The population demography of Betula maximowicziana,a cool‐temperate tree species in Japan,in relation to the last glacial period: its admixture‐like genetic structure is the result of simple population splitting not admixing

Conservation of the local genetic variation and evolutionary integrity of economically and ecologically important trees is a key aspect of studies involving forest genetics, and a population demographic history of the target species provides valuable information for this purpose. Here, the genetic structure of 48 populations of Betula maximowicziana was assessed using 12 expressed sequence tag–simple sequence repeat (EST‐SSR) markers. Genetic diversity was lower in northern populations than southern ones and structure analysis revealed three groups: northern and southern clusters and an admixed group. Eleven more genomic‐SSR loci were added and the demographic history of these three groups was inferred by approximate Bayesian computation (ABC). The ABC revealed that a simple split scenario was much more likely than isolation with admixture, suggesting that the admixture‐like structure detected in this species was due to ancestral polymorphisms. The ABC analysis suggested that the population growth and divergence of the three groups occurred 96 800 (95% CI, 20 500–599 000) and 28 300 (95% CI, 8700–98 400) years ago, respectively. We need to be aware of several sources of uncertainty in the inference such as assumptions about the generation time, overlapping of generations, confidence intervals of the estimated parameters and the assumed model in the ABC. However, the results of the ABC together with the model‐based maps of reconstructed past species distribution and palaeoecological data suggested that the modern genetic structure of B. maximowicziana originated prior to the last glacial maximum (LGM) and that some populations survived in the northern range even during the LGM.     

East Asian allopatry and north Eurasian sympatry in Long‐tailed Tit lineages despite similar population dynamics during the late Pleistocene

Eurasia is a large continent characterized by heterogeneous environments. Glacial cycles during the late Pleistocene have had variable impacts on the avifauna across Eurasia. Bird populations from South‐East Asia show stability through the Last Glacial Maximum (LGM), while populations from Europe exhibit evidence of post‐LGM expansion. We investigated the phylogeography of the Long‐tailed Tit (Aegithalos caudatus), which spans the longitudinal breadth of Eurasia to test how climatic history and regional topographical complexity affected populations and diversification within the species complex. Our results show that two lineages from central and southern China (lineages C and D) segregate geographically, while lineages across northern Eurasia (lineage A and B) show substantial sympatry. Bayesian estimates for the timing of diversification suggest that the four lineages diverged during the middle Pleistocene, splitting in parallel and undergoing concurrent demographic histories since divergence. A. caudatus lineages experienced similar and synchronous population size dynamics during glacial cycles before the LGM. We conclude that the difference in geo‐topologic complexity may be an important factor that led to the variation in secondary admixture between northern Eurasian and eastern Asian lineages.     

Evolutionary history of the scorpionfly Dicerapanorpa magna (Mecoptera,Panorpidae)

Climate changes can have fundamental impacts on the distributional patterns of montane species, and range shifts frequently lead to allopatric divergence followed by the establishment of secondary contact zones. Many European and North American organisms have retreated to southern refugia during glacial periods and colonized northward during postglacial periods, but little is known about the evolutionary response of cold‐adapted insects to Pleistocene climate changes in eastern Asia. The scorpionfly Dicerapanorpa magna (Chou), with cold temperate habitat preference and weak dispersal ability, provides a good model system to explore how climate changes have influenced the distribution and divergence of cold‐adapted insects in eastern Asia. This study reconstructed the demographic dynamics and evolutionary history of D. magna with phylogeographic approaches, and predicted the species’ suitable areas under the Last Glacial Maximum (LGM) and current scenarios with the ecological niche modelling analysis. The mitochondrial cytochrome c oxidase subunit I resolved three phylogenetic lineages in D. magna dating back to Pleistocene, corresponding well with the geographically isolated Qinling, Bashan and Minshan Mountains. The ecological niche modelling recovered the suitable habitats for D. magna were the Qinling and Bashan Mountains under LGM and current conditions. The three lineages of D. magna might be in a process of incipient speciation, and likely derived their current distribution from separate glacial origins, followed by vicariance and divergence.     

