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Multilocus species trees and species delimitation in a temporal context: application to the water shrews of the genus Neomys.

Igea J, Aymerich P, Bannikova AA, Gosálbez J, Castresana J - BMC Evol. Biol. (2015)

Bottom Line: We also showed that the extrapolation of non-specific rates or the use of simpler models would lead to very different split time estimates.We showed that the estimation of rigorous lineage-specific mutation rates for each locus allows the inference of robust split times in a species tree framework.These times, in turn, afford a better understanding of the timeframe required to achieve isolation and, eventually, speciation in sister lineages.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37, 08003, Barcelona, Spain. igea.javier@gmail.com.

ABSTRACT

Background: Multilocus data are becoming increasingly important in determining the phylogeny of closely related species and delimiting species. In species complexes where unequivocal fossil calibrations are not available, rigorous dating of the coalescence-based species trees requires accurate mutation rates of the loci under study but, generally, these rates are unknown. Here, we obtained lineage-specific mutation rates of these loci from a higher-level phylogeny with a reliable fossil record and investigated how different choices of mutation rates and species tree models affected the split time estimates. We implemented this strategy with a genus of water shrews, Neomys, whose taxonomy has been contentious over the last century.

Results: We sequenced 13 introns and cytochrome b from specimens of the three species currently recognized in this genus including two subspecies of N. anomalus that were originally described as species. A Bayesian multilocus species delimitation method and estimation of gene flow supported that these subspecies are distinct evolutionary lineages that should be treated as distinct species: N. anomalus (sensu stricto), limited to part of the Iberian Peninsula, and N. milleri, with a larger Eurasian range. We then estimated mutation rates from a Bayesian relaxed clock analysis of the mammalian orthologues with several fossil calibrations. Next, using the estimated Neomys-specific rates for each locus in an isolation-with-migration model, the split time for these sister taxa was dated at 0.40 Myr ago (with a 95 % confidence interval of 0.26 - 0.86 Myr), likely coinciding with one of the major glaciations of the Middle Pleistocene. We also showed that the extrapolation of non-specific rates or the use of simpler models would lead to very different split time estimates.

Conclusions: We showed that the estimation of rigorous lineage-specific mutation rates for each locus allows the inference of robust split times in a species tree framework. These times, in turn, afford a better understanding of the timeframe required to achieve isolation and, eventually, speciation in sister lineages. The application of species delimitation methods and an accurate dating strategy to the genus Neomys helped to clarify its controversial taxonomy.

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a Haplotype genealogies of the 13 introns amplified in the genus Neomys. The sizes of the circles are proportional to the number of haplotypes detected. b Distance tree based on an estimate of the average genomic divergence between the introns of Neomys specimens. The tree was rooted at the midpoint. The scale bar is in substitutions/site
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Fig3: a Haplotype genealogies of the 13 introns amplified in the genus Neomys. The sizes of the circles are proportional to the number of haplotypes detected. b Distance tree based on an estimate of the average genomic divergence between the introns of Neomys specimens. The tree was rooted at the midpoint. The scale bar is in substitutions/site

Mentions: Thirteen intron markers were sequenced from each of the 11 Neomys specimens with tissue samples available. The number of alleles determined for each lineage was 78 for N. a. anomalus, 94 for N. a. milleri, 52 for N. teres and 52 for N. fodiens, totaling 129,494 bp of nuclear sequence information for all specimens together. From the intron alignments, the percentage of gaps removed previous to the analyses varied between 0.2 and 7.3 % of the alignment positions, with an average of 2.1 %. All introns were variable between the different species and showed some degree of intraspecific variation, as shown in the maximum-likelihood trees (Additional file 1: Figure S1) and the haplotype genealogies reconstructed from these trees (Fig. 3a). The four lineages preliminary considered in the mitochondrial tree were shown to constitute separated groups in four of the introns (ALAD-10, CSF2-2, HIF1AN-5 and TRAIP-8) but not in the others (Additional file 1: Figure S1 and Fig. 3a), making necessary further analyses of the nuclear data.Fig. 3


Multilocus species trees and species delimitation in a temporal context: application to the water shrews of the genus Neomys.

