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Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species
Insular organisms often evolve predictable phenotypes, like flightlessness, extreme body sizes, or increased melanin deposition. The evolutionary forces and molecular targets mediating these patterns remain mostly unknown. Here we study the Chestnut-bellied Monarch (Monarcha castaneiventris) from th...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9624418/ https://www.ncbi.nlm.nih.gov/pubmed/36318577 http://dx.doi.org/10.1371/journal.pgen.1010474 |
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author | Campagna, Leonardo Mo, Ziyi Siepel, Adam Uy, J. Albert C. |
author_facet | Campagna, Leonardo Mo, Ziyi Siepel, Adam Uy, J. Albert C. |
author_sort | Campagna, Leonardo |
collection | PubMed |
description | Insular organisms often evolve predictable phenotypes, like flightlessness, extreme body sizes, or increased melanin deposition. The evolutionary forces and molecular targets mediating these patterns remain mostly unknown. Here we study the Chestnut-bellied Monarch (Monarcha castaneiventris) from the Solomon Islands, a complex of closely related subspecies in the early stages of speciation. On the large island of Makira M. c. megarhynchus has a chestnut belly, whereas on the small satellite islands of Ugi, and Santa Ana and Santa Catalina (SA/SC) M. c. ugiensis is entirely iridescent blue-black (i.e., melanic). Melanism has likely evolved twice, as the Ugi and SA/SC populations were established independently. To investigate the genetic basis of melanism on each island we generated whole genome sequence data from all three populations. Non-synonymous mutations at the MC1R pigmentation gene are associated with melanism on SA/SC, while ASIP, an antagonistic ligand of MC1R, is associated with melanism on Ugi. Both genes show evidence of selective sweeps in traditional summary statistics and statistics derived from the ancestral recombination graph (ARG). Using the ARG in combination with machine learning, we inferred selection strength, timing of onset and allele frequency trajectories. MC1R shows evidence of a recent, strong, soft selective sweep. The region including ASIP shows more complex signatures; however, we find evidence for sweeps in mutations near ASIP, which are comparatively older than those on MC1R and have been under relatively strong selection. Overall, our study shows convergent melanism results from selective sweeps at independent molecular targets, evolving in taxa where coloration likely mediates reproductive isolation with the neighboring chestnut-bellied subspecies. |
format | Online Article Text |
id | pubmed-9624418 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-96244182022-11-02 Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species Campagna, Leonardo Mo, Ziyi Siepel, Adam Uy, J. Albert C. PLoS Genet Research Article Insular organisms often evolve predictable phenotypes, like flightlessness, extreme body sizes, or increased melanin deposition. The evolutionary forces and molecular targets mediating these patterns remain mostly unknown. Here we study the Chestnut-bellied Monarch (Monarcha castaneiventris) from the Solomon Islands, a complex of closely related subspecies in the early stages of speciation. On the large island of Makira M. c. megarhynchus has a chestnut belly, whereas on the small satellite islands of Ugi, and Santa Ana and Santa Catalina (SA/SC) M. c. ugiensis is entirely iridescent blue-black (i.e., melanic). Melanism has likely evolved twice, as the Ugi and SA/SC populations were established independently. To investigate the genetic basis of melanism on each island we generated whole genome sequence data from all three populations. Non-synonymous mutations at the MC1R pigmentation gene are associated with melanism on SA/SC, while ASIP, an antagonistic ligand of MC1R, is associated with melanism on Ugi. Both genes show evidence of selective sweeps in traditional summary statistics and statistics derived from the ancestral recombination graph (ARG). Using the ARG in combination with machine learning, we inferred selection strength, timing of onset and allele frequency trajectories. MC1R shows evidence of a recent, strong, soft selective sweep. The region including ASIP shows more complex signatures; however, we find evidence for sweeps in mutations near ASIP, which are comparatively older than those on MC1R and have been under relatively strong selection. Overall, our study shows convergent melanism results from selective sweeps at independent molecular targets, evolving in taxa where coloration likely mediates reproductive isolation with the neighboring chestnut-bellied subspecies. Public Library of Science 2022-11-01 /pmc/articles/PMC9624418/ /pubmed/36318577 http://dx.doi.org/10.1371/journal.pgen.1010474 Text en © 2022 Campagna et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Campagna, Leonardo Mo, Ziyi Siepel, Adam Uy, J. Albert C. Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species |
title | Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species |
title_full | Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species |
title_fullStr | Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species |
title_full_unstemmed | Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species |
title_short | Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species |
title_sort | selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9624418/ https://www.ncbi.nlm.nih.gov/pubmed/36318577 http://dx.doi.org/10.1371/journal.pgen.1010474 |
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