Living with uncertainty: genetic imprints of climate shifts in East Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax)

In the upwelling zone of the northeastern Pacific, cold nutrient-rich conditions alternate with warm nutrient-poor intervals on timescales ranging from months to millennia. In this setting, the abundances of Pacific sardine (Sardinops sagax) and northern anchovy (Engraulis mordax) fluctuate by several orders of magnitude, with sardine dominating during warm conditions and anchovy dominating during cool conditions. Two population models can explain the response of these fishes to adverse conditions. Under the basin model, species distributions contract to a central (optimal) range during population crashes. Expectations of this model may include a single range-wide population with a decline in genetic diversity on both sides of a central refuge. In contrast, the self-recruitment model invokes a series of local oceanographic domains that maintain semi-isolated subpopulations. During adverse conditions, some subpopulations cannot complete the life cycle within the local environment and are extirpated. Expectations of this model include some degree of population genetic structure and no clear gradient in genetic diversity. We examined mitochondrial DNA cytochrome b sequences to assess these competing models for anchovy (N = 196; 539 bp) and sardine (N = 107; 425 bp). The mitochondrial DNA gene genealogies are shallow but diverse for both species. Haplotype frequencies are homogeneous among subpopulations, but genetic diversities peak for both species along Baja California and adjacent southern California. Mismatch distributions and Tajima's D-values reveal distinctive signatures of population bottlenecks and expansions. Sardine haplotypes coalesce at approximately 241,000 years bp, with an initial female effective population size Nf0 = 0 followed by exponential growth to Nf1 = 115 million. Anchovy haplotypes coalesce at approximately 282,000 years bp, with an initial population size of Nf0 = 14,000, followed by exponential growth to Nf1 = 2.3 million. These results indicate a founder event for sardine and a severe population decline for anchovy in the California Current during the late Pleistocene. Overall, these data support the basin model on decadal timescales, although local recruitment may dominate on shorter timescales.     

Isolation of polymorphic microsatellite loci from the European anchovy,Engraulis encrasicolus

The European anchovy (Engraulis encrasicolus L., Engraulidae) is a widely spread fish resource which is overexploited along its area of distribution. A proper knowledge of the population genetic structure of this fish species is crucial to allow a sustainable management of fishery stocks. We developed five polymorphic microsatellite loci (expected heterozygosity per locus ranging from 0.46 to 0.97) for E. encrasicolus. These genetic markers can be applied to define the population genetic structure of European anchovy.     

A Second Look at Mitochondrial DNA Variability in European Anchovy (Engraulis encrasicolus): Assessing Models of Population Structure and the Black Sea Isolation Hypothesis

Genetic architectures of marine fishes are generally shallow because of the large potential for gene flow in the sea. European anchovy, however, are unusual among small pelagic fishes in showing large differences among sub-basins and in harbouring two mtDNA phylogroups (‘A’ & ‘B’), representing 1.1–1.85 million years of separation. Here the mtDNA RFLP dataset of Magoulas et al. [1996, Mol. Biol. Evol. 13: 178–190] is re-examined to assess population models accounting for this subdivided population structure and to evaluate the zoogeographical origins of the two major phylogroups. Haplotype and nucleotide diversities are highest in the Ionian Sea and lowest in the Aegean and Black seas. However, this gradient is absent when ‘A’ and ‘B’ haplotypes are examined separately. Neither the self-sustaining nor the basin population models adequately describe anchovy population behaviour. Tests for neutrality, mismatch and nested clade analyses are concordant in depicting recent expansions of both phylogroups. Unimodel mismatch distributions and haplotype coalescences dating to the last (Eemian) interglacial (‘B’) and the Weichselian pleniglacial period (‘A’) indicate separate colonizations of the Mediterranean Basin. Phylogroup ‘A’ is unlikely to have arisen through continuous long-term isolation in the Black Sea because of climate extremes from displaced subpolar weather systems during the ice ages. Ancestors of both groups appear to have colonized the Mediterranean from the Atlantic in the late Pleistocene. Hence, zoogeographic models of anchovy in the Mediterranean must also include the eastern (and possibly southern) Atlantic.     

