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Integrative Taxonomy Recognizes Evolutionary Units Despite Widespread Mitonuclear Discordance : Evidence from a Rotifer Cryptic Species Complex

Papakostas, Spiros; Michaloudi, Evangelia; Proios, Konstantinos; Brehm, Michaela; Verhage, Laurens; Rota, Jadranka LU ; Peña, Carlos; Stamou, Georgia; Pritchard, Victoria L and Fontaneto, Diego, et al. (2016) In Systematic Biology 65(3). p.24-508
Abstract

Mitonuclear discordance across taxa is increasingly recognized as posing a major challenge to species delimitation based on DNA sequence data. Integrative taxonomy has been proposed as a promising framework to help address this problem. However, we still lack compelling empirical evidence scrutinizing the efficacy of integrative taxonomy in relation to, for instance, complex introgression scenarios involving many species. Here, we report remarkably widespread mitonuclear discordance between about 15 mitochondrial and 4 nuclear Brachionus calyciflorus groups identified using different species delimitation approaches. Using coalescent-, Bayesian admixture-, and allele sharing-based methods with DNA sequence or microsatellite data, we... (More)

Mitonuclear discordance across taxa is increasingly recognized as posing a major challenge to species delimitation based on DNA sequence data. Integrative taxonomy has been proposed as a promising framework to help address this problem. However, we still lack compelling empirical evidence scrutinizing the efficacy of integrative taxonomy in relation to, for instance, complex introgression scenarios involving many species. Here, we report remarkably widespread mitonuclear discordance between about 15 mitochondrial and 4 nuclear Brachionus calyciflorus groups identified using different species delimitation approaches. Using coalescent-, Bayesian admixture-, and allele sharing-based methods with DNA sequence or microsatellite data, we provide strong evidence in support of hybridization as a driver of the observed discordance. We then describe our combined molecular, morphological, and ecological approaches to resolving phylogenetic conflict and inferring species boundaries. Species delimitations based on the ITS1 and 28S nuclear DNA markers proved a more reliable predictor of morphological variation than delimitations using the mitochondrial COI gene. A short-term competition experiment further revealed systematic differences in the competitive ability between two of the nuclear-delimited species under six different growth conditions, independent of COI delimitations; hybrids were also observed. In light of these findings, we discuss the failure of the COI marker to estimate morphological stasis and morphological plasticity in the B. calyciflorus complex. By using B. calyciflorus as a representative case, we demonstrate the potential of integrative taxonomy to guide species delimitation in the presence of mitonuclear phylogenetic conflicts.

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publication status
published
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keywords
18S and 28S ribosomal RNA genes, cyclical parthenogens, cytochrome c oxidase subunit I, DNA barcoding, GMYC, haploweb, internal transcribed spacer I, reticulate evolution
in
Systematic Biology
volume
65
issue
3
pages
17 pages
publisher
Oxford University Press
external identifiers
  • scopus:84978829373
  • wos:000375210300012
ISSN
1063-5157
DOI
10.1093/sysbio/syw016
language
English
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no
id
179bf43b-bd6f-4cd7-958c-41b5db7d3d0f
date added to LUP
2016-10-21 11:59:13
date last changed
2017-11-19 04:34:05
@article{179bf43b-bd6f-4cd7-958c-41b5db7d3d0f,
  abstract     = {<p>Mitonuclear discordance across taxa is increasingly recognized as posing a major challenge to species delimitation based on DNA sequence data. Integrative taxonomy has been proposed as a promising framework to help address this problem. However, we still lack compelling empirical evidence scrutinizing the efficacy of integrative taxonomy in relation to, for instance, complex introgression scenarios involving many species. Here, we report remarkably widespread mitonuclear discordance between about 15 mitochondrial and 4 nuclear Brachionus calyciflorus groups identified using different species delimitation approaches. Using coalescent-, Bayesian admixture-, and allele sharing-based methods with DNA sequence or microsatellite data, we provide strong evidence in support of hybridization as a driver of the observed discordance. We then describe our combined molecular, morphological, and ecological approaches to resolving phylogenetic conflict and inferring species boundaries. Species delimitations based on the ITS1 and 28S nuclear DNA markers proved a more reliable predictor of morphological variation than delimitations using the mitochondrial COI gene. A short-term competition experiment further revealed systematic differences in the competitive ability between two of the nuclear-delimited species under six different growth conditions, independent of COI delimitations; hybrids were also observed. In light of these findings, we discuss the failure of the COI marker to estimate morphological stasis and morphological plasticity in the B. calyciflorus complex. By using B. calyciflorus as a representative case, we demonstrate the potential of integrative taxonomy to guide species delimitation in the presence of mitonuclear phylogenetic conflicts.</p>},
  author       = {Papakostas, Spiros and Michaloudi, Evangelia and Proios, Konstantinos and Brehm, Michaela and Verhage, Laurens and Rota, Jadranka and Peña, Carlos and Stamou, Georgia and Pritchard, Victoria L and Fontaneto, Diego and Declerck, Steven A J},
  issn         = {1063-5157},
  keyword      = {18S and 28S ribosomal RNA genes,cyclical parthenogens,cytochrome c oxidase subunit I,DNA barcoding,GMYC,haploweb,internal transcribed spacer I,reticulate evolution},
  language     = {eng},
  number       = {3},
  pages        = {24--508},
  publisher    = {Oxford University Press},
  series       = {Systematic Biology},
  title        = {Integrative Taxonomy Recognizes Evolutionary Units Despite Widespread Mitonuclear Discordance : Evidence from a Rotifer Cryptic Species Complex},
  url          = {http://dx.doi.org/10.1093/sysbio/syw016},
  volume       = {65},
  year         = {2016},
}