Cargando…

Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus

BACKGROUND: There is increasing recognition of the concordance between marine biogeographic and phylogeographic boundaries. However, it is still unclear how population-level divergence translates into species-level divergence, and what are the principal factors that first initiate that divergence, a...

Descripción completa

Detalles Bibliográficos
Autores principales: Farhadi, Ahmad, Jeffs, Andrew G., Farahmand, Hamid, Rejiniemon, Thankappan Sarasam, Smith, Greg, Lavery, Shane D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5563042/
https://www.ncbi.nlm.nih.gov/pubmed/28821229
http://dx.doi.org/10.1186/s12862-017-1050-8
_version_ 1783258063181971456
author Farhadi, Ahmad
Jeffs, Andrew G.
Farahmand, Hamid
Rejiniemon, Thankappan Sarasam
Smith, Greg
Lavery, Shane D.
author_facet Farhadi, Ahmad
Jeffs, Andrew G.
Farahmand, Hamid
Rejiniemon, Thankappan Sarasam
Smith, Greg
Lavery, Shane D.
author_sort Farhadi, Ahmad
collection PubMed
description BACKGROUND: There is increasing recognition of the concordance between marine biogeographic and phylogeographic boundaries. However, it is still unclear how population-level divergence translates into species-level divergence, and what are the principal factors that first initiate that divergence, and then maintain reproductive isolation. This study examines the likely forces driving population and lineage divergences in the broadly-distributed Indo-Pacific spiny lobster Panulirus homarus, which has peripheral divergent lineages in the west and east. The study focuses particularly on the West Indian Ocean, which is emerging as a region of unexpected diversity. Mitochondrial control region (mtCR) and COI sequences as well as genotypes of 9 microsatellite loci were examined in 410 individuals from 17 locations grouped into 7 regions from South Africa in the west, and eastward across to Taiwan and the Marquesas Islands. Phylogenetic and population-level analyses were used to test the significance and timing of divergences and describe the genetic relationships among populations. RESULTS: Analyses of the mtCR revealed high levels of divergence among the seven regions (Ф(ST) = 0.594, P < 0.001). Microsatellite analyses also revealed significant divergence among regions, but at a much lower level (F(ST) = 0.066, P < 0.001). The results reveal different patterns of mtCR v. nDNA divergence between the two distinct peripheral lineages: a subspecies in South Africa and Madagascar, and a phylogeographically diverged population in the Marquesas. The results also expose a number of other more fine-scale population divergences, particularly in the Indian Ocean. CONCLUSIONS: The divergence of peripheral lineages in the west and east of the species’ range appear to have been initiated and maintained by very different processes. The pattern of mitochondrial and nuclear divergence of the western lineage, implicates processes of parapatric isolation, secondary contact and introgression, and suggests possible maintenance through adaptation and behavioural reproductive isolation. In contrast, the eastern lineage appears to have diverged through a rare colonisation event, maintained through long-term isolation, and matches expectations of the core-periphery hypothesis. The process of active peripheral speciation may be a common force in the Indo-Pacific that helps drive some of the regions’ recognized biogeographic boundaries. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-1050-8) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5563042
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-55630422017-08-21 Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus Farhadi, Ahmad Jeffs, Andrew G. Farahmand, Hamid Rejiniemon, Thankappan Sarasam Smith, Greg Lavery, Shane D. BMC Evol Biol Research Article BACKGROUND: There is increasing recognition of the concordance between marine biogeographic and phylogeographic boundaries. However, it is still unclear how population-level divergence translates into species-level divergence, and what are the principal factors that first initiate that divergence, and then maintain reproductive isolation. This study examines the likely forces driving population and lineage divergences in the broadly-distributed Indo-Pacific spiny lobster Panulirus homarus, which has peripheral divergent lineages in the west and east. The study focuses particularly on the West Indian Ocean, which is emerging as a region of unexpected diversity. Mitochondrial control region (mtCR) and COI sequences as well as genotypes of 9 microsatellite loci were examined in 410 individuals from 17 locations grouped into 7 regions from South Africa in the west, and eastward across to Taiwan and the Marquesas Islands. Phylogenetic and population-level analyses were used to test the significance and timing of divergences and describe the genetic relationships among populations. RESULTS: Analyses of the mtCR revealed high levels of divergence among the seven regions (Ф(ST) = 0.594, P < 0.001). Microsatellite analyses also revealed significant divergence among regions, but at a much lower level (F(ST) = 0.066, P < 0.001). The results reveal different patterns of mtCR v. nDNA divergence between the two distinct peripheral lineages: a subspecies in South Africa and Madagascar, and a phylogeographically diverged population in the Marquesas. The results also expose a number of other more fine-scale population divergences, particularly in the Indian Ocean. CONCLUSIONS: The divergence of peripheral lineages in the west and east of the species’ range appear to have been initiated and maintained by very different processes. The pattern of mitochondrial and nuclear divergence of the western lineage, implicates processes of parapatric isolation, secondary contact and introgression, and suggests possible maintenance through adaptation and behavioural reproductive isolation. In contrast, the eastern lineage appears to have diverged through a rare colonisation event, maintained through long-term isolation, and matches expectations of the core-periphery hypothesis. The process of active peripheral speciation may be a common force in the Indo-Pacific that helps drive some of the regions’ recognized biogeographic boundaries. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-1050-8) contains supplementary material, which is available to authorized users. BioMed Central 2017-08-18 /pmc/articles/PMC5563042/ /pubmed/28821229 http://dx.doi.org/10.1186/s12862-017-1050-8 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research Article
Farhadi, Ahmad
Jeffs, Andrew G.
Farahmand, Hamid
Rejiniemon, Thankappan Sarasam
Smith, Greg
Lavery, Shane D.
Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus
title Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus
title_full Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus
title_fullStr Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus
title_full_unstemmed Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus
title_short Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus
title_sort mechanisms of peripheral phylogeographic divergence in the indo-pacific: lessons from the spiny lobster panulirus homarus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5563042/
https://www.ncbi.nlm.nih.gov/pubmed/28821229
http://dx.doi.org/10.1186/s12862-017-1050-8
work_keys_str_mv AT farhadiahmad mechanismsofperipheralphylogeographicdivergenceintheindopacificlessonsfromthespinylobsterpanulirushomarus
AT jeffsandrewg mechanismsofperipheralphylogeographicdivergenceintheindopacificlessonsfromthespinylobsterpanulirushomarus
AT farahmandhamid mechanismsofperipheralphylogeographicdivergenceintheindopacificlessonsfromthespinylobsterpanulirushomarus
AT rejiniemonthankappansarasam mechanismsofperipheralphylogeographicdivergenceintheindopacificlessonsfromthespinylobsterpanulirushomarus
AT smithgreg mechanismsofperipheralphylogeographicdivergenceintheindopacificlessonsfromthespinylobsterpanulirushomarus
AT laveryshaned mechanismsofperipheralphylogeographicdivergenceintheindopacificlessonsfromthespinylobsterpanulirushomarus