Genomic signatures of divergent selection are associated with social behaviour for spinner dolphin ecotypes

Kimberly R. Andrews; Brendan Epstein; Matthew S. Leslie; Paul Fiedler; Phillip A. Morin; A. Rus Hoelzel

doi:10.1111/mec.15865

Genomic signatures of divergent selection are associated with social behaviour for spinner dolphin ecotypes

Kimberly R. Andrews, Brendan Epstein, Matthew S. Leslie, Paul Fiedler, Phillip A. Morin, A. Rus Hoelzel

Plant and Microbial Biology

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4 Scopus citations

Abstract

Understanding the genomic basis of adaptation is critical for understanding evolutionary processes and predicting how species will respond to environmental change. Spinner dolphins in the eastern tropical Pacific (ETP) present a unique system for studying adaptation. Within this large geographical region are four spinner dolphin ecotypes with weak neutral genetic divergence and no obvious barriers to gene flow, but strong spatial variation in morphology, behaviour and habitat. These ecotypes have large population sizes, which could reduce the effects of drift and facilitate selection. To identify genomic regions putatively under divergent selective pressures between ecotypes, we used genome scans with 8994 RADseq single nucleotide polymorphisms (SNPs) to identify population differentiation outliers and genotype–environment association outliers. Gene ontology enrichment analyses indicated that outlier SNPs from both types of analyses were associated with multiple genes involved in social behaviour and hippocampus development, including 15 genes associated with the human social disorder autism. Evidence for divergent selection on social behaviour is supported by previous evidence that these spinner dolphin ecotypes differ in mating systems and associated social behaviours. In particular, three of the ETP ecotypes probably have a polygynous mating system characterized by strong premating competition among males, whereas the fourth ecotype probably has a polygynandrous mating system characterized by strong postmating competition such as sperm competition. Our results provide evidence that selection for social behaviour may be an evolutionary force driving diversification of spinner dolphins in the ETP, potentially as a result of divergent sexual selection associated with different mating systems. Future studies should further investigate the potential adaptive role of the candidate genes identified here, and could probably find further signatures of selection using whole genome sequence data.

Original language	English (US)
Pages (from-to)	1993-2008
Number of pages	16
Journal	Molecular ecology
Volume	30
Issue number	9
DOIs	https://doi.org/10.1111/mec.15865
State	Published - May 2021

Bibliographical note

Funding Information:
We extend sincere thanks to the scientists who collected the specimens used in this study, including the National Marine Fisheries Service West Coast Region Observer Program; Tim Gerrodette, Karin Forney and Lisa Ballance from the Southwest Fisheries Science Center; and the Instituto Nacional De La Pesca. These collections provided archival biomaterial to answer questions never imagined possible during the sampling efforts. We also thank William F. Perrin for providing support and guidance, and the staff at the SWFSC Marine Mammal and Sea Turtle Research Collection for providing technical support for molecular laboratory work, including Gabriela Serra‐Valente, Victoria Pease, Kelly Robertson, Louella Dolar, Nicole Beaulieu and Morgane Lauf. We thank Brenna Forester for helpful comments on the manuscript. KRA was supported by a European Union Marie Curie International Incoming Fellowship.

Funding Information:
We extend sincere thanks to the scientists who collected the specimens used in this study, including the National Marine Fisheries Service West Coast Region Observer Program; Tim Gerrodette, Karin Forney and Lisa Ballance from the Southwest Fisheries Science Center; and the Instituto Nacional De La Pesca. These collections provided archival biomaterial to answer questions never imagined possible during the sampling efforts. We also thank William F. Perrin for providing support and guidance, and the staff at the SWFSC Marine Mammal and Sea Turtle Research Collection for providing technical support for molecular laboratory work, including Gabriela Serra-Valente, Victoria Pease, Kelly Robertson, Louella Dolar, Nicole Beaulieu and Morgane Lauf. We thank Brenna Forester for helpful comments on the manuscript. KRA was supported by a European Union Marie Curie International Incoming Fellowship.

Publisher Copyright:
© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Keywords

F outlier tests
Stenella longirostris
environmental association analysis
genome scan
genotype–environment association
mating system

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title = "Genomic signatures of divergent selection are associated with social behaviour for spinner dolphin ecotypes",

abstract = "Understanding the genomic basis of adaptation is critical for understanding evolutionary processes and predicting how species will respond to environmental change. Spinner dolphins in the eastern tropical Pacific (ETP) present a unique system for studying adaptation. Within this large geographical region are four spinner dolphin ecotypes with weak neutral genetic divergence and no obvious barriers to gene flow, but strong spatial variation in morphology, behaviour and habitat. These ecotypes have large population sizes, which could reduce the effects of drift and facilitate selection. To identify genomic regions putatively under divergent selective pressures between ecotypes, we used genome scans with 8994 RADseq single nucleotide polymorphisms (SNPs) to identify population differentiation outliers and genotype–environment association outliers. Gene ontology enrichment analyses indicated that outlier SNPs from both types of analyses were associated with multiple genes involved in social behaviour and hippocampus development, including 15 genes associated with the human social disorder autism. Evidence for divergent selection on social behaviour is supported by previous evidence that these spinner dolphin ecotypes differ in mating systems and associated social behaviours. In particular, three of the ETP ecotypes probably have a polygynous mating system characterized by strong premating competition among males, whereas the fourth ecotype probably has a polygynandrous mating system characterized by strong postmating competition such as sperm competition. Our results provide evidence that selection for social behaviour may be an evolutionary force driving diversification of spinner dolphins in the ETP, potentially as a result of divergent sexual selection associated with different mating systems. Future studies should further investigate the potential adaptive role of the candidate genes identified here, and could probably find further signatures of selection using whole genome sequence data.",

