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Asymmetric reproductive isolation between terminal forms of the salamander ring species Ensatina eschscholtzii revealed by fine-scale genetic analysis of a hybrid zone

Devitt, Thomas J; Baird, Stuart JE; Moritz, Craig

Description

BACKGROUND Ring species, exemplified by salamanders of the Ensatina eschscholtzii complex, represent a special window into the speciation process because they allow the history of species formation to be traced back in time through the geographically differentiated forms connecting the two terminal forms of the ring. Of particular interest is the nature and extent of reproductive isolation between the geographically terminal forms, in this case E. e. eschscholtzii and E. e. klauberi. Previous...[Show more]

dc.contributor.authorDevitt, Thomas J
dc.contributor.authorBaird, Stuart JE
dc.contributor.authorMoritz, Craig
dc.date.accessioned2015-12-03T04:32:08Z
dc.date.available2015-12-03T04:32:08Z
dc.identifier.issn1471-2148
dc.identifier.urihttp://hdl.handle.net/1885/17003
dc.description.abstractBACKGROUND Ring species, exemplified by salamanders of the Ensatina eschscholtzii complex, represent a special window into the speciation process because they allow the history of species formation to be traced back in time through the geographically differentiated forms connecting the two terminal forms of the ring. Of particular interest is the nature and extent of reproductive isolation between the geographically terminal forms, in this case E. e. eschscholtzii and E. e. klauberi. Previous studies have documented infrequent hybridization at the end of the ring. Here, we report the first fine-scale genetic analysis of a hybrid zone between the terminal forms in southern California using individual-based Bayesian analyses of multilocus genetic data to estimate levels and direction of hybridization and maximum-likelihood analysis of linkage disequilibrium and cline shape to make inferences about migration and selection in the hybrid zone. RESULTS The center of the hybrid zone has a high proportion of hybrids, about half of which were classified as F1s. Clines are narrow with respect to dispersal, and there are significant deviations from Hardy-Weinberg equilibrium as well as nonrandom associations (linkage disequilibria) between alleles characteristic of each parental type. There is cytonuclear discordance, both in terms of introgression and the geographic position of mitochondrial versus nuclear clines. Genetic disequilibrium is concentrated on the eschscholtzii side of the zone. Nearly all hybrids possess klauberi mtDNA, indicating that most hybrids are formed from female klauberi mating with male eschscholtzii or male hybrids (but not vice versa). CONCLUSIONS Our results are consistent with a tension zone trapped at an ecotone, with gene combinations characteristic of klauberi showing up on the eschscholtzii side of the zone due to asymmetric hybridization. We suggest that the observed asymmetry is best explained by increased discriminatory power of eschscholtzii females, or asymmetric postzygotic isolation. The relatively high frequency of hybrids, particularly F1s, contrasts with other contacts between the terminal forms, and with other contacts between other divergent Ensatina lineages, highlighting the diverse outcomes of secondary contact within a single species complex.
dc.description.sponsorshipFunding for this work was provided by Sigma Xi, the National Science Foundation (Doctoral Dissertation Improvement Grant DEB-0909821 to TJD and NSF DEB-0641078 to CM), the University of California Department of Integrative Biology, and the Museum of Vertebrate Zoology Martens and Louise Kellogg funds.
dc.formathttp://bmcevolbiol.biomedcentral.com/
dc.publisherBioMed Central
dc.rights© Devitt et al; licensee BioMed Central Ltd. 2011. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://​creativecommons.​org/​licenses/​by/​2.​0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
dc.sourceBMC Evolutionary Biology
dc.source.urihttp://bmcevolbiol.biomedcentral.com/articles/10.1186/1471-2148-11-245
dc.subjectanimals
dc.subjectbase sequence
dc.subjectbayes theorem
dc.subjectcalifornia
dc.subjectecosystem
dc.subjectfemale
dc.subjectlikelihood functions
dc.subjectlinkage disequilibrium
dc.subjectmale
dc.subjectmodels, genetic
dc.subjectmolecular sequence data
dc.subjectreproduction
dc.subjectsequence alignment
dc.subjectsequence analysis, dna
dc.subjectsex factors
dc.subjecturodela
dc.subjectdemography
dc.subjectgenetic speciation
dc.subjecthybridization, genetic
dc.titleAsymmetric reproductive isolation between terminal forms of the salamander ring species Ensatina eschscholtzii revealed by fine-scale genetic analysis of a hybrid zone
dc.typeJournal article
local.description.notesImported from ARIES
local.identifier.citationvolume11
dc.date.issued2011-08-22
local.identifier.absfor060300
local.identifier.ariespublicationf5625xPUB7383
local.type.statusPublished Version
local.contributor.affiliationDevitt, Thomas J., University of California, United States of America
local.contributor.affiliationBaird, Stuart J.E., University of Porto, Portugal
local.contributor.affiliationMoritz, Craig, College of Medicine, Biology and Environment, CMBE Research School of Biology, Division of Evolution, Ecology & Genetics, The Australian National University
local.identifier.essn1471-2148
local.bibliographicCitation.issue1
local.bibliographicCitation.startpage245
local.bibliographicCitation.lastpage14
local.identifier.doi10.1186/1471-2148-11-245
dc.date.updated2015-12-11T10:05:32Z
local.identifier.scopusID2-s2.0-80052027937
local.identifier.thomsonID000294952500001
CollectionsANU Research Publications

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