Late‐glacial recolonization and phylogeography of European red deer (Cervus elaphus L.)

The Pleistocene was an epoch of extreme climatic and environmental changes. How individual species responded to the repeated cycles of warm and cold stages is a major topic of debate. For the European fauna and flora, an expansion–contraction model has been suggested, whereby temperate species were restricted to southern refugia during glacial times and expanded northwards during interglacials, including the present interglacial (Holocene). Here, we test this model on the red deer (Cervus elaphus) a large and highly mobile herbivore, using both modern and ancient mitochondrial DNA from the entire European range of the species over the last c. 40 000 years. Our results indicate that this species was sensitive to the effects of climate change. Prior to the Last Glacial Maximum (LGM) haplogroups restricted today to South‐East Europe and Western Asia reached as far west as the UK. During the LGM, red deer was mainly restricted to southern refugia, in Iberia, the Balkans and possibly in Italy and South‐Western Asia. At the end of the LGM, red deer expanded from the Iberian refugium, to Central and Northern Europe, including the UK, Belgium, Scandinavia, Germany, Poland and Belarus. Ancient DNA data cannot rule out refugial survival of red deer in North‐West Europe through the LGM. Had such deer survived, though, they were replaced by deer migrating from Iberia at the end of the glacial. The Balkans served as a separate LGM refugium and were probably connected to Western Asia with genetic exchange between the two areas.     

Interglacial genetic diversification of Moussonia deppeana (Gesneriaceae), a hummingbird‐pollinated,cloud forest shrub in northern Mesoamerica

Recent empirical work on cloud forest‐adapted species supports the role of both old divergences across major geographical areas and more recent divergences attributed to Pleistocene climate changes. The shrub Moussonia deppeana is distributed in northern Mesoamerica, with geographically disjunct populations. Based on sampling throughout the species range and employing plastid and nuclear markers, we (i) test whether the fragmented distribution is correlated with main evolutionary lineages, (ii) reconstruct its phylogeographical history to infer the history of cloud forest in northern Mesoamerica and (iii) evaluate a set of refugia/vicariance scenarios for the region and demographic patterns of the populations whose ranges expanded and tracked cloud forest conditions during the Last Glacial Maximum. We found a deep evolutionary split in M. deppeana about 6–3 Ma, which could be consistent with a Pliocene divergence. Comparison of variation in plastid and nuclear markers revealed several lineages mostly congruent with their isolated geographical distribution and restricted gene flow among groups. Results of species distribution modelling and coalescent simulations fit a model of multiple refugia diverging during interglacial cycles. The demographic history of M. deppeana is not consistent with an expanding–contracting cloud forest archipelago model during the Last Glacial Maximum. Instead, our data suggest that populations persisted across the geographical range throughout the glacial cycles, and experienced isolation and divergence during interglacial periods.     

The genetic structure of <Emphasis Type="Italic">Quercus crispula</Emphasis> in northeastern Japan as revealed by nuclear simple sequence repeat loci

Previous studies have reached different discussions about the genetic variation and genetic structure of Quercus crispula populations in northeastern Japan. This is a common oak species in Eastern Asia. Some studies have suggested that the populations in northeastern Japan were derived from those remaining in the southwest after the last glacial maximum (LGM), whilst other studies have found evidence that populations persisted in northeastern Japan during the LGM. Using seven highly polymorphic nuclear simple sequence repeat loci, we investigated the genetic structure of 16 Q. crispula populations along a latitudinal gradient in northeastern Japan (northern Honshu and Hokkaido), spanning about half of the species’ biogeographic range in the country. Although the level of population differentiation was low (F _ST = 0.021; G^￠_\textST G^{\prime}_{\text{ST}}  = 0.090), two geographically differentiated clusters were detected by STRUCTURE analysis. The first cluster included most of the populations in Hokkaido, and may indicate continued survival throughout past glacial periods. We found a significant decrease in allelic richness with latitude, so the second cluster may represent an expansion of the lineage from Honshu during the post-glacial period. These results should enhance our understanding of historical north–south migrations of this species in northeastern Japan.     

