Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability.
Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability.
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DOI：
10.1371/journal.pgen.1010063
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发表时间：
2022-03
期刊：
影响因子：
4.5
通讯作者：
Phillips PC
中科院分区：
文献类型：
--
作者：
Kasimatis KR;Moerdyk-Schauwecker MJ;Lancaster R;Smith A;Willis JH;Phillips PC
有性生殖是一个复杂的过程，导致了性别之间的差异和物种之间的分歧。从男性的角度来看，性选择可以通过作用于交配成功的方差（授精前选择）以及受精成功的方差（授精后选择）来优化生殖成功。授精前和授精后选择之间的平衡尚未使用强有力的假设检验框架，直接量化授精后选择对生殖成功的演变的影响进行了研究。在这里，我们使用实验进化的一个独特的工程遗传系统，允许精子生产被关闭和关闭专性的雄性-雌性群体的秀丽隐杆线虫。我们发现，增强后授精竞争增加了选择的效力，并超过了授精前的性选择，在男性生殖成功的多基因反应。我们发现，经过10次选择性事件发生超过30代后，授精选择增加了男性生殖成功的平均5至7倍。与预期相反，增强的受精前竞争阻碍了选择，减缓了进化的速度。此外，我们发现，授精后的选择导致在全基因组水平上的强多基因反应。我们的研究结果表明，授精后的性选择在快速优化雄性生殖适合度中起着至关重要的作用。因此，在考虑性选择的种群效应时，应明确考虑授精后的动态。在自然界中观察到的一些最引人注目、最多样化的表型--如野绵羊的头撞和孔雀的精致尾巴--都是性二态的。这些显着的表型是性选择的结果，优化繁殖成功的女性和男性独立。对于雄性来说，总的繁殖成功包括赢得交配事件，然后将交配事件转化为受精事件。因此，不仅要了解男性生殖成功是如何组成的，而且还要了解它是如何演变的，我们必须研究授精前和授精后性选择之间的相互作用。我们结合联合收割机的环境诱导控制精子生产的高度可重复的析因实验进化设计，直接量化的贡献，授精后选择男性生殖进化。我们证明，增强的精子竞争增加了选择的效力，提高了雄性进化的速度。或者，我们表明，增强的受精前竞争减缓了进化速度。使用全基因组方法，我们确定了60多个有助于男性受精成功的基因。总之，我们的新方法和结果表明，在授精后发生的分子相互作用的看不见的世界是作为交配前的因素根本重要。
Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. From a male’s perspective, sexual selection can optimize reproductive success by acting on the variance in mating success (pre-insemination selection) as well as the variance in fertilization success (post-insemination selection). The balance between pre- and post-insemination selection has not yet been investigated using a strong hypothesis-testing framework that directly quantifies the effects of post-insemination selection on the evolution of reproductive success. Here we use experimental evolution of a uniquely engineered genetic system that allows sperm production to be turned off and on in obligate male-female populations of Caenorhabditis elegans. We show that enhanced post-insemination competition increases the efficacy of selection and surpasses pre-insemination sexual selection in driving a polygenic response in male reproductive success. We find that after 10 selective events occurring over 30 generations post-insemination selection increased male reproductive success by an average of 5- to 7-fold. Contrary to expectation, enhanced pre-insemination competition hindered selection and slowed the rate of evolution. Furthermore, we found that post-insemination selection resulted in a strong polygenic response at the whole-genome level. Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness. Therefore, explicit consideration should be given to post-insemination dynamics when considering the population effects of sexual selection. Some of the most dramatic and diverse phenotypes observed in nature––such as head-butting in wild sheep and the elaborate tails of peacocks––are sexually dimorphic. These remarkable phenotypes are a result of sexual selection optimizing reproductive success in females and males independently. For males, total reproductive success is comprised of winning a mating event and then translating that mating event into a fertilization event. Therefore, to understand not only how male reproductive success is comprised, but also how it evolves, we must examine the interaction between pre- and post-insemination sexual selection. We combine environmentally-inducible control of sperm production within a highly reproducible factorial experimental evolution design to directly quantify the contribution of post-insemination selection to male reproductive evolution. We demonstrate that enhanced sperm competition increases the efficacy of selection and enhances the rate of male evolution. Alternatively, we show that enhanced pre-insemination competition slows the evolutionary rate. Using whole-genome approaches, we identify over 60 genes that contribute to male fertilization success. Brought together, our new approaches and results demonstrate that the unseen world of molecular interactions occurring during post-insemination are as fundamentally important as pre-mating factors.
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影响因子：
30.8
作者：
Andersen, Erik C.;Gerke, Justin P.;Shapiro, Joshua A.;Crissman, Jonathan R.;Ghosh, Rajarshi;Bloom, Joshua S.;Felix, Marie-Anne;Kruglyak, Leonid
通讯作者：
Kruglyak, Leonid
影响因子：
46.9
作者：
Doench JG;Fusi N;Sullender M;Hegde M;Vaimberg EW;Donovan KF;Smith I;Tothova Z;Wilen C;Orchard R;Virgin HW;Listgarten J;Root DE
通讯作者：
Root DE
DOI：
10.1006/bbrc.2000.2260
发表时间：
2000-03-05
影响因子：
3.1
作者：
Gengyo-Ando, K;Mitani, S
通讯作者：
Mitani, S
影响因子：
16.6
作者：
Devigili, Alessandro;Evans, Jonathan P.;Pilastro, Andrea
通讯作者：
Pilastro, Andrea
DOI：
10.1073/pnas.96.9.5083
发表时间：
1999-04-27
影响因子：
11.1
作者：
Holland, B;Rice, WR
通讯作者：
Rice, WR