Igea J, Aymerich P, Bannikova AA, Gosálbez J, Castresana J - BMC Evol. Biol. (2015)

a Haplotype genealogies of the 13 introns amplified in the genus Neomys. The sizes of the circles are proportional to the number of haplotypes detected. b Distance tree based on an estimate of the average genomic divergence between the introns of Neomys specimens. The tree was rooted at the midpoint. The scale bar is in substitutions/site
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4587729&req=5

Fig3: a Haplotype genealogies of the 13 introns amplified in the genus Neomys. The sizes of the circles are proportional to the number of haplotypes detected. b Distance tree based on an estimate of the average genomic divergence between the introns of Neomys specimens. The tree was rooted at the midpoint. The scale bar is in substitutions/site
Mentions: Thirteen intron markers were sequenced from each of the 11 Neomys specimens with tissue samples available. The number of alleles determined for each lineage was 78 for N. a. anomalus, 94 for N. a. milleri, 52 for N. teres and 52 for N. fodiens, totaling 129,494 bp of nuclear sequence information for all specimens together. From the intron alignments, the percentage of gaps removed previous to the analyses varied between 0.2 and 7.3 % of the alignment positions, with an average of 2.1 %. All introns were variable between the different species and showed some degree of intraspecific variation, as shown in the maximum-likelihood trees (Additional file 1: Figure S1) and the haplotype genealogies reconstructed from these trees (Fig. 3a). The four lineages preliminary considered in the mitochondrial tree were shown to constitute separated groups in four of the introns (ALAD-10, CSF2-2, HIF1AN-5 and TRAIP-8) but not in the others (Additional file 1: Figure S1 and Fig. 3a), making necessary further analyses of the nuclear data.Fig. 3

Bottom Line: We also showed that the extrapolation of non-specific rates or the use of simpler models would lead to very different split time estimates.We showed that the estimation of rigorous lineage-specific mutation rates for each locus allows the inference of robust split times in a species tree framework.These times, in turn, afford a better understanding of the timeframe required to achieve isolation and, eventually, speciation in sister lineages.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37, 08003, Barcelona, Spain. igea.javier@gmail.com.

ABSTRACT

Background: Multilocus data are becoming increasingly important in determining the phylogeny of closely related species and delimiting species. In species complexes where unequivocal fossil calibrations are not available, rigorous dating of the coalescence-based species trees requires accurate mutation rates of the loci under study but, generally, these rates are unknown. Here, we obtained lineage-specific mutation rates of these loci from a higher-level phylogeny with a reliable fossil record and investigated how different choices of mutation rates and species tree models affected the split time estimates. We implemented this strategy with a genus of water shrews, Neomys, whose taxonomy has been contentious over the last century.

Results: We sequenced 13 introns and cytochrome b from specimens of the three species currently recognized in this genus including two subspecies of N. anomalus that were originally described as species. A Bayesian multilocus species delimitation method and estimation of gene flow supported that these subspecies are distinct evolutionary lineages that should be treated as distinct species: N. anomalus (sensu stricto), limited to part of the Iberian Peninsula, and N. milleri, with a larger Eurasian range. We then estimated mutation rates from a Bayesian relaxed clock analysis of the mammalian orthologues with several fossil calibrations. Next, using the estimated Neomys-specific rates for each locus in an isolation-with-migration model, the split time for these sister taxa was dated at 0.40 Myr ago (with a 95 % confidence interval of 0.26 - 0.86 Myr), likely coinciding with one of the major glaciations of the Middle Pleistocene. We also showed that the extrapolation of non-specific rates or the use of simpler models would lead to very different split time estimates.

Conclusions: We showed that the estimation of rigorous lineage-specific mutation rates for each locus allows the inference of robust split times in a species tree framework. These times, in turn, afford a better understanding of the timeframe required to achieve isolation and, eventually, speciation in sister lineages. The application of species delimitation methods and an accurate dating strategy to the genus Neomys helped to clarify its controversial taxonomy.

Show MeSH