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The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs
BACKGROUND: In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histories co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus. The most divergent, S. perrico, separated from...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7853319/ https://www.ncbi.nlm.nih.gov/pubmed/33514314 http://dx.doi.org/10.1186/s12862-020-01731-3 |
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author | Carlon, David B. Robertson, D. Ross Barron, Robert L. Choat, John Howard Anderson, David J. Schwartz, Sonja A. Sánchez-Ortiz, Carlos A. |
author_facet | Carlon, David B. Robertson, D. Ross Barron, Robert L. Choat, John Howard Anderson, David J. Schwartz, Sonja A. Sánchez-Ortiz, Carlos A. |
author_sort | Carlon, David B. |
collection | PubMed |
description | BACKGROUND: In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histories co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus. The most divergent, S. perrico, separated from a Central Indo-Pacific ancestor in the late Miocene (6.6 Ma). We tested the hypothesis that S. compressus was the result of ongoing hybridization among the other three species by sequencing four nuclear markers and a mitochondrial locus in samples spanning 2/3 of the latitudinal extent of the TEP. RESULTS: A Structure model indicated that K = 3 fit the nuclear data and that S. compressus individuals had admixed genomes. Our data could correctly detect and assign pure adults and F1 hybrids with > 0.90 probability, and correct assignment of F2s was also high in some cases. NewHybrids models revealed that 89.8% (n = 59) of the S. compressus samples were F1 hybrids between either S. perrico × S. ghobban or S. perrico × S. rubroviolaceus. Similarly, the most recently diverged S. ghobban and S. rubroviolaceus were hybridizing in small numbers, with half of the admixed individuals assigned to F1 hybrids and the remainder likely > F1 hybrids. We observed strong mito-nuclear discordance in all hybrid pairs. Migrate models favored gene flow between S. perrico and S. ghobban, but not other species pairs. CONCLUSIONS: Mating between divergent species is giving rise to a region-wide, multispecies hybrid complex, characterized by a high frequency of parental and F1 genotypes but a low frequency of > F1 hybrids. Trimodal structure, and evidence for fertility of both male and female F1 hybrids, suggest that fitness declines sharply in later generation hybrids. In contrast, the hybrid population of the two more recently diverged species had similar frequencies of F1 and > F1 hybrids, suggesting accelerating post-mating incompatibility with time. Mitochondrial genotypes in hybrids suggest that indiscriminate mating by male S. perrico is driving pre-zygotic breakdown, which may reflect isolation of this endemic species for millions of years resulting in weak selection for conspecific mate recognition. Despite overlapping habitat use and high rates of hybridization, species boundaries are maintained by a combination of pre- and post-mating processes in this complex. |
format | Online Article Text |
id | pubmed-7853319 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-78533192021-02-09 The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs Carlon, David B. Robertson, D. Ross Barron, Robert L. Choat, John Howard Anderson, David J. Schwartz, Sonja A. Sánchez-Ortiz, Carlos A. BMC Ecol Evol Research Article BACKGROUND: In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histories co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus. The most divergent, S. perrico, separated from a Central Indo-Pacific ancestor in the late Miocene (6.6 Ma). We tested the hypothesis that S. compressus was the result of ongoing hybridization among the other three species by sequencing four nuclear markers and a mitochondrial locus in samples spanning 2/3 of the latitudinal extent of the TEP. RESULTS: A Structure model indicated that K = 3 fit the nuclear data and that S. compressus individuals had admixed genomes. Our data could correctly detect and assign pure adults and F1 hybrids with > 0.90 probability, and correct assignment of F2s was also high in some cases. NewHybrids models revealed that 89.8% (n = 59) of the S. compressus samples were F1 hybrids between either S. perrico × S. ghobban or S. perrico × S. rubroviolaceus. Similarly, the most recently diverged S. ghobban and S. rubroviolaceus were hybridizing in small numbers, with half of the admixed individuals assigned to F1 hybrids and the remainder likely > F1 hybrids. We observed strong mito-nuclear discordance in all hybrid pairs. Migrate models favored gene flow between S. perrico and S. ghobban, but not other species pairs. CONCLUSIONS: Mating between divergent species is giving rise to a region-wide, multispecies hybrid complex, characterized by a high frequency of parental and F1 genotypes but a low frequency of > F1 hybrids. Trimodal structure, and evidence for fertility of both male and female F1 hybrids, suggest that fitness declines sharply in later generation hybrids. In contrast, the hybrid population of the two more recently diverged species had similar frequencies of F1 and > F1 hybrids, suggesting accelerating post-mating incompatibility with time. Mitochondrial genotypes in hybrids suggest that indiscriminate mating by male S. perrico is driving pre-zygotic breakdown, which may reflect isolation of this endemic species for millions of years resulting in weak selection for conspecific mate recognition. Despite overlapping habitat use and high rates of hybridization, species boundaries are maintained by a combination of pre- and post-mating processes in this complex. BioMed Central 2021-01-21 /pmc/articles/PMC7853319/ /pubmed/33514314 http://dx.doi.org/10.1186/s12862-020-01731-3 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Carlon, David B. Robertson, D. Ross Barron, Robert L. Choat, John Howard Anderson, David J. Schwartz, Sonja A. Sánchez-Ortiz, Carlos A. The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs |
title | The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs |
title_full | The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs |
title_fullStr | The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs |
title_full_unstemmed | The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs |
title_short | The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs |
title_sort | origin of the parrotfish species scarus compressus in the tropical eastern pacific: region-wide hybridization between ancient species pairs |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7853319/ https://www.ncbi.nlm.nih.gov/pubmed/33514314 http://dx.doi.org/10.1186/s12862-020-01731-3 |
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