keywords = "F outlier tests, Stenella longirostris, environmental association analysis, genome scan, genotype–environment association, mating system",

author = "Andrews, {Kimberly R.} and Brendan Epstein and Leslie, {Matthew S.} and Paul Fiedler and Morin, {Phillip A.} and Hoelzel, {A. Rus}",

note = "Funding Information: We extend sincere thanks to the scientists who collected the specimens used in this study, including the National Marine Fisheries Service West Coast Region Observer Program; Tim Gerrodette, Karin Forney and Lisa Ballance from the Southwest Fisheries Science Center; and the Instituto Nacional De La Pesca. These collections provided archival biomaterial to answer questions never imagined possible during the sampling efforts. We also thank William F. Perrin for providing support and guidance, and the staff at the SWFSC Marine Mammal and Sea Turtle Research Collection for providing technical support for molecular laboratory work, including Gabriela Serra‐Valente, Victoria Pease, Kelly Robertson, Louella Dolar, Nicole Beaulieu and Morgane Lauf. We thank Brenna Forester for helpful comments on the manuscript. KRA was supported by a European Union Marie Curie International Incoming Fellowship. Funding Information: We extend sincere thanks to the scientists who collected the specimens used in this study, including the National Marine Fisheries Service West Coast Region Observer Program; Tim Gerrodette, Karin Forney and Lisa Ballance from the Southwest Fisheries Science Center; and the Instituto Nacional De La Pesca. These collections provided archival biomaterial to answer questions never imagined possible during the sampling efforts. We also thank William F. Perrin for providing support and guidance, and the staff at the SWFSC Marine Mammal and Sea Turtle Research Collection for providing technical support for molecular laboratory work, including Gabriela Serra-Valente, Victoria Pease, Kelly Robertson, Louella Dolar, Nicole Beaulieu and Morgane Lauf. We thank Brenna Forester for helpful comments on the manuscript. KRA was supported by a European Union Marie Curie International Incoming Fellowship. Publisher Copyright: {\textcopyright} 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.",

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N2 - Understanding the genomic basis of adaptation is critical for understanding evolutionary processes and predicting how species will respond to environmental change. Spinner dolphins in the eastern tropical Pacific (ETP) present a unique system for studying adaptation. Within this large geographical region are four spinner dolphin ecotypes with weak neutral genetic divergence and no obvious barriers to gene flow, but strong spatial variation in morphology, behaviour and habitat. These ecotypes have large population sizes, which could reduce the effects of drift and facilitate selection. To identify genomic regions putatively under divergent selective pressures between ecotypes, we used genome scans with 8994 RADseq single nucleotide polymorphisms (SNPs) to identify population differentiation outliers and genotype–environment association outliers. Gene ontology enrichment analyses indicated that outlier SNPs from both types of analyses were associated with multiple genes involved in social behaviour and hippocampus development, including 15 genes associated with the human social disorder autism. Evidence for divergent selection on social behaviour is supported by previous evidence that these spinner dolphin ecotypes differ in mating systems and associated social behaviours. In particular, three of the ETP ecotypes probably have a polygynous mating system characterized by strong premating competition among males, whereas the fourth ecotype probably has a polygynandrous mating system characterized by strong postmating competition such as sperm competition. Our results provide evidence that selection for social behaviour may be an evolutionary force driving diversification of spinner dolphins in the ETP, potentially as a result of divergent sexual selection associated with different mating systems. Future studies should further investigate the potential adaptive role of the candidate genes identified here, and could probably find further signatures of selection using whole genome sequence data.

AB - Understanding the genomic basis of adaptation is critical for understanding evolutionary processes and predicting how species will respond to environmental change. Spinner dolphins in the eastern tropical Pacific (ETP) present a unique system for studying adaptation. Within this large geographical region are four spinner dolphin ecotypes with weak neutral genetic divergence and no obvious barriers to gene flow, but strong spatial variation in morphology, behaviour and habitat. These ecotypes have large population sizes, which could reduce the effects of drift and facilitate selection. To identify genomic regions putatively under divergent selective pressures between ecotypes, we used genome scans with 8994 RADseq single nucleotide polymorphisms (SNPs) to identify population differentiation outliers and genotype–environment association outliers. Gene ontology enrichment analyses indicated that outlier SNPs from both types of analyses were associated with multiple genes involved in social behaviour and hippocampus development, including 15 genes associated with the human social disorder autism. Evidence for divergent selection on social behaviour is supported by previous evidence that these spinner dolphin ecotypes differ in mating systems and associated social behaviours. In particular, three of the ETP ecotypes probably have a polygynous mating system characterized by strong premating competition among males, whereas the fourth ecotype probably has a polygynandrous mating system characterized by strong postmating competition such as sperm competition. Our results provide evidence that selection for social behaviour may be an evolutionary force driving diversification of spinner dolphins in the ETP, potentially as a result of divergent sexual selection associated with different mating systems. Future studies should further investigate the potential adaptive role of the candidate genes identified here, and could probably find further signatures of selection using whole genome sequence data.

KW - F outlier tests

KW - Stenella longirostris

KW - environmental association analysis

KW - genome scan

KW - genotype–environment association

KW - mating system

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JO - Molecular ecology

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Genomic signatures of divergent selection are associated with social behaviour for spinner dolphin ecotypes

Abstract

Bibliographical note

Keywords

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