In other words, the P allele conferred the greatest advantage and experienced the strongest positive selection when in positive linkage disequilibrium with alleles conferring a capacity for effective female resistance to mating. High resistance therefore increased the number of offspring produced parthenogenetically, and facilitated rapid and widespread fixation of the mutant allele.
The introduction of the P allele into obligately sexual populations led to one of three distinct evolutionary outcomes: obligate sex, facultative parthenogenesis, or obligate parthenogenesis loss of sex. When males successfully evolved the capacity to coerce any female to mate, facultative parthenogenesis was the predominant outcome, and male extinction rarely occurred.
By contrast, when females evolved effective resistance, male extinction and therefore obligate parthenogenesis was the most common result. Importantly, this finding occurred both when coercion and resistance were modelled as traits determined by single loci and therefore when evolution occurred via selection on standing genetic variation , and when coercion and resistance were modelled as multi-locus traits representing a large mutational target and therefore when sexual arms races could escalate without limit; see Online Appendix This suggests that when effective resistance cannot evolve, male coercion can impede transitions to obligate parthenogenesis and contribute to the maintenance of sex albeit often in combination with parthenogenesis.
By contrast, if coercion can be overcome by effective resistance, transitions to obligate asexuality are likely. Our finding that resistance can be a key factor in transitions to facultative and obligate parthenogenesis is consistent with results of previous studies Kawatsu a ; Burke et al. However, our analysis provides a number of additional insights. In particular, we show that the potential for invasion of facultatively parthenogenetic mutants is strongly dependent on the relative costs of mating for males and females and the dynamics of sexual coevolution.
In addition, our analysis showed that the evolution of obligate parthenogenesis was contingent on the weight of resistance costs: populations evolved to be obligately asexual only to the extent that females were able to bear the cost of resisting mating attempts. This result supports previous findings that facultatively parthenogenetic females should resist only at low population densities where encounter rates are low Gerber and Kokko Our analysis also extends previous work by clarifying the roles of both mate scarcity and sexual conflict, and the consequences of fecundity costs of parthenogenetic reproduction, in evolutionary transitions to facultative and obligate parthenogenesis.
The limitations of resistance highlighted by our analysis have important implications for understanding the incidence of sex and parthenogenesis in nature.
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By contrast, high female resistance genotypes may be rare or absent from many populations due to strong selection against absolute resistance, or due to selection favouring convenience polyandry when costs of resistance are high Rowe Moreover, many resistance behaviours are plastic, with virgin females often the least resistant to mating 79, but see 80 , while fixed strategies of high resistance are probably rare in natural populations. These factors may severely inhibit transitions to asexuality because without the prior evolution of effective resistance transitions to obligate parthenogenesis might be almost impossible.
However, limitations of resistance may only inhibit parthenogenesis derived from spontaneous mutations. Parthenogens originating from interspecies hybridisation are often immediately reproductively isolated from their progenitors Simon et al. This may be one reason why many parthenogenetic organisms — including all known obligately parthenogenetic vertebrates Avise et al.
The evolution of facultative parthenogenesis is expected to mitigate some of the costs of sex at the population level Hurst and Peck By having the capacity to reproduce both sexually and asexually, females should gain the benefits of sex while avoiding some of the costs associated with males, including costs of mating Green and Noakes However, one of the novel findings of our study is that invasions of facultative parthenogenesis can either reduce or exacerbate ongoing sexual conflict over mating rate, depending on the relative costs of mating for males and females.
Our findings also show that facultative parthenogenesis can reduce or exacerbate the risk of population extinction, depending on the effectiveness and cost of resistance. This suggests that the potential benefits of facultative reproduction may be more context-dependent than generally assumed. Sexually antagonistic selection may have dynamic effects on facultative systems that current theory fails to capture.
Including sexual conflict in models of the maintenance of sex could point to interesting avenues for research. Our results provide several testable predictions. If male coercion inhibits the evolution of obligate parthenogenesis, taxa with greater potential for coercion may be less likely to exhibit obligately asexual forms. For example, at a broad phylogenetic scale, the rarity of asexuality in animals compared to plants Otto and Whitton may reflect the far greater variety of opportunities for coercion in animal systems.
For example, male animals can coerce females using behaviours and morphology e. Coercive strategies may be more limited in plants, which lack self-propelled motility, sense organs and nervous systems. Similarly, sessile animals that reproduce via external fertilisation may experience less coercion than free-living, internally-fertilising animals, and parthenogenesis may therefore be more common in such taxa.
Studies are needed to confirm these predictions. Given the broad parameter space over which facultative parthenogenesis spreads in our simulations via the mate scarcity mechanism, the fact that invasions by facultatively parthenogenetic mutants appear to occur so rarely in animal populations requires an explanation. Several factors could contribute to this discrepancy.
First, our models introduced asexual mutants in relatively large numbers, which reduced the likelihood that parthenogenesis would disappear via drift. Natural populations, however, probably give rise to facultatively parthenogenetic mutants at very low rates Schwander et al.
Second, the complex cytological and physiological changes associated with parthenogenetic reproduction such as spontaneous development of unreduced eggs; 91 may require mutations at multiple loci, which may be highly unlikely to occur simultaneously Neiman et al. Third, even if lineages can overcome such genetic constraints, facultative mutants may be less fecund than wild-type females Lamb and Willey Fourth, the spread of mutants may be further constrained in nature by costs associated with plastically switching between sex and parthenogenesis.
