Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability.
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 varian...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-02-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1010063 |
| _version_ | 1818050497905426432 |
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| author | Katja R Kasimatis Megan J Moerdyk-Schauwecker Ruben Lancaster Alexander Smith John H Willis Patrick C Phillips |
| author_facet | Katja R Kasimatis Megan J Moerdyk-Schauwecker Ruben Lancaster Alexander Smith John H Willis Patrick C Phillips |
| author_sort | Katja R Kasimatis |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-10T10:54:25Z |
| format | Article |
| id | doaj.art-0f06aa36ae4d412ca4d8b2bc60f04907 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-10T10:54:25Z |
| publishDate | 2022-02-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-0f06aa36ae4d412ca4d8b2bc60f049072022-12-22T01:51:55ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042022-02-01182e101006310.1371/journal.pgen.1010063Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability.Katja R KasimatisMegan J Moerdyk-SchauweckerRuben LancasterAlexander SmithJohn H WillisPatrick C PhillipsSexual 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.https://doi.org/10.1371/journal.pgen.1010063 |
| spellingShingle | Katja R Kasimatis Megan J Moerdyk-Schauwecker Ruben Lancaster Alexander Smith John H Willis Patrick C Phillips Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability. PLoS Genetics |
| title | Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability. |
| title_full | Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability. |
| title_fullStr | Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability. |
| title_full_unstemmed | Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability. |
| title_short | Post-insemination selection dominates pre-insemination selection in driving rapid evolution of male competitive ability. |
| title_sort | post insemination selection dominates pre insemination selection in driving rapid evolution of male competitive ability |
| url | https://doi.org/10.1371/journal.pgen.1010063 |
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