn=978-0-7167-4525-9|author-link2=John Maynard Smith|title-link=The Major Transitions in Evolution }}
* {{Cite book |last=Taylor |first=Timothy |title=The prehistory of sex: four million years of human sexual culture |publisher=Bantam Books |location=New York |year=1996 |isbn=978-0-553-09694-1 |url=https://archive.org/details/prehistoryofsexf00tay_zn9 }}
* {{Cite book |last=Williams |first=George |author-link=George C. Williams (biologist) |title=Sex and evolution |publisher=Princeton University Press |location=Princeton, N.J |year=1975 |isbn=978-0-691-08147-2}}

==External links==
* [http://www.livescience.com/health/050330_sex_good.html Why Sex is Good (2005)]
* [http://www.philippwesche.org/old1/es.html The Evolution of Sexs (2003)]
* [http://www.evolocus.com/Textbooks/Geodakian2012.pdf The Evolutionary Theory of Sex (2012)]
* [https://www.nature.com/scitable/topicpage/sexual-reproduction-and-the-evolution-of-sex-824/ Sexual Reproduction and the Evolution of Sex] ([https://archive.today/20231008141323/https://www.nature.com/scitable/topicpage/sexual-reproduction-and-the-evolution-of-sex-824/ Archived (2023)]) − [[Nature (journal)|Nature journal]] (2008)

{{Sex (biology)}}
{{Evolution}}
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{{portal bar|Biology|Evolutionary biology|Science}}

{{DEFAULTSORT:Evolution Of Sexual Reproduction}}
[[Category:Evolutionary biology]]
[[Category:Sexual reproduction]]
[[Category:Sexual selection]]