Genetic homogeneity between Korean and Japanese populations of the broad-leaved evergreen tree Machilus thunbergii (Lauraceae): A massive post-glacial immigration through the Korea Strait or something else?

The warm-temperate vegetation of Korea, currently limited to southern coastal areas, shifted during the Last Glacial Maximum (LGM) towards glacial refugia, putatively located in southern Japan. We hypothesized two scenarios of post-glacial re-colonization of warm-temperate species in relation to current levels of genetic diversity within their populations. If extant Korean populations originated from a single source (a single glacial refugium), we expect significantly lower levels of genetic diversity relative to those from Japan due to founder effects. Alternatively, if they were derived from multiple source populations, levels of genetic diversity within Korean populations will not be significantly reduced compared to those of Japanese ones. To test which of these scenarios is more likely, we investigated the patterns of genetic diversity in 14 populations (seven from southern Korea and seven from southern Japan) of the broad-leaved evergreen tree Machilus thunbergii, employing 11 allozyme loci. High levels of genetic variation in M. thunbergii were found both in southern Korea and southern Japan, with a considerable genetic homogeneity not only between the two regions but also between populations within the two regions. These results suggest a pattern of re-colonization after the LGM fitting the second scenario (immigration from multiple refugia), probably through multiple waves and/or with large founder populations.     

Ancient DNA supports southern survival of Richardson's collared lemming (Dicrostonyx richardsoni) during the last glacial maximum

Collared lemmings (genus Dicrostonyx) are circumpolar Arctic arvicoline rodents associated with tundra. However, during the last glacial maximum (LGM), Dicrostonyx lived along the southern ice margin of the Laurentide ice sheet in communities comprising both temperate and boreal species. To better understand these communities and the fate of these southern individuals, we compare mitochondrial cytochrome b sequence data from three LGM‐age Dicrostonyx fossils from south of the Laurentide ice sheet to sequences from modern Dicrostonyx sampled from across their present‐day range. We test whether the Dicrostonyx populations from LGM‐age continental USA became extinct at the Pleistocene–Holocene transition ~11000 years ago or, alternatively, if they belong to an extant species whose habitat preferences can be used to infer the palaeoclimate along the glacial margin. Our results indicate that LGM‐age Dicrostonyx from Iowa and South Dakota belong to Dicrostonyx richardsoni, which currently lives in a temperate tundra environment west of Hudson Bay, Canada. This suggests a palaeoclimate south of the Laurentide ice sheet that contains elements similar to the more temperate shrub tundra characteristic of extant D. richardsoni habitat, rather than the very cold, dry tundra of the Northern Arctic. While more data are required to determine whether or not the LGM southern population is ancestral to extant D. richardsoni, it seems most probable that the species survived the LGM in a southern refugium.     

Genetic turnovers and northern survival during the last glacial maximum in European brown bears

The current phylogeographic pattern of European brown bears (Ursus arctos) has commonly been explained by postglacial recolonization out of geographically distinct refugia in southern Europe, a pattern well in accordance with the expansion/contraction model. Studies of ancient DNA from brown bear remains have questioned this pattern, but have failed to explain the glacial distribution of mitochondrial brown bear clades and their subsequent expansion across the European continent. We here present 136 new mitochondrial sequences generated from 346 remains from Europe, ranging in age between the Late Pleistocene and historical times. The genetic data show a high Late Pleistocene diversity across the continent and challenge the strict confinement of bears to traditional southern refugia during the last glacial maximum (LGM). The mitochondrial data further suggest a genetic turnover just before this time, as well as a steep demographic decline starting in the mid‐Holocene. Levels of stable nitrogen isotopes from the remains confirm a previously proposed shift toward increasing herbivory around the LGM in Europe. Overall, these results suggest that in addition to climate, anthropogenic impact and inter‐specific competition may have had more important effects on the brown bear's ecology, demography, and genetic structure than previously thought.     

