Phylogeographical structure of the pygmy shrew: revisiting the roles of southern and northern refugia in Europe (original) (raw)
Related papers
2019
Southern and northern glacial refugia are considered paradigms that explain the complex phylogeographic patterns and processes of European biota. Although the Eurasian pygmy shrew Sorex minutus Linnaeus, 1766 (Eulipotyphla, Soricidae) has been used a model species to study geographic isolation and genetic diversification in Mediterranean peninsulas in the Last Glacial Maximum (LGM), and post-glacial population expansion from cryptic northern glacial refugia in Western and Central Europe, there has been incomplete knowledge about the phylogeographic structure, genetic differentiation and demographic history within these regions. Here, we provide a revisited statistical phylogeographic study of S. minutus with greater sampling coverage in terms of numbers of individuals and geographic range, making it the most comprehensive investigation of this species to date. The results showed support for genetically distinct and diverse phylogeographic groups consistent with southern and northern glacial refugia, as expected from previous studies, but also identified geographical barriers concordant with glaciated mountain ranges during the LGM, early diversification events dated between the Upper Pleistocene and Lower Holocene for the main phylogeographic groups, and recent (post-LGM) patterns of demographic expansions. The results have implications for the conservation of intraspecific diversity and the preservation of the evolutionary potential of S. minutus.
2010
Here, I investigate the phylogeography and morphology of the Eurasian pygmy shrew Sorex minutus, searching for significantly differentiated lineages, colonisation routes and demographic parameters that would explain the effects of the Quaternary glaciations on the current distribution of the species. I also explore the genetic and morphological diversity and origin of pygmy shrew populations in the British Isles, particularly focusing on Ireland and the Orkney islands. Mitochondrial and nuclear DNA markers were used for the phylogeographic analyses, and a geometric morphometrics approach was implemented on mandible and skull samples. There was an evident phylogeographic structure across Eurasia consistent with occurrence of southern glacial refugia, and there were two distinct lineages in Northern-Central Europe and near the Pyrenees supporting the existence of northern glacial refugia through the characteristics of their distribution and population expansion. Haplotypes from Britai...
Ecography, 2000
The southern European peninsulas (Iberian, Italian and Balkan) are traditionally recognized as glacial refugia from where many species colonized central and northern Europe after the Last Glacial Maximum (LGM). However, evidence that some species had more northerly refugia is accumulating from phylogeographic, palaeontological and palynological studies, and more recently from species distribution modelling (SDM), but further studies are needed to test the idea of northern refugia in Europe. Here, we take a rarely implemented multidisciplinary approach to assess if the pygmy shrew Sorex minutus, a widespread Eurasian mammal species, had northern refugia during the LGM, and if these influenced its postglacial geographic distribution. First, we evaluated the phylogeographic and population expansion patterns using mtDNA sequence data from 123 pygmy shrews. Then, we used SDM to predict present and past (LGM) potential distributions using two different training data sets, two different algorithms (Maxent and GARP) and climate reconstructions for the LGM with two different general circulation models. An LGM distribution in the southern peninsulas was predicted by the SDM approaches, in line with the occurrence of lineages of S. minutus in these areas. The phylogeographic analyses also indicated a widespread and strictly northern-central European lineage, not derived from southern peninsulas, and with a postglacial population expansion signature. This was consistent with the SDM predictions of suitable LGM conditions for S. minutus occurring across central and eastern Europe, from unglaciated parts of the British Isles to much of the eastern European Plain. Hence, S. minutus likely persisted in parts of central and eastern Europe during the LGM, from where it colonized other northern areas during the late-glacial and postglacial periods. Our results provide new insights into the glacial and postglacial colonization history of the European mammal fauna, notably supporting glacial refugia further north than traditionally recognized.