In the facultatively parthenogenetic stick insect, Extatosoma tiaratum , females that switch to sex after initially ovipositing parthenogenetically suffer elevated mortality and decreased egg production compared to females reproducing exclusively sexually or asexually Burke et al. Such factors could greatly reduce the potential for sexual populations to generate and be invaded by facultatively parthenogenetic mutants.
However, physiological constraints alone seem unable to explain the wide distribution of obligate sex in the animal kingdom. If parthenogenesis is beneficial, any constraint on parthenogenetic fecundity should be eliminated by long-term selection, as has been demonstrated in artificial selection experiments on the facultatively parthenogenetic fly Drosophila mercatorum Stalker ; Carson Thus, a mechanism that consistently inhibits parthenogenesis in multiple taxa over long evolutionary time frames seems necessary.
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Sexual conflict mediated by male coercion could be such a mechanism. Mating rate is a widespread source of sexual conflict in animals Wedell et al. Because coevolution of male coercion and female resistance can lead to never-ending sexual arms races Rice and Holland ; Holland and Rice ; Gavrilets , sexual conflict could be a consistent long-term inhibitor of parthenogenesis in many lineages.
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However, given our finding that high coercion cannot prevent alleles for facultative parthenogenesis from invading via the mate scarcity mechanism, a combination of constraints — including developmental, physiological, and ecological constraints like sexual coercion — may interact to prevent facultatively parthenogenetic mutants from invading sexual populations in the natural world.
In addition, coercive sons could provide indirect fitness benefits to sexually reproducing females in facultatively parthenogenetic systems Kawatsu These indirect benefits would increase as parthenogenesis spreads and as populations become more female-biased, selecting for male-biased offspring sex-ratios. Such benefits may compound the constraining effect of coercion on transitions to obligate asexuality. The widespread distribution and long-term maintenance of obligate sexual reproduction is an enduring paradox. Identifying genetic benefits of sexual reproduction has been the dominant approach to this problem Hartfield and Keightley But constraints that inhibit invasions of spontaneously derived parthenogenesis could enable obligate sex to persist Vrijenhoek ; Neiman ; Engelstadter , and recent studies suggest that male coercion could play this role Kawatsu a ; Burke et al.
Our results clarify the contribution of sexual conflict and sexually antagonistic coevolution in the maintenance of obligate sex. We show that facultatively parthenogenetic mutants can invade sexual populations because of the benefit to females of reproducing prior to encountering males mate scarcity mechanism , but the probability of facultative populations transitioning to obligate asexuality depends largely on the potential for females to evolve effective, low-cost resistance to mating, such that linkage disequilibrium can build up between alleles for female resistance and alleles for facultative parthenogenesis.
This is because, although females may benefit by reproducing parthenogenetically instead of sexually, obligate parthenogenesis is likely to evolve only if females can overcome male coercion and thereby reproduce without paying the costs of sex. The difficulty of such a feat suggests that sex may be an evolutionary trap imposed on populations by the evolution of coercive males. Thanks to A. Crean, A.
Hooper, Z. Wylde, E. Macartney and A.
Runagall-McNaull for helpful discussions on model design. This model allows for long-term evolution with unlimited escalation of coercion and resistance via mutation and selection, such that neither sex can permanently gain the upper hand in sexual coevolution. All other parameters are set up as in the discrete-trait models described in Methods, the only difference between the continuous-trait model and the discrete-trait i. At the start of continuous-trait model simulations, individuals of each sex are given random trait values for coercion and resistance obtained from a normal distribution of mean 0 and standard deviation 1.
This method of modelling mutation assumes that genetic variance is not diminished by persistent selection, and is therefore not realistic for a moderate number of loci. However, we used this approach in order to maximize evolvability of male coercion and female resistance traits, thereby allowing for a sexual arms race unconstrained by short-term limitations on genetic variance.
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We ran 25 simulations of each of unique parameter combinations of the continuous-trait model, and collected the same data as described for discrete-trait models. In an additional run, we collected mean antagonistic trait values for each sex along with the other statistics described in Methods. We found that, in continuous-trait simulations, P allele invasion was intermediate in frequency compared to the two discrete-trait models compare and contrast Figures 2 A , 2 B and A1 A.
The proportion of simulations ending in obligate parthenogenesis was also intermediate compare and contrast Figures 2 C , 2 D and A1 B. These intermediate results emerged because of the dynamics of chase-away sexual coevolution: every coevolutionary step by one sex further escalated the arms race and selected for counter-adaptation in the other sex, such that coercion was never able to completely subdue resistance, or vice versa.
Graph A shows P allele outcomes; graph B shows reproductive mode outcomes. The small coloured squares in graph A show the proportion of 25 simulation runs per parameter combination ending in P fixation dark orange , P-p polymorphism light orange , P extinction beige , and P never arising white. Coloured squares in graph B show the proportion of 25 simulation runs per parameter combination ending in obligate parthenogenesis dark blue , facultative parthenogenesis medium blue , obligate sex light blue , and population extinction white. However, the negative effect of costly resistance on extinction rates was not as severe in the continuous-trait model as in the resistance model contrast Figures 2 D and A1 B.
This is because escalating sexual coevolution produced more diverse resistance and coercion genotypes than did sexual coevolution resolved in favour of females. This greater variation in female ability to resist also explains why P allele invasions and transitions to obligate parthenogenesis were less frequent in the continuous-trait model compared to the resistance model contrast Figures 2 B and D with Figures A1 A and B , respectively : escalating arms races prevented fixation of permanently high resistance genotypes by facilitating the continuous production of ever more coercive males.
With females unable to decisively gain the upper hand, the ability of linkage disequilibrium between resistance and the P allele to drive males extinct was reduced.