Mitochondrial introgressive hybridization following a demographic expansion in the tomato frogs of Madagascar,genus Dyscophus

Madagascar is a biodiversity hotspot with a unique fauna and flora largely endemic at the species level and highly threatened by habitat destruction. The processes underlying population‐level differentiation in Madagascar's biota are poorly understood and have been proposed to be related to Pleistocene climatic cycles, yet the levels of genetic divergence observed are often suggestive of ancient events. We combined molecular markers of different variability to assess the phylogeography of Madagascar's emblematic tomato frogs (Dyscophus guineti and D. antongilii) and interpret the observed pattern as resulting from ancient and recent processes. Our results suggest that the initial divergence between these taxa is probably old as reflected by protein‐coding nuclear genes and by a strong mitochondrial differentiation of the southernmost population. Dramatic changes in their demography appear to have been triggered by the end of the last glacial period and possibly by the short return of glacial conditions known as the 8K event. This dramatic change resulted in an approximately 50‐fold reduction of the effective population size in various populations of both species. We hypothesize these species' current mitochondrial DNA diversity distribution reflects a swamping of the mitochondrial genetic diversity of D. guineti by that of D. antongilii previous to the populations' bottlenecks during the Holocene, and probably as a consequence of D. antongilii demographic expansion approximately 1 million years ago. Our data support the continued recognition of D. antongilii and D. guineti as separate species and flag D. guineti as the more vulnerable species to past and probably also future environmental changes.     

Investigating past range dynamics for a weed of cultivation,Silene vulgaris

Since the last glacial maximum (LGM), many plant and animal taxa have expanded their ranges by migration from glacial refugia. Weeds of cultivation may have followed this trend or spread globally following the expansion of agriculture or ruderal habitats associated with human‐mediated disturbance. We tested whether the range expansion of the weed Silene vulgaris across Europe fit the classical model of postglacial expansion from southern refugia, or followed known routes of the expansion of human agricultural practices. We used species distribution modeling to predict spatial patterns of postglacial expansion and contrasted these with the patterns of human agricultural expansion. A population genetic analysis using microsatellite loci was then used to test which scenario was better supported by spatial patterns of genetic diversity and structure. Genetic diversity was highest in southern Europe and declined with increasing latitude. Locations of ancestral demes from genetic cluster analysis were consistent with areas of predicted refugia. Species distribution models showed the most suitable habitat in the LGM on the southern coasts of Europe. These results support the typical postglacial northward colonization from southern refugia while refuting the east‐to‐west agricultural spread as the main mode of expansion for S. vulgaris. We know that S. vulgaris has recently colonized many regions (including North America and other continents) through human‐mediated dispersal, but there is no evidence for a direct link between the Neolithic expansion of agriculture and current patterns of genetic diversity of S. vulgaris in Europe. Therefore, the history of range expansion of S. vulgaris likely began with postglacial expansion after the LGM, followed by more recent global dispersal by humans.     