Polymorphic microsatellite markers for stock identification in Japanese anchovy (Engraulis japonica)

Japanese anchovy (Engraulis japonica) is a migratory marine fish of high economic significance in Taiwan. The adult Japanese anchovies migrate from the East China sea to spawn in coastal waters of Taiwan; the larvae then drift back to the East China Sea to complete their life cycle. We developed six highly polymorphic microsatellites for E. Japonica (expected heterozygosity ranging from 0.751 to 0.971) and these microsatellites can be used as genetic markers for identifying stocks to establish regulations in fishing management. Moreover, the markers will be useful in inferring the stock origins and migration routes in the future.     

Conservation status of the White-Bellied Sea-Eagle <Emphasis Type="Italic">Haliaeetus leucogaster</Emphasis> in Australia determined using mtDNA control region sequence data

Considered to have a declining world population, concern has been expressed in recent years over the conservation status of the White-bellied Sea-Eagle Haliaeetus leucogaster (Gmelin, 1788) within Australia. We used mitochondrial (mtDNA) control region sequence data to investigate the current distribution of genetic variation in this species at the continental level and within and between specified regional units. We were specifically interested in identifying breaks in genetic connectivity between the west and east of the continent and between Tasmania and the Australian mainland. We also investigated the likelihood of a bottleneck at the time of colonisation, and propose hypotheses regarding colonisation history. Sequence data were obtained from 128 individuals describing 15 haplotypes. Overall, diversity was low and AMOVA results failed to provide any significant level of genetic subdivision between regions. We suggest that the population expanded from a bottleneck approximately 160,000 years ago during the late Pleistocene, and spread throughout the continent through a contiguous range expansion. There is insufficient evidence to suggest division of the population into different units for conservation management purposes based on the theoretical definition of the ‘evolutionary significant unit’. It is clear from the analysis that there are signatures of both historical and contemporary processes affecting the current distribution. Additional sampling and confirmation of the perceived pattern of population structure using a nuclear marker is recommended to validate conservation monitoring and management at a continental scale.     

The homogenous genetic structure and inferred unique history of range shifts during the Pleistocene climatic oscillations of <Emphasis Type="Italic">Arcterica nana</Emphasis> (Maxim.) Makino (Ericaceae)

Previous phylogeographic studies of alpine plants in Japan have inferred that populations in central Honshu persisted during the Pleistocene climatic oscillations and suggested interglacial survival in high mountains. However, Arcterica nana (Maxim.) Makino (Ericaceae) exhibits a homogenous genetic structure throughout Japan and may therefore have a unique phylogeographic history. This inconsistency could have resulted from insufficient resolution of previously analyzed chloroplast DNA sequences. Therefore, we conducted a phylogeographic investigation based on amplified fragment length polymorphisms. Using 176 individuals from 21 populations, the relationships among individuals and populations were determined by principal coordinate analysis and a neighbor-joining tree, respectively. In addition, genetic differentiation was estimated using analysis of molecular variance and spatial autocorrelation analysis. These analyses demonstrate a homogenous structure throughout the entire Japanese range, supporting the previous cpDNA phylogeography. Although this genetic structure is inconsistent with those of other alpine plants, it is difficult to postulate that pre-existing genetic differentiation was swamped exclusively within A. nana. Therefore, this homogenous genetic structure may have been caused by the distinct history of populations of A. nana. Specifically, the southern-ward migration and the subsequent continuous populations enabled gene flow throughout the Japanese archipelago during the last glacial period. Thus, our data suggest that alpine plants in the Japanese archipelago did not always experience a shared distribution change following climatic oscillations.     

Living in a tilted world: climate change and geography limit speciation in Old World anchovies (Engraulis; Engraulidae)

Historical changes in the distributions of temperate species in response to Milankovitch climate cycles have been well documented in palaeontological studies and recently evaluated with phylogeographical methods. How these cycles influence biological diversity remains a matter of debate. Molecular surveys of terrestrial and freshwater fauna demonstrate glacial refugia in low latitudes and range expansions into high latitudes, but few genetic studies have assessed the corresponding impact on marine fauna. In the present study, mtDNA sequences (N = 84) are surveyed to understand the impact of long‐term climate oscillations on ‘Old World’ anchovies (genus Engraulis), a monophyletic group occurring in north and south temperate zones of the eastern Atlantic and the western Pacific. The analysis of a 521‐bp sequence of mtDNA cytochrome b indicates a late Miocene or Pliocene dispersal from the north‐eastern Pacific (California–Mexico) to the north‐western Pacific (Japan), followed by Pleistocene dispersal from the north‐western Pacific to Europe. Geography mandates that populations in southern Africa and Australia were stepping‐stones for this dispersal. However, neither population occupies an intermediate position in the mtDNA genealogy; both populations are more recently derived from their northern neighbours. Haplotype diversity is high (h = 0.93–0.97) in European, Australian, and Japanese anchovies, but low (h = 0.22) in the southern African population, where all haplotypes are more closely related to European specimens than to each other. These southern populations occupy a precarious position, lacking north–south coastlines that allow range shifts during climatic extremes. Recurring extinctions and episodic recolonizations from northern hemisphere populations are the likely results. In this case, ocean‐climatic changes retard rather than enhance opportunities for evolutionary radiations. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88 , 673–689.     