The aim of the present study was to investigate the genetic structure of the Valais shrew (Sorex antinorii) by a combined phylogeographical and landscape genetic approach, and thereby to infer the locations of glacial refugia and establish the influence of geographical barriers. We sequenced part of the mitochondrial cytochrome b (cyt b) gene of 179 individuals of S. antinorii sampled across the entire species' range. Six specimens attributed to S. arunchi were included in the analysis. The phylogeographical pattern was assessed by Bayesian molecular phylogenetic reconstruction, population genetic analyses, and a species distribution modelling (SDM)-based hindcasting approach. We also used landscape genetics (including isolation-by-resistance) to infer the determinants of current intra-specific genetic structure. The phylogeographical analysis revealed shallow divergence among haplotypes and no clear substructure within S. antinorii. The starlike structure of the median-joining network is consistent with population expansion from a single refugium, probably located in the Apennines. Long branches observed on the same network also suggest that another refugium may have existed in the north-eastern part of Italy. This result is consistent with SDM, which also suggests several habitable areas for S. antinorii in the Italian peninsula during the LGM. Therefore S. antinorii appears to have occupied disconnected glacial refugia in the Italian peninsula, supporting previous data for other species showing multiple refugia within southern refugial areas. By coupling genetic analyses and SDM, we were able to infer how past climatic suitability contributed to genetic divergence of populations. The genetic differentiation shown in the present study does not support the specific status of S. arunchi. P. 2006. Hares on thin ice: introgression of mitochondrial DNA in hares and its implications for recent phylogenetic analyses. Molecular Phylogenetics and Evolution 40: 640-641. Araújo MB, New M. 2007. Ensemble forecasting of species distributions. Trends in Ecology and Evolution 22: 42-47. Avise J. 2000. Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press. Bandelt H-J, Forster P, Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37-48. Basset P, Yannic G, Hausser J. 2006. Genetic and karyotypic structure in the shrews of the Sorex araneus group: are they independent? Molecular Ecology 15: 1577-1587. Bilton DT, Mirol PM, Mascheretti S, Fredga K, Zima J, Searle JB. 1998. Mediterranean Europe as an area of endemism for small mammals rather than a source for northwards postglacial colonization. Proceedings of the Royal Society of London Series B, Biological Sciences 265: 1219-1226. Brünner H, Lugon-Moulin N, Balloux F, Fumagalli L, Hausser J. 2002. A taxonomical re-evaluation of the Valais chromosome race of the common shrew Sorex araneus (Insectivora: Soricidae). Acta Theriologica 47: 245-275. Canestrelli D, Cimmaruta R, Nascetti G. 2007. Phylogeography and historical demography of the Italian treefrog, Hyla intermedia, reveals multiple refugia, population expansions and secondary contacts within peninsular Italy. Molecular Ecology 16: 4808-4482. Canestrelli D, Cimmaruta R, Nascetti G. 2008. Population genetic structure and diversity of the Apennine endemic stream frog, Rana italica -insights on the Pleistocene evolutionary history of the Italian peninsular biota. Molecular Ecology 17: 3856-3872.
The aim of the present study was to investigate the genetic structure of the Valais shrew (Sorex antinorii) by a combined phylogeographical and landscape genetic approach, and thereby to infer the locations of glacial refugia and establish the influence of geographical barriers. We sequenced part of the mitochondrial cytochrome b (cyt b) gene of 179 individuals of S. antinorii sampled across the entire species' range. Six specimens attributed to S. arunchi were included in the analysis. The phylogeographical pattern was assessed by Bayesian molecular phylogenetic reconstruction, population genetic analyses, and a species distribution modelling (SDM)-based hindcasting approach. We also used landscape genetics (including isolation-by-resistance) to infer the determinants of current intra-specific genetic structure. The phylogeographical analysis revealed shallow divergence among haplotypes and no clear substructure within S. antinorii. The starlike structure of the median-joining network is consistent with population expansion from a single refugium, probably located in the Apennines. Long branches observed on the same network also suggest that another refugium may have existed in the north-eastern part of Italy. This result is consistent with SDM, which also suggests several habitable areas for S. antinorii in the Italian peninsula during the LGM. Therefore S. antinorii appears to have occupied disconnected glacial refugia in the Italian peninsula, supporting previous data for other species showing multiple refugia within southern refugial areas. By coupling genetic analyses and SDM, we were able to infer how past climatic suitability contributed to genetic divergence of populations. The genetic differentiation shown in the present study does not support the specific status of S. arunchi. P. 2006. Hares on thin ice: introgression of mitochondrial DNA in hares and its implications for recent phylogenetic analyses. Molecular Phylogenetics and Evolution 40: 640-641. Araújo MB, New M. 2007. Ensemble forecasting of species distributions. Trends in Ecology and Evolution 22: 42-47. Avise J. 2000. Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press. Bandelt H-J, Forster P, Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37-48. Basset P, Yannic G, Hausser J. 2006. Genetic and karyotypic structure in the shrews of the Sorex araneus group: are they independent? Molecular Ecology 15: 1577-1587. Bilton DT, Mirol PM, Mascheretti S, Fredga K, Zima J, Searle JB. 1998. Mediterranean Europe as an area of endemism for small mammals rather than a source for northwards postglacial colonization. Proceedings of the Royal Society of London Series B, Biological Sciences 265: 1219-1226. Brünner H, Lugon-Moulin N, Balloux F, Fumagalli L, Hausser J. 2002. A taxonomical re-evaluation of the Valais chromosome race of the common shrew Sorex araneus (Insectivora: Soricidae). Acta Theriologica 47: 245-275. Canestrelli D, Cimmaruta R, Nascetti G. 2007. Phylogeography and historical demography of the Italian treefrog, Hyla intermedia, reveals multiple refugia, population expansions and secondary contacts within peninsular Italy. Molecular Ecology 16: 4808-4482. Canestrelli D, Cimmaruta R, Nascetti G. 2008. Population genetic structure and diversity of the Apennine endemic stream frog, Rana italica -insights on the Pleistocene evolutionary history of the Italian peninsular biota. Molecular Ecology 17: 3856-3872.