Identification of glacial refugia in south-eastern North America by phylogeographical analyses of a forest understorey plant, Trillium cuneatum

Aim We examine several hypotheses emerging from biogeographical and fossil records regarding glacial refugia of a southern thermophilic plant species. Specifically, we investigated the glacial history and post‐glacial colonization of a forest understorey species, Trillium cuneatum. We focused on the following questions: (1) Did T. cuneatum survive the Last Glacial Maximum (LGM) in multiple refugia, and (if so) where were they located, and is the modern genetic structure congruent with the fossil record‐based reconstruction of refugia for mesic deciduous forests? (2) What are the post‐glacial colonization patterns in the present geographical range? Location South‐eastern North America. Methods We sampled 45 populations of T. cuneatum throughout its current range. We conducted phylogeographical analyses based on maternally inherited chloroplast DNA (cpDNA haplotypes) and used TCS software to reconstruct intraspecific phylogeny. Results We detected six cpDNA haplotypes, geographically highly structured into non‐overlapping areas. With one exception, none of the populations had mixed haplotype composition. TCS analysis resulted in two intraspecific cpDNA lineages, with one clade subdivided further by shallower diversification. Main conclusions Our investigation revealed that T. cuneatum survived the LGM in multiple refugia, belonging to two (western, eastern) genealogical lineages geographically structured across south‐eastern North America. The western clade is confined to the south‐western corner of T. cuneatum’s modern range along the Lower Mississippi Valley, where fossil records document a major refugium of mesic deciduous forest. For the eastern clade, modern patterns of cpDNA haplotype distribution suggest cryptic vicariance, in the form of forest contractions and subsequent expansions associated with Pleistocene glacial cycles, rather than simple southern survival and subsequent northward colonization. The north–south partitioning of cpDNA haplotypes was unexpected, suggesting that populations of this rather southern thermophilic species may have survived in more northern locations than initially expected based on LGM climate reconstruction, and that the Appalachian Mountains functioned as a barrier to the dispersal of propagules originating in more southern refugia. Furthermore, our results reveal south‐west to north‐east directionality in historical migration through the Valley and Ridge region of north‐west Georgia.     

Molecular data and ecological niche modelling reveal the Pleistocene history of a semi‐aquatic bug (Microvelia douglasi douglasi) in East Asia

This study investigated the Pleistocene history of a semi‐aquatic bug, Microvelia douglasi douglasi Scott, 1874 (Hemiptera: Veliidae) in East Asia. We used M. douglasi douglasi as a model species to explore the effects of historical climatic fluctuations on montane semi‐aquatic invertebrate species. Two hypotheses were developed using ecological niche models (ENMs). First, we hypothesized that M. douglasi douglasi persisted in suitable habitats in southern Guizhou, southern Yunnan, Hainan, Taiwan and southeast China during the LIG. After that, the populations expanded (Hypothesis 1). As the spatial prediction in the LGM was significantly larger than in the LIG, we then hypothesized that the population expanded during the LIG to LGM transition (Hypothesis 2). We tested these hypotheses using mitochondrial data (COI+COII) and nuclear data (ITS1 + 5.8S+ITS2). Young lineages, relatively deep splits, lineage differentiation among mountain ranges in central, south and southwest China and high genetic diversities were observed in these suitable habitats. Evidence of mismatch distributions and neutrality tests indicate that a population expansion occurred in the late Pleistocene. The Bayesian skyline plot (BSP) revealed an unusual population expansion that likely happened during the cooling transition between LIG and LGM. The results of genetic data were mostly consistent with the spatial predictions from ENM, a finding that can profoundly improve phylogeographic research. The ecological requirements of M. douglasi douglasi, together with the geographical heterogeneity and climatic fluctuations of Pleistocene in East Asia, could have shaped this unusual demographic history. Our study contributes to our knowledge of semi‐aquatic bug/invertebrate responses to Pleistocene climatic fluctuations in East Asia.     