Phylogeography of the black fly Simulium tani (Diptera: Simuliidae) from Thailand as inferred from mtDNA sequences

Intraspecific phylogeography has been used widely as a tool to infer population history. However, little attention has been paid to Southeast Asia despite its importance in terms of biodiversity. Here we used the cytochrome oxidase I gene of mitochondrial DNA (mtDNA) for a phylogeographic study of 147 individuals of the black fly Simulium tani from Thailand. The mtDNA revealed high genetic differentiation between the major geographical regions of north, east and central/south Thailand. Mismatch distributions indicate population expansions during the mid-Pleistocene and the late Pleistocene suggesting that current population structure and diversity may be due in part to the species' response to Pleistocene climatic fluctuations. The genealogical structure of the haplotypes, high northern diversity and maximum-likelihood inference of historical migration rates, suggest that the eastern and central/southern populations originated from northern populations in the mid-Pleistocene. Subsequently, the eastern region had had a largely independent history but the central/southern population may be largely the result of recent (c. 100,000 years ago) expansion, either from the north again, or from a relictual population in the central region. Cytological investigation revealed that populations from the south and east have two overlapping fixed chromosomal inversions. Since these populations also share ecological characteristics it suggests that inversions are involved in ecological adaptation. In conclusion both contemporary and historical ecological conditions are playing an important role in determining population genetic structure and diversity.     

Low genetic diversity and biased distribution of mitochondrial DNA haplotypes in the Japanese macaque (Macaca fuscata yakui) on Yakushima Island

The Japanese macaques (Macaca fuscata yakui) on Yakushima Island are an endemic subspecies and are closely related to the population of Kyushu, one of the main islands of Japan. Using feces collected throughout Yakushima Island, we examined mitochondrial DNA (mtDNA) to investigate the phylogeography of Japanese macaques. Six haplotypes were observed for a 203-bp fragment of the mtDNA control region. The nucleotide diversity () was low (0.0021). The genetic divergence within the Yakushima population was lower (0.009) than that among four haplotypes of the Kyushu population (0.015), calculated using Kimuras two-parameter method. The mismatch distribution analysis of the six haplotypes of the Yakushima population suggested that the Yakushima population had experienced a sudden expansion in population size, which could be related to the bottleneck effect. The geographic distribution of the mtDNA haplotypes was not uniform. One haplotype was distributed widely, whereas the other five haplotypes were distributed only in the lowlands. The low genetic diversity and biased distribution are discussed in relation to an environmental crash caused by ancient volcanic activity near this island, which is postulated to have happened about 7,300 years ago, and the delayed recovery of highland vegetation.     

Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): past fragmentation and island colonization in the Brazilian Atlantic Forest

The Brazilian Atlantic Forest is one of the world's major biodiversity hotspots and is threatened by a severe habitat loss. Yet little is known about the processes that originated its remarkable richness of endemic species. Here we present results of a large-scale survey of the genetic variation at the mitochondrial cytochrome b gene of the pitviper, jararaca lancehead (Bothrops jararaca), and two closely related insular species (Bothrops insularis and Bothrops alcatraz), endemic of this region. Phylogenetic and network analyses revealed the existence of two well-supported clades, exhibiting a southern and a northern distribution. The divergence time of these two phylogroups was estimated at 3.8 million years ago, in the Pliocene, a period of intense climatic changes and frequent fragmentation of the tropical rainforest. Our data also suggest that the two groups underwent a large size expansion between 50,000 and 100,000 years ago. However, the southern group showed a more marked signal of population size fluctuation than the northern group, corroborating evidences that southern forests may have suffered a more pronounced reduction in area in the late Pleistocene. The insular species B. alcatraz and B. insularis presented very low diversity, each one sharing haplotypes with mainland individuals placed in different subclades. Despite their marked morphological and behavioural uniqueness, these two insular species seem to have originated very recently and most likely from distinct costal B. jararaca populations, possibly associated with late Pleistocene or Holocene sea level fluctuations.     

