Multilocus phylogeny and Bayesian estimates of species boundaries reveal hidden evolutionary relationships and cryptic diversity in Southeast Asian monitor lizards

Recent conceptual, technological and methodological advances in phylogenetics have enabled increasingly robust statistical species delimitation in studies of biodiversity. As the variety of evidence purporting species diversity has increased, so too have the kinds of tools and inferential power of m...

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Published inMolecular ecology Vol. 22; no. 13; pp. 3495 - 3510
Main Authors Welton, L. J, Siler, C. D, Oaks, J. R, Diesmos, A. C, Brown, R. M
Format Journal Article
LanguageEnglish
Published Oxford Blackwell Scientific Publications 01.07.2013
Blackwell Publishing Ltd
Blackwell
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Online AccessGet full text
ISSN0962-1083
1365-294X
1365-294X
DOI10.1111/mec.12324

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Abstract Recent conceptual, technological and methodological advances in phylogenetics have enabled increasingly robust statistical species delimitation in studies of biodiversity. As the variety of evidence purporting species diversity has increased, so too have the kinds of tools and inferential power of methods for delimiting species. Here, we showcase an organismal system for a data‐rich, comparative molecular approach to evaluating strategies of species delimitation among monitor lizards of the genus Varanus. The water monitors (Varanus salvator Complex), a widespread group distributed throughout Southeast Asia and southern India, have been the subject of numerous taxonomic treatments, which have drawn recent attention due to the possibility of undocumented species diversity. To date, studies of this group have relied on purportedly diagnostic morphological characters, with no attention given to the genetic underpinnings of species diversity. Using a 5‐gene data set, we estimated phylogeny and used multilocus genetic networks, analysis of population structure and a Bayesian coalescent approach to infer species boundaries. Our results contradict previous systematic hypotheses, reveal surprising relationships between island and mainland lineages and uncover novel, cryptic evolutionary lineages (i.e. new putative species). Our study contributes to a growing body of literature suggesting that, used in concert with other sources of data (e.g. morphology, ecology, biogeography), multilocus genetic data can be highly informative to systematists and biodiversity specialists when attempting to estimate species diversity and identify conservation priorities. We recommend holding in abeyance taxonomic decisions until multiple, converging lines of evidence are available to best inform taxonomists, evolutionary biologists and conservationists.
AbstractList Recent conceptual, technological and methodological advances in phylogenetics have enabled increasingly robust statistical species delimitation in studies of biodiversity. As the variety of evidence purporting species diversity has increased, so too have the kinds of tools and inferential power of methods for delimiting species. Here, we showcase an organismal system for a data‐rich, comparative molecular approach to evaluating strategies of species delimitation among monitor lizards of the genus Varanus. The water monitors (Varanus salvator Complex), a widespread group distributed throughout Southeast Asia and southern India, have been the subject of numerous taxonomic treatments, which have drawn recent attention due to the possibility of undocumented species diversity. To date, studies of this group have relied on purportedly diagnostic morphological characters, with no attention given to the genetic underpinnings of species diversity. Using a 5‐gene data set, we estimated phylogeny and used multilocus genetic networks, analysis of population structure and a Bayesian coalescent approach to infer species boundaries. Our results contradict previous systematic hypotheses, reveal surprising relationships between island and mainland lineages and uncover novel, cryptic evolutionary lineages (i.e. new putative species). Our study contributes to a growing body of literature suggesting that, used in concert with other sources of data (e.g. morphology, ecology, biogeography), multilocus genetic data can be highly informative to systematists and biodiversity specialists when attempting to estimate species diversity and identify conservation priorities. We recommend holding in abeyance taxonomic decisions until multiple, converging lines of evidence are available to best inform taxonomists, evolutionary biologists and conservationists.
