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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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Map showing the distribution of Neomys anomalus anomalus, N. a. milleri and N. teres. The original distributions were downloaded from the IUCN Red List of Threatened Species website [72, 73] and they were modified to reflect the results of our genetic analyses. Dots indicate samples used for sequencing nuclear introns and cytochrome b (large dots) or only cytochrome b (small dots). The locations of additional cytochrome b sequences downloaded from databases are indicated with diamonds (with empty diamonds corresponding to samples being used in the cytochrome b tree but not in the species tree analyses). All localities correspond to a single specimen, except the localities of N. teres. Locality numbers are given in Tables S1 (for samples obtained for this work) and S2 (for database sequences) of Additional file 1. Type localities of N. a. anomalus (San Martín de la Vega, Madrid, Spain) and N. a. milleri (Chesières, Alpes Vaudoises, Switzerland) are indicated with a star symbol. The distribution of N. fodiens largely overlaps with that of the other species and it is not shown here; see Additional file 1: Tables S1 and S2 for further details
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Fig1: Map showing the distribution of Neomys anomalus anomalus, N. a. milleri and N. teres. The original distributions were downloaded from the IUCN Red List of Threatened Species website [72, 73] and they were modified to reflect the results of our genetic analyses. Dots indicate samples used for sequencing nuclear introns and cytochrome b (large dots) or only cytochrome b (small dots). The locations of additional cytochrome b sequences downloaded from databases are indicated with diamonds (with empty diamonds corresponding to samples being used in the cytochrome b tree but not in the species tree analyses). All localities correspond to a single specimen, except the localities of N. teres. Locality numbers are given in Tables S1 (for samples obtained for this work) and S2 (for database sequences) of Additional file 1. Type localities of N. a. anomalus (San Martín de la Vega, Madrid, Spain) and N. a. milleri (Chesières, Alpes Vaudoises, Switzerland) are indicated with a star symbol. The distribution of N. fodiens largely overlaps with that of the other species and it is not shown here; see Additional file 1: Tables S1 and S2 for further details

Mentions: Multilocus species delimitation methods and dated species trees can be particularly useful for groups with contentious taxonomies. The water shrews of the genus Neomys are a case in point. This mammalian genus currently contains three recognized species [22]: N. fodiens, which has a Palaearctic distribution extending to Lake Baikal, with additional populations in eastern Russia and China; N. teres, which is present in the Caucasus and adjacent parts of Turkey and Iran; and N. anomalus, which has a patchy distribution over part of continental Europe and the Middle East. Two subspecies of N. anomalus (N. a. anomalus and N. a. milleri) were originally described in 1907 as separate species, by Cabrera [23] and Mottaz [24] respectively. Previously described morphological differences originally referred to the overall shape of the skull, rounded in N. milleri and more angular in N. anomalus [23, 24]. Further analyses revealed size differences in several measurements, particularly the length of the tail and hind foot, with N. anomalus being larger in both measurements [25–27]. However, these two taxa were cited as members of the same species in 1944 [28] and subsequent works followed the recognition of a single species [22, 29], without giving any clear argument for the regrouping. The known distribution of N. a. anomalus is centered in the Iberian Peninsula and N. a. milleri occupies the rest of the species’ Eurasian range (Fig. 1). All the species in this genus live in semi-aquatic habitats and usually feed underwater. Adaptations to aquatic life include stiff hairs on the tail and feet that aid in swimming and diving. These adaptations have been shown to be more prominent in N. fodiens [30] but, when these species live in sympatry, various instances of character displacement and convergence have been demonstrated [31, 32]. The phylogeny of this genus was studied using mitochondrial data, and N. fodiens was shown to be a sister group to the other species in the genus [33, 34].Fig. 1


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)

Map showing the distribution of Neomys anomalus anomalus, N. a. milleri and N. teres. The original distributions were downloaded from the IUCN Red List of Threatened Species website [72, 73] and they were modified to reflect the results of our genetic analyses. Dots indicate samples used for sequencing nuclear introns and cytochrome b (large dots) or only cytochrome b (small dots). The locations of additional cytochrome b sequences downloaded from databases are indicated with diamonds (with empty diamonds corresponding to samples being used in the cytochrome b tree but not in the species tree analyses). All localities correspond to a single specimen, except the localities of N. teres. Locality numbers are given in Tables S1 (for samples obtained for this work) and S2 (for database sequences) of Additional file 1. Type localities of N. a. anomalus (San Martín de la Vega, Madrid, Spain) and N. a. milleri (Chesières, Alpes Vaudoises, Switzerland) are indicated with a star symbol. The distribution of N. fodiens largely overlaps with that of the other species and it is not shown here; see Additional file 1: Tables S1 and S2 for further details
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: Map showing the distribution of Neomys anomalus anomalus, N. a. milleri and N. teres. The original distributions were downloaded from the IUCN Red List of Threatened Species website [72, 73] and they were modified to reflect the results of our genetic analyses. Dots indicate samples used for sequencing nuclear introns and cytochrome b (large dots) or only cytochrome b (small dots). The locations of additional cytochrome b sequences downloaded from databases are indicated with diamonds (with empty diamonds corresponding to samples being used in the cytochrome b tree but not in the species tree analyses). All localities correspond to a single specimen, except the localities of N. teres. Locality numbers are given in Tables S1 (for samples obtained for this work) and S2 (for database sequences) of Additional file 1. Type localities of N. a. anomalus (San Martín de la Vega, Madrid, Spain) and N. a. milleri (Chesières, Alpes Vaudoises, Switzerland) are indicated with a star symbol. The distribution of N. fodiens largely overlaps with that of the other species and it is not shown here; see Additional file 1: Tables S1 and S2 for further details
Mentions: Multilocus species delimitation methods and dated species trees can be particularly useful for groups with contentious taxonomies. The water shrews of the genus Neomys are a case in point. This mammalian genus currently contains three recognized species [22]: N. fodiens, which has a Palaearctic distribution extending to Lake Baikal, with additional populations in eastern Russia and China; N. teres, which is present in the Caucasus and adjacent parts of Turkey and Iran; and N. anomalus, which has a patchy distribution over part of continental Europe and the Middle East. Two subspecies of N. anomalus (N. a. anomalus and N. a. milleri) were originally described in 1907 as separate species, by Cabrera [23] and Mottaz [24] respectively. Previously described morphological differences originally referred to the overall shape of the skull, rounded in N. milleri and more angular in N. anomalus [23, 24]. Further analyses revealed size differences in several measurements, particularly the length of the tail and hind foot, with N. anomalus being larger in both measurements [25–27]. However, these two taxa were cited as members of the same species in 1944 [28] and subsequent works followed the recognition of a single species [22, 29], without giving any clear argument for the regrouping. The known distribution of N. a. anomalus is centered in the Iberian Peninsula and N. a. milleri occupies the rest of the species’ Eurasian range (Fig. 1). All the species in this genus live in semi-aquatic habitats and usually feed underwater. Adaptations to aquatic life include stiff hairs on the tail and feet that aid in swimming and diving. These adaptations have been shown to be more prominent in N. fodiens [30] but, when these species live in sympatry, various instances of character displacement and convergence have been demonstrated [31, 32]. The phylogeny of this genus was studied using mitochondrial data, and N. fodiens was shown to be a sister group to the other species in the genus [33, 34].Fig. 1

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
Related in: MedlinePlus