Polymorphic microsatellite loci for the Japanese anchovy Engraulis japonicus (Engraulidae)

We isolated and characterized 14 polymorphic microsatellite loci in the Japanese anchovy (Engraulis japonicus) using a (GT)(13)-enriched genomic library. The numbers of alleles per locus ranged from 6 to 31, with a mean of 17.8. The observed and expected heterozygosities ranged from 0.180 to 0.949 and from 0.172 to 0.966, with means of 0.731 and 0.825, respectively. All 14 loci were in Hardy-Weinberg equilibrium and no significant linkage disequilibrium between loci pairs was detected. These microsatellite markers will be useful for analyzing the population genetic structure and gene flow of E. japonicus.     

Phylogeography of Diadophis punctatus: extensive lineage diversity and repeated patterns of historical demography in a trans-continental snake

Dynamic climatic oscillations during the Pleistocene had profound effects on the distributions of species across North America. Although the role of historical climate change on speciation remains controversial, the impact on genetic variation within species has been well documented. We examined mtDNA sequences from the cytochrome b gene (1117 bp) and a portion of the NADH-4 gene (659 bp) for 286 individuals of Diadophis punctatus to infer phylogeographic patterns and population structure and to examine historical demographic patterns in both glaciated and unglaciated regions of North America. We inferred 14 lineages that replace each other geographically across the United States. Several of these lineages appear to be confined to specific habitats (floodplains, grasslands, montane environments) and traverse previously identified genetic barriers for terrestrial vertebrates including the Mississippi and Apalachicola Rivers, the Appalachian Mountains, and the western continental divide. We also observed overlapping ranges between some haplotype groups and several instances of secondary contact associated with ecological transition zones in eastern South Carolina, southern Oklahoma and central California. Within the US, diversification began during the late Miocene and continued into the mid-Pleistocene, suggesting these lineages pre-dated the last glacial maximum. Coalescent and non-coalescent demographic analyses indicate that independent lineages currently occupying previously glaciated or unsuitable areas in eastern, central and western US underwent post-glacial population expansion likely from southern refugia during the late Pleistocene/early Holocene. Conversely, southern lineages display patterns consistent with long-term population stability. Such long-term persistence of genetic structure may be due to the competitive effects between lineages or ecosystem stability in more southern latitudes.     

Field mortality estimates of anchovy larvae, Engraulis encrasicolus, in the western Mediterranean

Eggs and larvae of anchovy were obtained from plankton collections made along the Catalan coast (north-western Mediterranean) from 1983 to 1985 in order to determine spawning seasons and areas and other aspects of its life history. Previous studies have shown the existence of two main spawning areas, to the north and south of the Catalan coast, respectively. The northern one is characterized by a shorter spawning period related with the thermal cycle.
Mortality rates of larvae aged 4.9-15 days were calculated from the peak spawning month (June) of the three years, separately by spawning areas. Data on abundance by length classes were adjusted for escape and net avoidance and for duration of growth through a size class as derived from otolith readings. Mortality rates ranged from 0.17 to 0.58. Mortality was higher in 1983 than in 1984 and 1985, coinciding with a high production of anchovy eggs in that year. Mortality at the northern spawning area was lower than at the southern one.     

Phylogeography recapitulates topography: very fine-scale local endemism of a saproxylic 'giant' springtail at Tallaganda in the Great Dividing Range of south-east Australia

Comparative phylogeography can reveal processes and historical events that shape the biodiversity of species and communities. As part of a comparative research program, the phylogeography of a new, endemic Australian genus and species of log-dependent (saproxylic) collembola was investigated using mitochondrial sequences, allozymes and anonymous single-copy nuclear markers. We found the genetic structure of the species corresponds with five a priori microbiogeographical regions, with population subdivision at various depths owing to palaeoclimatic influences. Closely related mtDNA haplotypes are codistributed within a single region or occur in adjacent regions, nuclear allele frequencies are more similar among more proximate populations, and interpopulation migration is rare. Based on mtDNA divergence, a late Miocene-late Pliocene coalescence is likely. The present-day distribution of genetic diversity seems to have been impacted by three major climatic events: Pliocene cooling and drying (2.5-7 million years before present, Mybp), early Pleistocene wet-dry oscillations (c. 1.2 Mybp) and the more recent glacial-interglacial cycles that have characterized the latter part of the Quaternary (<0.4 Mybp).     

