Differing associations between sex determination and sex‐linked inversions in two ecotypes of Littorina saxatilis
Abstract Sexual antagonism is a common hypothesis for driving the evolution of sex chromosomes, whereby recombination suppression is favored between sexually antagonistic loci and the sex‐determining locus to maintain beneficial combinations of alleles. This results in the formation of a sex‐determi...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Oxford University Press
2022-10-01
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| Series: | Evolution Letters |
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| Online Access: | https://doi.org/10.1002/evl3.295 |
| _version_ | 1827837659730411520 |
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| author | Katherine E. Hearn Eva L. Koch Sean Stankowski Roger K. Butlin Rui Faria Kerstin Johannesson Anja M. Westram |
| author_facet | Katherine E. Hearn Eva L. Koch Sean Stankowski Roger K. Butlin Rui Faria Kerstin Johannesson Anja M. Westram |
| author_sort | Katherine E. Hearn |
| collection | DOAJ |
| description | Abstract Sexual antagonism is a common hypothesis for driving the evolution of sex chromosomes, whereby recombination suppression is favored between sexually antagonistic loci and the sex‐determining locus to maintain beneficial combinations of alleles. This results in the formation of a sex‐determining region. Chromosomal inversions may contribute to recombination suppression but their precise role in sex chromosome evolution remains unclear. Because local adaptation is frequently facilitated through the suppression of recombination between adaptive loci by chromosomal inversions, there is potential for inversions that cover sex‐determining regions to be involved in local adaptation as well, particularly if habitat variation creates environment‐dependent sexual antagonism. With these processes in mind, we investigated sex determination in a well‐studied example of local adaptation within a species: the intertidal snail, Littorina saxatilis. Using SNP data from a Swedish hybrid zone, we find novel evidence for a female‐heterogametic sex determination system that is restricted to one ecotype. Our results suggest that four putative chromosomal inversions, two previously described and two newly discovered, span the putative sex chromosome pair. We determine their differing associations with sex, which suggest distinct strata of differing ages. The same inversions are found in the second ecotype but do not show any sex association. The striking disparity in inversion‐sex associations between ecotypes that are connected by gene flow across a habitat transition that is just a few meters wide indicates a difference in selective regime that has produced a distinct barrier to the spread of the newly discovered sex‐determining region between ecotypes. Such sex chromosome‐environment interactions have not previously been uncovered in L. saxatilis and are known in few other organisms. A combination of both sex‐specific selection and divergent natural selection is required to explain these highly unusual patterns. |
| first_indexed | 2024-03-12T06:49:07Z |
| format | Article |
| id | doaj.art-49e5d130ccd946dd982c2df6f169e137 |
| institution | Directory Open Access Journal |
| issn | 2056-3744 |
| language | English |
| last_indexed | 2024-03-12T06:49:07Z |
| publishDate | 2022-10-01 |
| publisher | Oxford University Press |
| record_format | Article |
| series | Evolution Letters |
| spelling | doaj.art-49e5d130ccd946dd982c2df6f169e1372023-09-03T00:22:37ZengOxford University PressEvolution Letters2056-37442022-10-016535837410.1002/evl3.295Differing associations between sex determination and sex‐linked inversions in two ecotypes of Littorina saxatilisKatherine E. Hearn0Eva L. Koch1Sean Stankowski2Roger K. Butlin3Rui Faria4Kerstin Johannesson5Anja M. Westram6Ecology and Evolutionary Biology, School of Biosciences University of Sheffield Sheffield S10 2TN United KingdomEcology and Evolutionary Biology, School of Biosciences University of Sheffield Sheffield S10 2TN United KingdomEcology and Evolutionary Biology, School of Biosciences University of Sheffield Sheffield S10 2TN United KingdomEcology and Evolutionary Biology, School of Biosciences University of Sheffield Sheffield S10 2TN United KingdomCIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado Campus de Vairão, Universidade do Porto Vairão 4485‐661 PortugalDepartment of Marine Sciences University of Gothenburg Strömstad SE‐45296 SwedenISTA (Institute of Science and Technology Austria) Klosterneuburg 3400 AustriaAbstract Sexual antagonism is a common hypothesis for driving the evolution of sex chromosomes, whereby recombination suppression is favored between sexually antagonistic loci and the sex‐determining locus to maintain beneficial combinations of alleles. This results in the formation of a sex‐determining region. Chromosomal inversions may contribute to recombination suppression but their precise role in sex chromosome evolution remains unclear. Because local adaptation is frequently facilitated through the suppression of recombination between adaptive loci by chromosomal inversions, there is potential for inversions that cover sex‐determining regions to be involved in local adaptation as well, particularly if habitat variation creates environment‐dependent sexual antagonism. With these processes in mind, we investigated sex determination in a well‐studied example of local adaptation within a species: the intertidal snail, Littorina saxatilis. Using SNP data from a Swedish hybrid zone, we find novel evidence for a female‐heterogametic sex determination system that is restricted to one ecotype. Our results suggest that four putative chromosomal inversions, two previously described and two newly discovered, span the putative sex chromosome pair. We determine their differing associations with sex, which suggest distinct strata of differing ages. The same inversions are found in the second ecotype but do not show any sex association. The striking disparity in inversion‐sex associations between ecotypes that are connected by gene flow across a habitat transition that is just a few meters wide indicates a difference in selective regime that has produced a distinct barrier to the spread of the newly discovered sex‐determining region between ecotypes. Such sex chromosome‐environment interactions have not previously been uncovered in L. saxatilis and are known in few other organisms. A combination of both sex‐specific selection and divergent natural selection is required to explain these highly unusual patterns.https://doi.org/10.1002/evl3.295Hybrid zonelocal adaptationrecombination suppressionsex chromosomessexual antagonism |
| spellingShingle | Katherine E. Hearn Eva L. Koch Sean Stankowski Roger K. Butlin Rui Faria Kerstin Johannesson Anja M. Westram Differing associations between sex determination and sex‐linked inversions in two ecotypes of Littorina saxatilis Evolution Letters Hybrid zone local adaptation recombination suppression sex chromosomes sexual antagonism |
| title | Differing associations between sex determination and sex‐linked inversions in two ecotypes of Littorina saxatilis |
| title_full | Differing associations between sex determination and sex‐linked inversions in two ecotypes of Littorina saxatilis |
| title_fullStr | Differing associations between sex determination and sex‐linked inversions in two ecotypes of Littorina saxatilis |
| title_full_unstemmed | Differing associations between sex determination and sex‐linked inversions in two ecotypes of Littorina saxatilis |
| title_short | Differing associations between sex determination and sex‐linked inversions in two ecotypes of Littorina saxatilis |
| title_sort | differing associations between sex determination and sex linked inversions in two ecotypes of littorina saxatilis |
| topic | Hybrid zone local adaptation recombination suppression sex chromosomes sexual antagonism |
| url | https://doi.org/10.1002/evl3.295 |
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