The roles of vicariance and isolation by distance in shaping biotic diversification across an ancient archipelago: evidence from a Seychelles caecilian amphibian.


Journal

BMC evolutionary biology
ISSN: 1471-2148
Titre abrégé: BMC Evol Biol
Pays: England
ID NLM: 100966975

Informations de publication

Date de publication:
26 08 2020
Historique:
received: 07 04 2020
accepted: 12 08 2020
entrez: 28 8 2020
pubmed: 28 8 2020
medline: 13 11 2020
Statut: epublish

Résumé

Island systems offer excellent opportunities for studying the evolutionary histories of species by virtue of their restricted size and easily identifiable barriers to gene flow. However, most studies investigating evolutionary patterns and processes shaping biotic diversification have focused on more recent (emergent) rather than ancient oceanic archipelagos. Here, we focus on the granitic islands of the Seychelles, which are unusual among island systems because they have been isolated for a long time and are home to a monophyletic radiation of caecilian amphibians that has been separated from its extant sister lineage for ca. 65-62 Ma. We selected the most widespread Seychelles caecilian species, Hypogeophis rostratus, to investigate intraspecific morphological and genetic (mitochondrial and nuclear) variation across the archipelago (782 samples from nine islands) to identify patterns and test processes that shaped their evolutionary history within the Seychelles. Overall a signal of strong geographic structuring with distinct northern- and southern-island clusters were identified across all datasets. We suggest that these distinct groups have been isolated for ca. 1.26 Ma years without subsequent migration between them. Populations from the somewhat geographically isolated island of Frégate showed contrasting relationships to other islands based on genetic and morphological data, clustering alternatively with northern-island (genetic) and southern-island (morphological) populations. Although variation in H. rostratus across the Seychelles is explained more by isolation-by-distance than by adaptation, the genetic-morphological incongruence for affinities of Frégate H. rostratus might be caused by local adaptation over-riding the signal from their vicariant history. Our findings highlight the need of integrative approaches to investigate fine-scale geographic structuring to uncover underlying diversity and to better understand evolutionary processes on ancient, continental islands.

Sections du résumé

BACKGROUND
Island systems offer excellent opportunities for studying the evolutionary histories of species by virtue of their restricted size and easily identifiable barriers to gene flow. However, most studies investigating evolutionary patterns and processes shaping biotic diversification have focused on more recent (emergent) rather than ancient oceanic archipelagos. Here, we focus on the granitic islands of the Seychelles, which are unusual among island systems because they have been isolated for a long time and are home to a monophyletic radiation of caecilian amphibians that has been separated from its extant sister lineage for ca. 65-62 Ma. We selected the most widespread Seychelles caecilian species, Hypogeophis rostratus, to investigate intraspecific morphological and genetic (mitochondrial and nuclear) variation across the archipelago (782 samples from nine islands) to identify patterns and test processes that shaped their evolutionary history within the Seychelles.
RESULTS
Overall a signal of strong geographic structuring with distinct northern- and southern-island clusters were identified across all datasets. We suggest that these distinct groups have been isolated for ca. 1.26 Ma years without subsequent migration between them. Populations from the somewhat geographically isolated island of Frégate showed contrasting relationships to other islands based on genetic and morphological data, clustering alternatively with northern-island (genetic) and southern-island (morphological) populations.
CONCLUSIONS
Although variation in H. rostratus across the Seychelles is explained more by isolation-by-distance than by adaptation, the genetic-morphological incongruence for affinities of Frégate H. rostratus might be caused by local adaptation over-riding the signal from their vicariant history. Our findings highlight the need of integrative approaches to investigate fine-scale geographic structuring to uncover underlying diversity and to better understand evolutionary processes on ancient, continental islands.

Identifiants

pubmed: 32847507
doi: 10.1186/s12862-020-01673-w
pii: 10.1186/s12862-020-01673-w
pmc: PMC7448330
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

110

Subventions

Organisme : National Geographic
ID : 1743
Pays : International
Organisme : Biotechnology and Biological Sciences Research Council
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : P20 GM103408
Pays : United States
Organisme : National Science Foundation
ID : BSR 88-17453
Pays : International
Organisme : National Geographic
ID : 1633
Pays : International
Organisme : Darwin Initiative
ID : 19-002
Pays : International
Organisme : National Science Foundation
ID : BSR 90-24505
Pays : International

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Auteurs

Simon T Maddock (ST)

Present address: Faculty of Science and Engineering, University of Wolverhampton, Wolverhampton, WV1 1LY, UK. s.t.maddock@gmail.com.
Department of Life Sciences, The Natural History Museum, London, SW7 5BD, UK. s.t.maddock@gmail.com.
Department of Genetics, Evolution and Environment, University College London, WC1E 6BT, London, UK. s.t.maddock@gmail.com.
Island Biodiversity and Conservation Centre, University of Seychelles, Mahé, Seychelles. s.t.maddock@gmail.com.

Ronald A Nussbaum (RA)

Research Museums Center, University of Michigan, Ann Arbor, MI, 48108, USA.

Julia J Day (JJ)

Department of Genetics, Evolution and Environment, University College London, WC1E 6BT, London, UK.

Leigh Latta (L)

Division of Natural Sciences and Mathematics, Lewis-Clark State College, Lewiston, ID, 83501, USA.

Mark Miller (M)

Department of Biology, Utah State University, Logan, UT, 84322, USA.

Debra L Fisk (DL)

McPherson Eye Research Institute, University of Wisconsin, Madison, WI, 53705, USA.

Mark Wilkinson (M)

Department of Life Sciences, The Natural History Museum, London, SW7 5BD, UK.

Sara Rocha (S)

Biomedical Research Center (CINBIO), University of Vigo, Vigo, Spain.
Galicia Sur Health Research Institute, Vigo, Spain.

David J Gower (DJ)

Department of Life Sciences, The Natural History Museum, London, SW7 5BD, UK.

Michael E Pfrender (ME)

Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, 46556, USA.

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