McAllester Christopher S, Pool John E
Laboratory of Genetics, University of Wisconsin, Madison, United States.
Elife. 2025 Apr 16;12:RP93338. doi: 10.7554/eLife.93338.
Chromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for the maintenance of inversion polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one of which has negative frequency-dependent fitness. These conditions yield a form of frequency-dependent disruptive selection, favoring two predominant haplotypes segregating alleles that favor opposing antagonistic phenotypes. An inversion associated with one haplotype can reduce the fitness load incurred by generating recombinant offspring, reinforcing its linkage to the haplotype and enabling both haplotypes to accumulate more antagonistic variants than expected otherwise. We develop and apply a forward simulator to examine these dynamics under a tradeoff between survival and male display. These simulations indeed generate inversion-associated haplotypes with opposing sex-specific fitness effects. Antagonism strengthens with time, and can ultimately yield karyotypes at surprisingly predictable frequencies, with striking genotype frequency differences between sexes and between developmental stages. To test whether this model may contribute to well-studied yet enigmatic inversion polymorphisms in , we track inversion frequencies in laboratory crosses to test whether they influence male reproductive success or survival. We find that two of the four tested inversions show significant evidence for the tradeoff examined, with favoring survival and favoring male reproduction. In line with the apparent sex-specific fitness effects implied for both of those inversions, was also found to be less costly to the viability and/or longevity of males than females, whereas was more beneficial to female survival. Based on this work, we expect that balancing selection on antagonistically pleiotropic traits may provide a significant and underappreciated contribution to the maintenance of natural inversion polymorphism.
染色体倒位多态性可能很常见,但其持续存在的原因往往不明。我们提出了一个维持倒位多态性的模型,该模型要求一些变异对两种表型产生拮抗作用,其中一种表型具有负频率依赖适合度。这些条件产生了一种频率依赖的分裂选择形式,有利于两种主要单倍型分离出有利于相反拮抗表型的等位基因。与一种单倍型相关的倒位可以通过产生重组后代来降低适合度负担,加强其与单倍型的连锁,并使两种单倍型能够积累比其他情况更多的拮抗变异。我们开发并应用了一个正向模拟器来研究在生存和雄性展示之间权衡下的这些动态。这些模拟确实产生了具有相反性别特异性适合度效应的与倒位相关的单倍型。拮抗作用随时间增强,最终可以产生频率惊人可预测的核型,在性别和发育阶段之间存在显著的基因型频率差异。为了测试这个模型是否可能有助于解释在[具体物种]中经过充分研究但仍神秘的倒位多态性,我们在实验室杂交中跟踪倒位频率,以测试它们是否影响雄性繁殖成功或生存。我们发现,四个测试倒位中的两个显示出了所研究权衡的显著证据,其中[某个倒位]有利于生存,[另一个倒位]有利于雄性繁殖。与这两个倒位所暗示的明显性别特异性适合度效应一致,还发现[某个倒位]对雄性生存力和/或寿命的成本低于雌性,而[另一个倒位]对雌性生存更有益。基于这项工作,我们预计对拮抗多效性性状的平衡选择可能为维持自然倒位多态性做出重大且未被充分认识的贡献。