Mitochondrial DNA variation and Quaternary range dynamics in the endangered Yellow Spotted Mountain Newt,Neurergus derjugini (Caudata,Salamandridae)

In temperate regions of the Earth Pleistocene, climatic fluctuations significantly influenced distribution of species. However, little is known on how glacial and interglacial cycles affected range dynamics of the species occupying lower latitudes. In this study, we investigated mitochondrial DNA (mtDNA) variation and reconstructed the potential current and past (during the mid‐Holocene, 6 ka BP, and the Last Glacial Maximum, LGM, 21 ka BP) distribution of Neurergus derjugini, an endangered amphibian species endemic to the mid‐Zagros Mountains in Iran and Iraq. Six haplotypes identified in the control region (D‐loop) form a well‐supported monophyletic clade, distinct from other Neurergus species and revealing a sister relationship to Neurergus kaiseri. Nucleotide diversity quantifying mean divergence between the sequences is low and does not support the recognition of distinct evolutionary lineages in Neurergus derjugini. The landscape connectivity analysis and the haplotype parsimony network reveal higher gene flow rate between the breeding streams in the southern part of the range, while the northern populations are more isolated. The potential distribution of Neurergus derjugini is restricted to valleys close to mountain tops, wherein very high elevations and dry habitats appear to be unsuitable. During the mid‐Holocene and LGM conditions, the range of the species may have been more extended and shifted to lower elevations. These findings show retraction of the Neurergus derjugini range during the Quaternary and indicate that range dynamics of the species occupying lower latitudes may not follow a scenario of glacial retraction and postglacial expansion.     

Comparative phylogeography and demographic history of two marsupials of the Atlantic Forest in eastern Brazil

The Atlantic Forest biodiversity hotspot in eastern South America has been the focus of several phylogeographic studies concerning relationships between populations and areas and how taxa respond to environmental changes. We infer and compare the demographic and biogeographic histories of two didelphid marsupial species, Gracilinanus microtarsus and Marmosops incanus, from the Atlantic Forest of eastern Brazil to determine how these species responded to environmental changes over time, using mitochondrial and nuclear DNA sequences. We found great intraspecific genetic divergence in both species and a strong geographic structure related to similar and spatially cohesive groups within each species. These groups are consistent with the same topographical barriers, such as mountains and river valleys. Intraspecific clades are very old, dating back to a period of tectonic activities in the Neogene (5.39–8.57 Mya). Changes in the environment over the last 7 million years lead to fairly concordant demographic changes in both marsupial species, including population expansion during the last glacial maximum (ca. 21,000 years ago) or last interglacial (ca. 120,000 years ago) or both. These results do not fit the Pleistocene refuge hypothesis as an explanation of the historical biogeography and diversification of both species in the Atlantic Forest, but are compatible with the Atlantis Forest hypothesis.     

Refugia,colonization and diversification of an arid‐adapted bird: coincident patterns between genetic data and ecological niche modelling

Phylogeographical studies are common in boreal and temperate species from the Palaearctic, but scarce in arid‐adapted species. We used nuclear and mitochondrial markers to investigate phylogeography and to estimate chronology of colonization events of the trumpeter finch Bucanetes githagineus, an arid‐adapted bird. We used 271 samples from 16 populations, most of which were fresh samples but including some museum specimens. Microsatellite data showed no clear grouping according to the sampling locations. Microsatellite and mitochondrial data showed the clearest differentiation between Maghreb and Canary Islands and between Maghreb and Western Sahara. Mitochondrial data suggest differentiation between different Maghreb populations and among Maghreb and Near East populations, between Iberian Peninsula and Canary Islands, as well as between Western Sahara and Maghreb. Our coalescence analyses indicate that the trumpeter finch colonized North Africa during the humid Marine Isotope Stage 5 (MIS5) period of the Sahara region 125 000 years ago. We constructed an ecological niche model (ENM) to estimate the geographical distribution of climatically suitable habitats for the trumpeter finch. We tested whether changes in the species range in relation to glacial–interglacial cycles could be responsible for observed patterns of genetic diversity and structure. Modelling results matched with those from genetic data as the species' potential range increases in interglacial scenarios (in the present climatic scenario and during MIS5) and decreases in glacial climates (during the last glacial maximum, LGM, 21 000 years ago). Our results suggest that the trumpeter finch responded to Pleistocene climatic changes by expanding and contracting its range.     

