The paradox of obligate sex: the roles of sexual conflict and mate scarcity in transitions to facultative and obligate asexuality

The maintenance of obligate sex in animals is a long-standing evolutionary paradox. To solve this puzzle, evolutionary models need to explain why obligately sexual populations consistently resist invasion by facultative strategies that combine the benefits of both sexual and asexual reproduction. Sexual antagonism and mate availability are thought to shape the occurrence of reproductive modes in facultative systems. But it is unclear how such factors interact with each other to influence facultative invasions and transitions to obligate asexuality. Using individual-based models, we clarify how sexually antagonistic coevolution and mate availability affect the likelihood that a mutant allele that gives virgin females the ability to reproduce parthenogenetically will invade an obligately sexual population. We show that male coercion cannot stop the allele from spreading because mutants generally benefit by producing at least some offspring asexually prior to encountering males. We find that effects of sexual conflict can lead to positive frequency-dependent dynamics, where the spread of the allele is promoted by effective (no-cost) resistance when males are common, and by mate limitation when sex-ratios are female-biased. However, once the mutant allele fixes, effective coercion prevents the complete loss of sex unless linkage disequilibrium can build up between the allele and alleles for effective resistance. Our findings clarify how limitations of female resistance imposed by the genetic architecture of sexual antagonism can promote the maintenance of sexual reproduction. At the same time, our finding of widespread obligate sex when costs of parthenogenesis are high suggests that developmental constraints could contribute to the rarity of facultative reproductive strategies in nature.

动物专性有性生殖（obligate sex）的维持机制，长期以来都是演化生物学领域的一大未解悖论。为破解这一难题，演化模型需要阐释：为何专性有性生殖种群始终能够抵御兼具有性与无性生殖优势的兼性生殖策略（facultative strategies）的入侵。学界普遍认为，性拮抗（sexual antagonism）与配偶可获得性（mate availability）会塑造兼性生殖系统中生殖模式的出现，但目前尚不清楚这些因素如何相互作用，影响兼性策略的入侵以及向专性无性生殖（obligate asexuality）的转变。本研究借助基于个体的模型（individual-based models），阐明了性拮抗协同演化与配偶可获得性，如何影响使处女雌性获得孤雌生殖（parthenogenesis）能力的突变等位基因（mutant allele）入侵专性有性生殖种群的概率。研究表明，雄性胁迫（male coercion）无法阻止该等位基因的扩散，因为突变体通常可在遭遇雄性前，通过无性生殖产生至少部分后代，从而获得适应性收益。研究发现，性冲突（sexual conflict）的作用可引发正频率依赖动态（positive frequency-dependent dynamics）：当雄性种群密度较高时，有效的（无成本）抗性会促进该等位基因的扩散；而当性比偏向雌性时，配偶限制（mate limitation）则会推动其扩散。不过，一旦该突变等位基因在种群中固定，有效的雄性胁迫便可阻止有性生殖的彻底丧失，除非该等位基因与有效抗性等位基因之间能够建立连锁不平衡（linkage disequilibrium）。本研究结果阐明了性拮抗的遗传架构（genetic architecture）所施加的雌性抗性限制，如何助力维持有性生殖。与此同时，当孤雌生殖存在较高成本时，自然界中仍广泛存在专性有性生殖的现象，这表明发育限制（developmental constraints）或许是自然界中兼性生殖策略较为罕见的原因之一。