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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...

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Autores principales: Campagna, Leonardo, Mo, Ziyi, Siepel, Adam, Uy, J. Albert C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
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.
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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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