Genetic diversity of two mitochondrial DNA genes in Spirometra erinaceieuropaei (Cestoda: Diphyllobothridae) from Poland

The tapeworm species Spirometra erinaceieuropaei was documented mainly in Asia and Europe. In recent years, plerocercoid larvae (spargana) of this parasite have been found in different hosts in north‐eastern Poland. The evolutionary history and way of S. erinaceieuropaei spreading across Eurasia have been not described yet. However, this phenomenon could be closely related to the evolutionary history and migration routes of studied tapeworm host species. We investigated the genetic variability and divergence pattern among S. erinaceieuropaei populations in intermediate and paratenic hosts from north‐eastern Poland based on complete mitochondrial sequences of cytochrome b (cytb) and cytochrome c oxidase subunit I (cox1) genes. Analysis of 319 consolidated sequences of these two genes showed no genetic structure across study area. Comparison of sequences from Poland and China showed distinct separation of S. erinaceieuropaei populations from these two regions. They split from their common ancestor approximately 28.6 million years ago. Demographic expansion of Polish population of S. erinaceieuropaei started from glacial refugia approximately 12.5 thousand years ago, and recent population expansion has been observed in the tapeworm population from north‐eastern Poland.     

Postglacial population expansion of Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>) inferred from mitochondrial DNA phylogeography

We investigated the diversity and phylogeography of mitochondrial DNA (mtDNA) in Japanese macaques (Macaca fuscata), an endemic species in Japan that has the northernmost distribution of any non-human primate species. DNA samples from 135 localities representing the entire range of this species were compared. A total of 53 unique haplotypes were observed for the 412-bp partial mtDNA control region sequence, with length variation distinguishing the two subspecies. Clustering analyses suggested two putative major haplogroups, of which one was geographically distributed in eastern Japan and the other in western Japan. The populations in the east showed lower mtDNA diversity than those in the west. Phylogeographical relationships of haplotypes depicted with minimum spanning network suggested differences in population structure. Population expansion was significant for the eastern but not the western population, suggesting establishment of the ancestral population was relatively long ago in the west and recent in the east. Based on fossil evidence and past climate and vegetation changes, we inferred that the postulated population expansion may have taken place after the last glacial period (after 15,000 years ago). Mitochondrial DNA showed contrasting results in both variability and phylogenetic status of local populations to those of previous studies using protein variations, particularly for populations in the periphery of the range, with special inference on habitat change during the glacial period in response to cold adaptation. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Explosive radiation and spatial expansion across the cold environments of the Old World in an avian family

Our objective was to elucidate the biogeography and speciation patterns in an entire avian family, which shows a complex pattern of overlapping and nonoverlapping geographical distributions, and much variation in plumage, but less in size and structure. We estimated the phylogeny and divergence times for all of the world's species of Prunella based on multiple genetic loci, and analyzed morphometric divergence and biogeographical history. The common ancestor of Prunella was present in the Sino‐Himalayan Mountains or these mountains and Central Asia–Mongolia more than 9 million years ago (mya), but a burst of speciations took place during the mid‐Pliocene to early Pleistocene. The relationships among the six primary lineages resulting from that differentiation are unresolved, probably because of the rapid radiation. A general increase in sympatry with increasing time since divergence is evident. With one exception, species in clades younger than c. 3.7 my are allopatric. Species that are widely sympatric, including the most recently diverged (2.4 mya) sympatric sisters, are generally more divergent in size/structure than allo‐/parapatric close relatives. The distributional pattern and inferred ages suggest divergence in allopatry and substantial waiting time until secondary contact, likely due to competitive exclusion. All sympatrically breeding species are ecologically segregated, as suggested by differences in size/structure and habitat. Colonizations of new areas were facilitated during glacial periods, followed by fragmentation during interglacials—contrary to the usual view that glacial periods resulted mainly in fragmentations.