Recent conceptual, technological and methodological advances in phylogenetics have enabled increasingly robust statistical species delimitation in studies of biodiversity. As the variety of evidence purporting species diversity has increased, so too have the kinds of tools and inferential power of methods for delimiting species. Here, we showcase an organismal system for a data-rich, comparative molecular approach to evaluating strategies of species delimitation among monitor lizards of the genus Varanus. The water monitors (Varanus salvator Complex), a widespread group distributed throughout Southeast Asia and southern India, have been the subject of numerous taxonomic treatments, which have drawn recent attention due to the possibility of undocumented species diversity. To date, studies of this group have relied on purportedly diagnostic morphological characters, with no attention given to the genetic underpinnings of species diversity. Using a 5-gene data set, we estimated phylogeny and used multilocus genetic networks, analysis of population structure and a Bayesian coalescent approach to infer species boundaries. Our results contradict previous systematic hypotheses, reveal surprising relationships between island and mainland lineages and uncover novel, cryptic evolutionary lineages (i.e. new putative species). Our study contributes to a growing body of literature suggesting that, used in concert with other sources of data (e.g. morphology, ecology, biogeography), multilocus genetic data can be highly informative to systematists and biodiversity specialists when attempting to estimate species diversity and identify conservation priorities. We recommend holding in abeyance taxonomic decisions until multiple, converging lines of evidence are available to best inform taxonomists, evolutionary biologists and conservationists. [PUBLICATION ABSTRACT]
Recent conceptual, technological and methodological advances in phylogenetics have enabled increasingly robust statistical species delimitation in studies of biodiversity. As the variety of evidence purporting species diversity has increased, so too have the kinds of tools and inferential power of methods for delimiting species. Here, we showcase an organismal system for a data-rich, comparative molecular approach to evaluating strategies of species delimitation among monitor lizards of the genus Varanus. The water monitors (Varanus salvator Complex), a widespread group distributed throughout Southeast Asia and southern India, have been the subject of numerous taxonomic treatments, which have drawn recent attention due to the possibility of undocumented species diversity. To date, studies of this group have relied on purportedly diagnostic morphological characters, with no attention given to the genetic underpinnings of species diversity. Using a 5-gene data set, we estimated phylogeny and used multilocus genetic networks, analysis of population structure and a Bayesian coalescent approach to infer species boundaries. Our results contradict previous systematic hypotheses, reveal surprising relationships between island and mainland lineages and uncover novel, cryptic evolutionary lineages (i.e. new putative species). Our study contributes to a growing body of literature suggesting that, used in concert with other sources of data (e.g. morphology, ecology, biogeography), multilocus genetic data can be highly informative to systematists and biodiversity specialists when attempting to estimate species diversity and identify conservation priorities. We recommend holding in abeyance taxonomic decisions until multiple, converging lines of evidence are available to best inform taxonomists, evolutionary biologists and conservationists.Recent conceptual, technological and methodological advances in phylogenetics have enabled increasingly robust statistical species delimitation in studies of biodiversity. As the variety of evidence purporting species diversity has increased, so too have the kinds of tools and inferential power of methods for delimiting species. Here, we showcase an organismal system for a data-rich, comparative molecular approach to evaluating strategies of species delimitation among monitor lizards of the genus Varanus. The water monitors (Varanus salvator Complex), a widespread group distributed throughout Southeast Asia and southern India, have been the subject of numerous taxonomic treatments, which have drawn recent attention due to the possibility of undocumented species diversity. To date, studies of this group have relied on purportedly diagnostic morphological characters, with no attention given to the genetic underpinnings of species diversity. Using a 5-gene data set, we estimated phylogeny and used multilocus genetic networks, analysis of population structure and a Bayesian coalescent approach to infer species boundaries. Our results contradict previous systematic hypotheses, reveal surprising relationships between island and mainland lineages and uncover novel, cryptic evolutionary lineages (i.e. new putative species). Our study contributes to a growing body of literature suggesting that, used in concert with other sources of data (e.g. morphology, ecology, biogeography), multilocus genetic data can be highly informative to systematists and biodiversity specialists when attempting to estimate species diversity and identify conservation priorities. We recommend holding in abeyance taxonomic decisions until multiple, converging lines of evidence are available to best inform taxonomists, evolutionary biologists and conservationists.
Author Brown, R. M.
Siler, C. D.
Oaks, J. R.
Diesmos, A. C.
Welton, L. J.