Biological Journal of The Linnean Society, 2010
At the Last Glacial Maximum (LGM), the southern European peninsulas were important refugia for temperate species. Current genetic subdivision of species within these peninsulas may reflect past population subdivision at the LGM, as in 'refugia within refugia', and/or at other time periods. In the present study, we assess whether pygmy shrew populations from different regions within Italy are genetically and morphologically distinct. One maternally and two paternally inherited molecular markers (cytochrome b and Y-chromosome introns, respectively) were analysed using several phylogenetic methods. A geometric morphometric analysis was performed on mandibles to evaluate size and shape variability between populations. Mandible shape was also explored with a functional approach that considered the mandible as a first-order lever affecting bite force. We found genetically and morphologically distinct European, Italian, and southern Italian groups. Mandible size increased with decreasing latitude and southern Italian pygmy shrews exhibited mandibles with the strongest bite force. It is not clear whether or not the southern Italian and Italian groups of pygmy shrews occupied different refugia within the Italian peninsula at the LGM. It is likely, however, that geographic isolation earlier than the LGM on islands at the site of present-day Calabria was important in generating the distinctive southern Italian group of pygmy shrews, and also the genetic groups in other small vertebrates that we review here. Calabria is an important hotspot for genetic diversity, and is worthy of conservation attention.
Phylogeography of the Alpine shrew,Sorex alpinus(Soricidae, Mammalia)
Folia Zoologica, 2016
Cold tolerant species often exhibit specific responses to Pleistocene climate oscillations, including range expansions during glacial periods and altitudinal shifts between glacial and interglacial periods. Small terrestrial mammals are ideal candidates to study these processes due to their limited dispersal abilities, short generation time and rapid sequence evolution. The aim of this study was to investigate phylogeographical structure of the Alpine shrew (Sorex alpinus) within its recently fragmented range in the central and southern European mountain system. To examine its genetic structure, we sequenced the hypervariable domain of the mitochondrial control region in 51 individuals from 18 localities, covering the majority of the distributional area of the species. We analyzed the sequence dataset using population and landscape genetic approaches. We discovered shallow mitochondrial genealogy with degree of differentiation among site-specific haplogroups. This pattern, together with demographic analyses showing population expansion, corroborate the hypothesis that during the glacial periods, S. alpinus expanded its range into lower elevations between northern and high mountain system glaciers. This expansion was followed by a postglacial range breakup, retreat to moderate elevations of high mountain systems, and a formation of relict enclaves in smaller hilly areas.
Molecular Ecology, 2008
Using one male-inherited, one female-inherited and eight biparentally inherited markers, we investigate the population genetic structure of the Valais shrew (Sorex antinorii) in the Swiss Alps. Bayesian analysis on autosomal microsatellites suggests a clear genetic differentiation between two groups of populations. This geographically based structure is consistent with two separate postglacial recolonization routes of the species into Switzerland from Italian refugia after the last Pleistocene glaciations. Sex-specific markers also confirm genetic structuring among western and eastern areas, since very few haplotypes for either Y chromosome or mtDNA genome are shared between the two regions. Overall, these results suggest that two already well-differentiated genetic lineages colonized the Swiss Alps and came into secondary contact in the Rhône Valley. Low level of admixture between the two lineages is likely explained by the mountainous landscape structure of lateral valleys orthogonal to the main Rhône valley.
Evolutionary history and phylogeographic relationships of shrews from Sorex araneus group
PLOS ONE
Shrews of the Sorex genus are an evolutionarily successful group that includes more than 77 species widely distributed in Eurasia and North America. The genus is one of the rare cases where karyotypic changes reflect well the evolutionary relationships among its species. The taxa showing the greatest variation in karyotype are usually classified into the Sorex araneus group. Its evolution was associated with chromosomal rearrangements, which could have promoted fast diversification of this group into many chromosomal races and species. These processes were additionally complicated by introgressions of mitochondrial DNA, which made the evolutionary history of this group quite complex and difficult to infer. To tackle the problem, we performed multi-method phylogenetic analyses based on mitochondrial cytochrome b that is considered a good molecular marker available for many representatives of Sorex. The results were compared with phylogenies based on chromosomal rearrangement data and put into temporal and spatial context using molecular dating and historical biogeography methods. We complemented the study with the estimation of diversification rates within the S. araneus group as well as comparing the results with paleontological records and climatic oscillations within the last 4 million years. Based on the gathered data, we proposed a hypothetical scenario for the evolution and geographic dispersion of species belonging to the S. araneus group. The shrews began to diversify about 2.7 million years ago in Eurasia and then migrated at least twice to North America. The evolution of shrews was driven by Pleistocene glacial and interglacial cycles, which increased their speciation rate and the emergence of new lineages. The migrations of populations were accompanied by introgressions of mitochondrial DNA into native shrews and occurred at least twice.