The origin and maintenance of sex has long puzzled evolutionary biologists due to the inherent fitness costs associated with sexual reproductive strategies relative to asexual reproductive strategies. Therefore, elucidation of the benefits of sex in particular environmental scenarios are necessary to explain the overall prevalence of sexual lineages over asexual ones. In addition, this type of cost/benefit analysis may also be useful in explaining the evolutionary exceptions.
Costs of sex
Lewis (1987) outlined the five costs associated with sex that must be countered for sexual organisms to predominate over their asexual conspecifics. 1) First, sexual females suffer a 2-fold genome dilution relative to a parthenogen which contributes all of her genetic material to the resultant progeny. 2) In addition, at low population densities, sexual pairing may be difficult to coordinate especially if females are only receptive for a short period of time. 3) Further, the act of finding and acquiring a mate may be risky business since sexual individuals may suffer increase exposure to predators, diseases, and mate competition aggression. 4) Finally, sexual recombination may disrupt advantageous genetic combinations and 5) meiosis and syngamy exhibit temporal and energetic costs relative to mitotic (asexual) reproduction.
Costs of asex
Although it would seem that asexuals should predominate due two the potentially 2-fold fitness advantage over sexuals. Muller (1964) hypothesized that asexual lineages are selected against due to the accumulation of deleterious mutations within these non-crossing lineages. In other words, these clones can never exhibit fewer mutations than the least loaded clonal lineage and random loss of these least loaded lineages inevitably leads to a progressive accumulation of mutations over evolutionary time. As such, clade selection may explain the general rarity of asexual lineages due to increased extinction rates within these lineages and the observation that asexual lineages tend to lack much diversification supports this idea (Williams 1992). However, this long-term trend does explain the presence or absence of asexual strategies relative to sexual strategies over the short term. In addition, several exceptions occur such as the proliferation of an entire order of parthenogenic Bdelloid rotifers (Williams 1992). Therefore, alternate explanations are necessary to explain the persistence of these lineages.
DNA repair hypothesis
Michod proposes that sex evolved as a mechanism of DNA repair. He argues that meiosis and outcrossing can function to repair (and/or mask) both kinds of genetic errors, damage and mutation. Genetic changes that mechanistically hinder the separation and/or linking of DNA strands are considered damage because replication is not possible without repair. Mutations, however, do not interfere with replication and cannot be recognized by repair enzymes and thus this type of error can only be corrected by a backup chromosome (diploidy) or outcrossing (Michod 1995).
Sex as an Adaptive Strategy
While sex may have originated as a mechanism of DNA repair, it remains difficult to explain its maintenance against other more productive alternatives over the short-term. For example, Williams noted that the existence of facultative parthenogens (species that can reproduce sexually and asexually, suggests that there must be a short-term advantage to sexual strategies. In contrast, most species are obligately sexual and much fewer are obligately asexual. This variation in reproductive strategies suggests that very little recombination and out-crossing are necessary to cope with the perils of DNA damage and mutation. Therefore, when facultative asexuality exists in a particular species, we expect there to be ecological and genetic differences between the sexual and asexual progeny and that these strategies are employed adaptively.
Variable environments
Williams proposed the lottery principle to explain that the genetic variety created by sex can provide the means for adapting to a rapidly changing abiotic and/or biotic environment. He likened asexual reproduction to purchasing a large of lottery tickets with all the same numbers, and sexual reproduction as a smaller number of tickets with all different numbers. In his view, asexual organisms are poorly equipped to cope with rapidly changing environments since they have only one type of genotype “ticket” whereas sexual ones may increase their odds of success by diversifying their genetic “tickets” (Williams 1975). Unfortunately, there is not currently a lot of support for the “lottery principle” since the global distribution of sexual and asexual organisms exhibits that opposite trend. Sexual organisms tend to occur in stable environments whereas asexual ones occur in the unstable ones. However, it appears that Williams was partially correct in his assessment that diversifying your “bets” should increase your odds of success in environments with rapidly changing biotic elements. As such, the Red Queen hypothesis posits that sexually reproducing species can be maintained by their ability to evade co-evolving parasites by creating genetically diverse offspring (Bell and Maynard-Smith 1987). While some evidence suggests that outcrossing does provide a fitness advantage when faced with co-evolving parasites, this theory assumes that clonal lines are not genetically diverse. However, if the rate of accumulation of deleterious mutations is sufficiently low than theoretically a diverse set of clones derived from repeated parthenogenesis and thus asexual could competitively exclude sexual populations (Lively & Howard 1994). Further, several simulation models suggest that sex cannot be maintained by the presence of co-evolving parasites alone (Howard & Lively 1994, Ochoa & Jaffe 1999)
Sex Ratio as an Environmental Adaptation
While facultative asexuals are able to differentially allocate reproduction to sexual and asexual progeny in response to environmental cues. Similarly some sexually reproducing organisms are able to bias the production of male or female progeny in response to environmental cues as well. For example, Werren and Charnov (1978) proposed that if the relative fitness of males and females varies predictably in time, than it may be adaptive for females to alter their sex ratios seasonally. Roy et. al. (2003) tested this hypothesis and found evidence for an environmentally adaptive sex ratio in the spider mite, Tetranychus mcdanieli. Specifically they found that female-biased sex ratios occurred at extreme temperatures. The onset of such temperatures in their natural environment is often a predictive cue of the onset of extreme conditions such as winter or drought. In this species, females are generally more robust than males and thus are better able to survive adverse weather conditions. Therefore, during periods of extreme temperatures, females that bias their sex ratio toward females should be favored by natural selection. Consequently, this spider mite experiment supports the general idea that the existence of biased sex ratios might reflect differential ability of males and females to survive under predictably varying ecological conditions.
Pluralistic Theory of the Maintenance of Sex
Considering the compelling evidence for both DNA repair and sex as an environmentally adaptive strategy, I assert that these hypotheses may be complimentary and that pluralistic models may more effectively explain the maintenance of sex. For example, computer simulations conducted by Howard & Lively (1994) suggest that rates of deleterious mutations, selection pressure against these mutations, parasite transmission rate, and parasite virulence interact to maintain to prevalence of sex in populations. While their hypothesis may not explain the prevalence of sex in all evolutionary scenarios, I expect that the interaction between selective mechanisms will undoubtedly be important in understanding the maintenance of sex and the diversity of reproductive strategies found among and within species in different selective environments.
Literature Cited
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Lewis, W. M. 1987. The cost of sex. In Stearns, S. C. (ed.) The Evolution of Sex and its Consequences. Birkhuser Verlag, Basel.
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