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Issue 13
Keywords nuclear DNA
species delimitation
Taxonomy
Tropical zone
Philippines
Conservation
Diversity
Mitochondrial DNA
Phylogeny
Cryptic
Vertebrata
Southeast Asia
Sauria
Genetics
Reptilia
conservation genetics
Language English
License CC BY 4.0
2013 John Wiley & Sons Ltd.
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istex:5BDAB6238432F6AE79199D61C7BB5526BA13A120
Fulbright and Fulbright-Hayes Fellowships
University of Kansas Biodiversity Institute
Appendix S1 Specimen voucher numbers, identification and geographic location of samples for this study. Appendix S2 Description of *BEAST methodology for inferring BP&P starting topologies. Appendix S3 Description of BP&P species delimitation methodology.Fig. S1 Mitochondrial (left) and concatenated nuclear (right) maximum likelihood phylogenetic estimates. Only bootstrap support >70% is indicated. Fig. S2 Individual maximum likelihood gene trees for the four nuclear loci sampled. Only bootstrap support >70% is indicated. Fig. S3 Mitochondrial and nuclear (ND1-ND2, DGL-α, L52, L74, PRLR) statistical haplotype networks inferred by TCS (Clement et al. ). Fig. S4 Distance-based (neighbour-joining) nuclear haplotype network as inferred by the NeighborNet algorithm of splitstree. Input standardized distance matrix created with the program pofad. Fig. S5 Distruct visualization (Rosenberg ) visualization of structure analyses and summarized geographic distribution of major Varanus demes (Pritchard et al. ) for K = 6 populations. Fig. S6 Bayesian estimates of the Varanus salvator Complex species tree as inferred by the program *beast. Fig. S7 Recognized major faunal regions and island groups of the Philippines, including distributions of Varanus species.Table S1 Individual loci, original publications and polymerase chain reaction (PCR) thermal profiles for each. Annealing temperature was varied to improve amplification for problematic samples. Table S2 Loci and associated primers sequenced for this study. Thermal profiles for PCR and cycle sequencing reactions vary only by annealing temperature (55-58º) across primers and samples. Table S3 Estimated models of evolution by data partition, as inferred by jmodeltest. Final models selected by AIC and applied for partitioned, model-based analyses. Table S4 Summary of results among loci for tests of neutrality using Tajima's D (Tajima ).
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Fujita MK, Leaché AD, Burbrink FT, McGuire JA, Moritz C (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology and Evolution, 27, 480-488.
Harris JD, Sá-Sousa P (2002) Molecular phylogenetics of Iberian Wall Lizards (Podarcis): is Podarcis hispanica a species complex? Molecular Phylogenetics and Evolution, 23, 75-81.
King D, King M, Baverstock P (1991) A new phylogeny of the Varanidae. Mertensiella, 2, 211-219.
Leaché AD, Fujita MK (2010) Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society. B, Biological Sciences, 277, 3071-3077.
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Cassens I, Van Waerebeek K, Best PB et al. (2003) The phylogeography of dusky dolphins (Lagenorhynchus obscurus); a critical examination of network methods and rooting procedures. Molecular Ecology, 12, 1781-1792.
Marshall DC (2010) Cryptic failure of partitioned Bayesian phylogenetic analyses: lost in the land of long trees. Systematic Biology, 59, 108-117.
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Zarza E, Reynolds VH, Emerson BC (2008) Diversification in the northern neotropics: mitochondrial and nuclear DNA phylogeography of the iguana Ctenosaura pectinata and related species. Molecular Ecology, 17, 3259-3275.
Hubisz MJ, Falush D, Stephens M et al. (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology, 9, 1322-1332.
Sites JW, Marshall JC (2004) Operational criteria for delimiting species. Annual Review of Ecology, Evolution, and Systematics, 35, 199-227.
Schulte JA, Melville J, Larson A (2003) Molecular phylogenetic evidence for ancient divergence of lizard taxa on either side of Wallace's Line. Proceedings of the Royal Society. B, Biological Sciences, 270, 597-603.
