Shou Hsien Li

Phylogeography of the Alcippe morrisonia (Aves: Timaliidae): long population history beyond late Pleistocene glaciations

BackgroundThe role of Pleistocene glacial oscillations in current biodiversity and distribution patterns varies with latitude, physical topology and population life history and has long been a topic of discussion. However, there had been little phylogeographical research in south China, where the geophysical complexity is associated with great biodiversity. A bird endemic in Southeast Asia, the Grey-cheeked Fulvetta, Alcippe morrisonia, has been reported to show deep genetic divergences among its seven subspecies. In the present study, we investigated the phylogeography of A. morrisonia to explore its population structure and evolutionary history, in order to gain insight into the effect of geological events on the speciation and diversity of birds endemic in south China.ResultsMitochondrial genes cytochrome b (Cytb) and cytochrome c oxidase I (COI) were represented by 1236 nucleotide sites from 151 individuals from 29 localities. Phylogenetic analysis showed seven monophyletic clades congruent with the geographically separated groups, which were identified as major sources of molecular variance (90.92%) by AMOVA. TCS analysis revealed four disconnected networks, and that no haplotype was shared among the geographical groups. The common ancestor of these populations was dated to 11.6 Mya and several divergence events were estimated along the population evolutionary history. Isolation by distance was inferred by NCPA to be responsible for the current intra-population genetic pattern and gene flow among geographical groups was interrupted. A late Pleistocene demographic expansion was detected in the eastern geographical groups, while the expansion time (0.2–0.4 Mya) was earlier than the Last Glacial Maximum.ConclusionIt is proposed that the complicated topology preserves high genetic diversity and ancient lineages for geographical groups of A. morrisonia in China mainland and its two major islands, and restricts gene exchange during climate oscillations. Isolation by distance seems to be an important factor of genetic structure formation within geographical populations. Although glacial influence to population fluctuation was observed in late Pleistocene, it seems that populations in eastern China were more susceptible to climate change, and all geographical groups were growing stably through the Last Glacial Maximum. Coalescence analysis suggested that the ancestor of A. morrisonia might be traced back to the late Miocene, and the current phylogeographical structure of A. morrisonia is more likely to be attributable to a series geological events than to Pleistocene glacial cycles.

Sailing through the Late Pleistocene: unusual historical demography of an East Asian endemic, the Chinese Hwamei (Leucodioptron canorum canorum), during the last glacial period

Pleistocene climate fluctuations shaped the patterns of genetic diversity observed in extant species. In contrast to Europe and North America where the effects of recent glacial cycles on genetic diversity have been well studied, the genetic legacy of the Late Pleistocene for East Asia, a region of great topographical complexity and presumably milder historical climate, remains poorly understood. We analysed 3.86 kb of the mitochondrial genome of 186 Chinese Hwamei birds, Leucodioptron canorum canorum, and found that contrary to the conventional expectation of population decline during cold periods (stadials), the demographic history of this species shows continuous population growth since the penultimate glacial period (about 170 000 years ago). Refugia were identified in the south, coastal regions, and northern inland areas, implying that topographic complexity played a substantial role in providing suitable habitats for the Chinese Hwamei during cold periods. Intermittent gene flow between these refugia during the warmer periods (interstadials) might have resulted in a large effective population of this bird through the last glacial period.

Postglacial colonization of the Tibetan plateau inferred from the matrilineal genetic structure of the endemic red-necked snow finch, Pyrgilauda ruficollis

Most phylogeographical studies of postglacial colonization focus on high latitude locations in the Northern Hemisphere. Here, we studied the phylogeographical structure of the red‐necked snow finch Pyrgilauda ruficollis, an endemic species of the Tibetan plateau. We analysed 879 base pairs (bp) of the mitochondrial cytochrome b gene and 529 bp of the control region in 41 birds from four regional groups separated by mountain ranges. We detected 34 haplotypes, 31 of which occurred in a single individual and only three of which were shared among sampling sites within regional groups or among regional groups. Haplotype diversity was high (h = 0.94); nucleotide diversity was low (ð = 0.00415) and genetic differentiation was virtually non‐existent. Analyses of mismatch distributions and geographically nested clades yielded results consistent with contiguous range expansion, and the expansion times were estimated as 0.07–0.19 million years ago (Ma). Our results suggest that P. ruficollis colonized the Tibetan plateau after the extensive glacial period (0.5–0.175 Ma), expanding from the eastern margin towards the inner plateau. Thus, in contrast to many of the postglacial phylogeographical structures known at high latitudes, this colonization occurred without matrilineal population structuring. This might be due to the short glacial cycles typical of the Tibetan plateau, adaptation of P. ruficollis to cold conditions, or refugia and colonized habitat being semicontinuous and thus promoting population mixing.

