Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan
Abstract Batesian mimicry is a well‐studied adaptation for predation avoidance, in which a mimetic species resembles an unpalatable model species. Batesian mimicry can be under positive selection because of the protection gained against predators, due to resemblance to unpalatable model species. How...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Wiley
2019-05-01
|
| Series: | Ecology and Evolution |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/ece3.5182 |
| _version_ | 1818455119733194752 |
|---|---|
| author | Kaori Tsurui‐Sato Yukuto Sato Emi Kato Mitsuho Katoh Ryosuke Kimura Haruki Tatsuta Kazuki Tsuji |
| author_facet | Kaori Tsurui‐Sato Yukuto Sato Emi Kato Mitsuho Katoh Ryosuke Kimura Haruki Tatsuta Kazuki Tsuji |
| author_sort | Kaori Tsurui‐Sato |
| collection | DOAJ |
| description | Abstract Batesian mimicry is a well‐studied adaptation for predation avoidance, in which a mimetic species resembles an unpalatable model species. Batesian mimicry can be under positive selection because of the protection gained against predators, due to resemblance to unpalatable model species. However, in some mimetic species, nonmimetic individuals are present in populations, despite the benefits of mimicry. The mechanism for evolution of such mimetic polymorphism remains an open question. Here, we address the hypothesis that the abundance of mimics is limited by that of the models, leading to mimetic polymorphism. In addition, other forces such as the effects of common ancestry and/or isolation by distance may explain this phenomenon. To investigate this question, we focused on the butterfly, Papilio polytes, that exhibits mimetic polymorphism on multiple islands of the Ryukyus, Japan, and performed field surveys and genetic analysis. We found that the mimic ratio of P. polytes was strongly correlated with the model abundance observed on each of the five islands, suggesting negative frequency‐dependent selection is driving the evolution of polymorphism in P. polytes populations. Molecular phylogenetic analysis indicated that the southern island populations are the major source of genetic diversity, and the middle and northern island populations arose by relatively recent migration. This view was also supported by mismatch distribution and Tajima's D analyses, suggesting a recent population expansion on the middle and northern islands, and stable population persistence on the southern islands. The frequency of the mimetic forms within P. polytes populations is thus explained by variations in the model abundance rather than by population structure. Thus, we propose that predation pressure, rather than neutral forces, have shaped the Batesian mimicry polymorphism in P. polytes observed in the Ryukyus. |
| first_indexed | 2024-12-14T22:05:43Z |
| format | Article |
| id | doaj.art-9d82cded188e4dfa808c31a4f161d6d4 |
| institution | Directory Open Access Journal |
| issn | 2045-7758 |
| language | English |
| last_indexed | 2024-12-14T22:05:43Z |
| publishDate | 2019-05-01 |
| publisher | Wiley |
| record_format | Article |
| series | Ecology and Evolution |
| spelling | doaj.art-9d82cded188e4dfa808c31a4f161d6d42022-12-21T22:45:52ZengWileyEcology and Evolution2045-77582019-05-019105991600210.1002/ece3.5182Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, JapanKaori Tsurui‐Sato0Yukuto Sato1Emi Kato2Mitsuho Katoh3Ryosuke Kimura4Haruki Tatsuta5Kazuki Tsuji6Center for Strategic Research Project University of the Ryukyus Okinawa JapanCenter for Strategic Research Project University of the Ryukyus Okinawa JapanDepartment of Agro‐Environmental Sciences, Faculty of Agriculture University of the Ryukyus Okinawa JapanDepartment of Agro‐Environmental Sciences, Faculty of Agriculture University of the Ryukyus Okinawa JapanDepartment of Human Biology and Anatomy, Graduate School of Medicine University of the Ryukyus Okinawa JapanDepartment of Agro‐Environmental Sciences, Faculty of Agriculture University of the Ryukyus Okinawa JapanDepartment of Agro‐Environmental Sciences, Faculty of Agriculture University of the Ryukyus Okinawa JapanAbstract Batesian mimicry is a well‐studied adaptation for predation avoidance, in which a mimetic species resembles an unpalatable model species. Batesian mimicry can be under positive selection because of the protection gained against predators, due to resemblance to unpalatable model species. However, in some mimetic species, nonmimetic individuals are present in populations, despite the benefits of mimicry. The mechanism for evolution of such mimetic polymorphism remains an open question. Here, we address the hypothesis that the abundance of mimics is limited by that of the models, leading to mimetic polymorphism. In addition, other forces such as the effects of common ancestry and/or isolation by distance may explain this phenomenon. To investigate this question, we focused on the butterfly, Papilio polytes, that exhibits mimetic polymorphism on multiple islands of the Ryukyus, Japan, and performed field surveys and genetic analysis. We found that the mimic ratio of P. polytes was strongly correlated with the model abundance observed on each of the five islands, suggesting negative frequency‐dependent selection is driving the evolution of polymorphism in P. polytes populations. Molecular phylogenetic analysis indicated that the southern island populations are the major source of genetic diversity, and the middle and northern island populations arose by relatively recent migration. This view was also supported by mismatch distribution and Tajima's D analyses, suggesting a recent population expansion on the middle and northern islands, and stable population persistence on the southern islands. The frequency of the mimetic forms within P. polytes populations is thus explained by variations in the model abundance rather than by population structure. Thus, we propose that predation pressure, rather than neutral forces, have shaped the Batesian mimicry polymorphism in P. polytes observed in the Ryukyus.https://doi.org/10.1002/ece3.5182female‐limited mimetic polymorphismmimic ratiomodel abundancephylogenetic analysespopulation genetics |
| spellingShingle | Kaori Tsurui‐Sato Yukuto Sato Emi Kato Mitsuho Katoh Ryosuke Kimura Haruki Tatsuta Kazuki Tsuji Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan Ecology and Evolution female‐limited mimetic polymorphism mimic ratio model abundance phylogenetic analyses population genetics |
| title | Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan |
| title_full | Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan |
| title_fullStr | Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan |
| title_full_unstemmed | Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan |
| title_short | Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan |
| title_sort | evidence for frequency dependent selection maintaining polymorphism in the batesian mimic papilio polytes in multiple islands in the ryukyus japan |
| topic | female‐limited mimetic polymorphism mimic ratio model abundance phylogenetic analyses population genetics |
| url | https://doi.org/10.1002/ece3.5182 |
| work_keys_str_mv | AT kaoritsuruisato evidenceforfrequencydependentselectionmaintainingpolymorphisminthebatesianmimicpapiliopolytesinmultipleislandsintheryukyusjapan AT yukutosato evidenceforfrequencydependentselectionmaintainingpolymorphisminthebatesianmimicpapiliopolytesinmultipleislandsintheryukyusjapan AT emikato evidenceforfrequencydependentselectionmaintainingpolymorphisminthebatesianmimicpapiliopolytesinmultipleislandsintheryukyusjapan AT mitsuhokatoh evidenceforfrequencydependentselectionmaintainingpolymorphisminthebatesianmimicpapiliopolytesinmultipleislandsintheryukyusjapan AT ryosukekimura evidenceforfrequencydependentselectionmaintainingpolymorphisminthebatesianmimicpapiliopolytesinmultipleislandsintheryukyusjapan AT harukitatsuta evidenceforfrequencydependentselectionmaintainingpolymorphisminthebatesianmimicpapiliopolytesinmultipleislandsintheryukyusjapan AT kazukitsuji evidenceforfrequencydependentselectionmaintainingpolymorphisminthebatesianmimicpapiliopolytesinmultipleislandsintheryukyusjapan |