Growth of larval Pacific anchovy Engraulis japonicus in the Yellow Sea as indicated by otolith microstructure analysis

Larval Pacific anchovy Engraulis japonicus were sampled from coastal waters off the central west coast of Korea from June to November 1996. Using otolith microstructure analysis (daily growth increments), three cohorts (spring, early summer and late summer) were distinguished based on backcalculated spawning dates. Growth rates differed between cohorts, with higher growth rates for late-summer cohorts than either the spring or early-summer cohorts. Growth rate was positively related to surface water temperature, with an optimum temperature range of between 20 and 26° C occurring during the late summer (late July through to mid-September). The study highlights that early growth rates of Pacific anchovy are dependent on ecosystem (particularly water temperature) attributes during early life.     

Shaping of genetic structure along Pleistocene and modern river systems in the hydrochorous riparian azalea, Rhododendron ripense (Ericaceae)

To determine the effects of hydrochory on the formation of the present range of a species and the spatial distribution of genetic variation, we assessed the rangewide genetic structure of a hydrochorous riparian Japanese species (Rhododendron ripense) using four nuclear microsatellite loci. The patterns of isolation by distance and Bayesian clustering analyses of 33 populations suggested that the present range, characterized by both localized and disjunct distributions across the sea, arose from two contrasting colonization events: (1) primary colonization along two Pleistocene rivers that have been submerged and become partly isolated by marine transgression by 6000 years ago, and (2) additional range expansions from these rivers into unconnected neighboring rivers as a result of river captures. Along the Pleistocene rivers, frequent gene flow by hydrochory resulted in the retention of considerable genetic diversity within each population and genetic homogenization among populations. Within unconnected neighboring rivers, genetic diversity was also retained by the simultaneous redistribution of many individuals as a result of river captures, whereas restricted gene flow within a river resulted in genetic divergence among the river populations. Thus, the evolutionary history of hydrochorous R. ripense appears to have been strongly shaped by both ancient and modern rivers.     

Phylogeography of the common shrimp, Crangon crangon (L.) across its distribution range

The common or brown shrimp Crangon crangon (L.) is a highly abundant and important taxon, both ecologically and commercially, yet knowledge on its population structure and historical biogeography is limited. We studied population genetic structure across the distribution range of this species by sequencing a 388 bp fragment of the cytochrome-c-oxidase I gene for 140 individuals from 25 locations. Strong population structuring and high levels of genetic diversity were observed. Four main phylogroups were uncovered: northeastern Atlantic, western Mediterranean, Adriatic Sea and Black Sea. Gene flow of these shrimp across known oceanographical barriers (e.g., the Strait of Gibraltar and/or Oran-Almeria front, Sicilian Straits, and Turkish Straits) is severely restricted. The oldest and most variable populations currently inhabit the western Mediterranean. The observed absence of structure across the entire northeastern Atlantic shelf is proposed not to be due to gene flow, but to relatively recent colonization following the glacial cycles of the late Pleistocene. Black Sea shrimp are currently disconnected from Mediterranean populations, and colonization is inferred, on the basis of coalescent analysis, to have happened relatively recently, but possibly earlier than 7000 years ago. We postulate the hypothesis that C. crangon survived the last brackish-water (<7 per thousand) period inside the Black Sea and/or one of the adjacent inland seas. We conclude that (1) common shrimp populations from different basins are strongly differentiated, (2) gene flow across basins is probably very limited, and (3) the biogeographic history of the taxon is largely in accordance with the geographic history of its distribution range. This study provides further evidence that high population connectivity of marine species (e.g., by policy makers) should not be assumed.     