Siler CD, Brown RM (2010) Phylogeny-based species delimitation in Philippine loam-swimming skinks (Reptilia: Squamata: Scincidae: Brachymeles): taxonomic revision of the pentadactyl species groups and description of three new species. Herpetological Monographs, 24, 1-54.
Barrett CF, Freudenstein JV (2011) An integrative approach to delimiting species in a rare but widespread mycoheterotrophic orchid. Molecular Ecology, 20, 2771-2786.
R Development Core Team (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.
Ronquist F, Huelsenbeck J (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
Hoogerwerf A (1954) Notes on the vertebrate fauna of the Krakatau i
1989; 40
2011; 477
2010; 10
2004; 20
2006a; 60
1991; 15
2010; 107
1992; 121
2010; 17
1942c; 466
2004; 4
2003; 270
1997; 1
2003; 51
2003; 52
1942b; 465
1996; 77
1997; 8
1995; 20
2004; 32
2010; 27
1942a; 462
2010; 26
2010; 24
2000; 14
2006; 23
2006; 22
1997; 145
2004; 35
2008; 25
2011; 65
2007; 7
2005; 76
2012; 27
1981
1995; 29
2003; 164
1959; 40
2009; 63
2010; 37
1954; 22
2006; 55
2002; 76
1993; 41
2005; 85
2007; 90
2008; 57
2012; 39
1992
2010b; 57
1999
2007; 16
2004; 53
1989; 123
1975; 28
1988; 27
2000; 74
1992; 28
2008; 47
2005; 4
1885
1995; 146
2010a; 6
2012; 43
2003; 341
1998; 9
2005; 14
1768
2010; 56
2010; 55
2012; 164
2010; 59
2002; 51
2000; 9
2009; 155
1999; 125
2003; 18
2003; 19
2003; 12
2006b; 55
2009; 53
2010a; 2446
2013; 159
2010; 277
2010; 278
2011; 20
1997; 19
2001; 16
2001; 17
2011; 27
1975; 3
2012; 63
2009; 23
1991; 2
2011
2008; 17
2009
2005; 41
2008
2007
2004
2000; 155
2002
2001; 68
2007; 56
2011; 178
1998; 25
2002; 23
2009; 9
1963
2005; 54
2009; 3
2012; 4
2007; 45
2005; 55
2010b; 24
2007; 48
2012; 8
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  article-title: Species delimitation: new approaches for discovering diversity
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  article-title: Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows
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Snippet Recent conceptual, technological and methodological advances in phylogenetics have enabled increasingly robust statistical species delimitation in studies of...
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SubjectTerms Amphibia. Reptilia
Animal populations
Animals
Asia, Southeastern
Bayes Theorem
Bayesian analysis
Biodiversity
Biogeography
Biological and medical sciences
Biological evolution
Boundaries
conservation genetics
Conservation of Natural Resources
data collection
DNA, Mitochondrial - genetics
Evolution, Molecular
Evolutionary biology
Fundamental and applied biological sciences. Psychology
Genetic diversity
Genetic Loci
Genetic Speciation
Genetic Variation
Genetics of eukaryotes. Biological and molecular evolution
Haplotypes
India
Lacertilia
Lizards
Lizards - classification
Lizards - genetics
mitochondrial DNA
Molecular Sequence Data
nuclear DNA
Philippines
Phylogenetics
Phylogeny
Phylogeography
Population genetics, reproduction patterns
Population structure
Reptiles & amphibians
Sequence Alignment
Sequence Analysis, DNA
South East Asia
Southeast Asia
species delimitation
Species diversity
Varanus
Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution
Water monitoring
Title Multilocus phylogeny and Bayesian estimates of species boundaries reveal hidden evolutionary relationships and cryptic diversity in Southeast Asian monitor lizards
URI https://api.istex.fr/ark:/67375/WNG-0XZ0FMSM-4/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fmec.12324
https://www.ncbi.nlm.nih.gov/pubmed/23710945
https://www.proquest.com/docview/1371453234
https://www.proquest.com/docview/1372696035
https://www.proquest.com/docview/1399923047
https://www.proquest.com/docview/1803136677
Volume 22
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