Phylogeography of Simulium siamense Takaoka and Suzuki complex (Diptera: Simuliidae) in Thailand

The phylogeography of Simulium siamense complex was inferred from mitochondrial DNA sequences. A 586‐bp fragment of the cytochrome oxidase I was sequenced for 92 individuals from 13 populations throughout Thailand, representing five cytoforms (A, B, C, F and G). The cytoforms are not genetically different at the molecular level except for cytoform B, which is genetically distinct from the others. This might indicate that cytoform B is a distinct species. Further morphological and molecular work using other genes is needed to clarify this. Our results also argue for the need of integrated approach, both cytological and molecular studies to understanding biodiversity of black flies. The star‐like shape of the mtDNA genealogy is consistent with the sudden population expansion of the mismatch distribution analysis and large negative values of Fu's F_s and Tajima's D‐tests, indicating a population demographic expansion. The expansion time is estimated to be in the late Pleistocene (about 120 000 years ago). Therefore, the overall low level of genetic structure could be due to sharing a recent history. The ancestral haplotype was found in the mountainous area in northeastern Thailand, suggesting that this area could have been the refugium of the species complex during the Pleistocene glaciations. Our results are consistent with previous findings about population expansion in response to the Pleistocene climatic change, thus revealing the importance of this historical event in shaping the genetic structure and diversity of Southeast Asian mainland species.     

Low genetic diversity and significant population structuring in the relict Amentotaxus argotaenia complex (Taxaceae) based on ISSR fingerprinting

Amentotaxus, a genus of the Taxaceae, represents an ancient lineage that has long existed in Eurasia. All Amentotaxus species experienced frequent population expansion and contraction over periodical glaciations in Tertiary and Quaternary. Among them, Amentotaxus argotaenia complex consists of three morphologically alike species, A. argotaenia, Amentotaxus yunnanensis, and Amentotaxus formosana. This complex is distributed in the subtropical region of mainland China and Taiwan where many Pleistocene refugia have been documented. In this study, genetic diversity and population structuring within and between species were investigated based on the inter-simple sequence repeats (ISSR) fingerprinting. Mean genetic diversity within populations was estimated in three ways: (1) the percentage of polymorphic loci out of all loci (P) (2) Neis unbiased expected heterozygosity (He), and (3) Shannons index of phenotypic diversity. For a total of 310 individuals of 15 populations sampled from the three species, low levels of ISSR genetic variation within populations were detected, with P=4.66–16.58%, He=0.0176–0.0645 and Hpop=0.0263–0.0939, agreeing with their seriously threatened status. AMOVA analyses revealed that the differences between species only accounted for 27.38% of the total variation, whereas differences among populations and within populations were 57.70 and 14.92%, respectively, indicating substantial isolation between the patch-like populations. A neighbor-joining tree identified a close affinity between A. yunnanensis and A. formosana. Genetic drift due to small population size, plus limited current gene flow, resulted in significant genetic structuring. Low levels of intrapopulational genetic variation and considerable interpopulational divergence were also attributable to demographic bottlenecks during and/or after the Pleistocene glaciations.     

Phylogeography and paleodistribution models of a widespread birch (Betula platyphylla Suk.) across East Asia: Multiple refugia,multidirectional expansion,and heterogeneous genetic pattern

Widespread tree species cover large geographical areas and play important roles in various vegetation types. Understanding how these species responded to historical climatic changes is important for understanding community assembly mechanisms with evolutionary and conservation implications. However, the location of refugial areas and postglacial history of widespread trees in East Asia remain poorly known. We combined microsatellite data (63 populations, 1756 individuals) and ecological niche modeling to examine the range‐wide population diversity, genetic structure, and historical demography of a pioneer tree species, Asian white birch (Betula platyphylla Suk.) across East Asia. We found a north‐to‐south trend of declining genetic diversity and five clusters, corresponding to geographical regions. Different clusters were inferred to have diverged through Pleistocene climatic oscillations and have different expansion routes, leading to genetic admixture in some populations. Ecological niche models indicated that the distribution of B. platyphylla during the last glacial maximum still had a large latitude span with slight shifts toward southeast, and northern populations had more variable distribution ranges than those in the south during later climatic oscillations. Our results reflect the relatively stable distribution through the last glacial–interglacial cycles and recent multidirectional expansion of B. platyphylla, providing new hypotheses for the response pattern of widespread tree species to climate change. The gradual genetic pattern from northeast to southwest and alternative distribution dynamics possibly resulted from environmental differences caused by latitude and topographic heterogeneity.