Faecal DNA typing to determine the abundance and spatial organisation of otters ( Lutra lutra ) along two stream systems in Kinmen

In this study, non-invasive molecular methods were used to investigate the abundance and spatial organisation of otters (Lutra lutra) in Kinmen. DNA samples were extracted from fresh spraints collected seasonally along two streams from February to November 2001 and genotyped using a panel of 7 microsatellites and the SRY gene. Out of 343 spraints, 222 were successfully genotyped and 38 different genotypes (19 females and 19 males) were identified. Thirteen of these were residents that were identified in more than one season and 25 were floaters that were only identified in a single season. The average number of otters per km found along the two streams (1.5–1.8 for all otters, or 0.8–1.1 for residents only) was higher than that estimated in other studies. Female residents lived in exclusive group ranges and the ranges of male residents overlapped with no more than one group range of female residents. Otters appearing in the same range tended to be more closely related to each other. This study demonstrates that non-invasive molecular methods can be used to reveal a more comprehensive estimation of size and structure in an otter population.

Drastic population fluctuations explain the rapid extinction of the passenger pigeon

Significance The number of passenger pigeons went from billions to zero in mere decades, in contrast to conventional wisdom that enormous population size provides a buffer against extinction. Our understanding of the passenger pigeon’s extinction, however, has been limited by a lack of knowledge of its long-term population history. Here we use both genomic and ecological analyses to show that the passenger pigeon was not always super abundant, but experienced dramatic population fluctuations, which could increase its vulnerability to human exploitation. Our study demonstrates that high-throughput–based ancient DNA analyses combined with ecological niche modeling can provide evidence allowing us to assess factors that led to the surprisingly rapid demise of the passenger pigeon. To assess the role of human disturbances in species’ extinction requires an understanding of the species population history before human impact. The passenger pigeon was once the most abundant bird in the world, with a population size estimated at 3–5 billion in the 1800s; its abrupt extinction in 1914 raises the question of how such an abundant bird could have been driven to extinction in mere decades. Although human exploitation is often blamed, the role of natural population dynamics in the passenger pigeon’s extinction remains unexplored. Applying high-throughput sequencing technologies to obtain sequences from most of the genome, we calculated that the passenger pigeon’s effective population size throughout the last million years was persistently about 1/10,000 of the 1800’s estimated number of individuals, a ratio 1,000-times lower than typically found. This result suggests that the passenger pigeon was not always super abundant but experienced dramatic population fluctuations, resembling those of an “outbreak” species. Ecological niche models supported inference of drastic changes in the extent of its breeding range over the last glacial–interglacial cycle. An estimate of acorn-based carrying capacity during the past 21,000 y showed great year-to-year variations. Based on our results, we hypothesize that ecological conditions that dramatically reduced population size under natural conditions could have interacted with human exploitation in causing the passenger pigeon’s rapid demise. Our study illustrates that even species as abundant as the passenger pigeon can be vulnerable to human threats if they are subject to dramatic population fluctuations, and provides a new perspective on the greatest human-caused extinction in recorded history.

Rejecting strictly allopatric speciation on a continental island: prolonged postdivergence gene flow between Taiwan (Leucodioptron taewanus, Passeriformes Timaliidae) and Chinese (L. canorum canorum) hwameis

Allopatry is conventionally considered the geographical mode of speciation for continental island organisms. However, strictly allopatric speciation models that assume the lack of postdivergence gene flow seem oversimplified given the recurrence of land bridges during glacial periods since the late Pliocene. Here, to evaluate whether a continental island endemic, the Taiwan hwamei (Leucodioptron taewanus, Passeriformes Timaliidae) speciated in strict allopatry, we used weighted‐regression‐based approximate Bayesian computation (ABC) to analyse the genetic polymorphism of 18 neutral nuclear loci (total length: 8500 bp) in Taiwan hwamei and its continental sister species, the Chinese hwamei (L. canorum canorum). The nonallopatry model was found to fit better with observed genetic polymorphism of the two hwamei species (posterior possibility = 0.82). We also recovered unambiguous signals of nontrivial bidirectional postdivergence gene flow (Nem » 1) between Chinese hwamei and Taiwan hwamei until 0.5 Ma. Divergence time was estimated to be 3.5 to 2  million years earlier than that estimated from mitochondrial cytochrome b sequences. Finally, using the inferred nonallopatry model to simulate genetic variation at 24 nuclear genes examined showed that the adiponectin receptor 1 gene may be under divergent adaptation. Our findings imply that the role of geographical barrier may be less prominent for the speciation of continental island endemics, and suggest a shift in speciation studies from simply correlating geographical barrier and genetic divergence to examining factors that facilitate and maintain divergence, e.g. differential selection and sexual selection, especially in the face of interpopulation gene flow.

Incomplete lineage sorting or secondary admixture: Disentangling historical divergence from recent gene flow in the Vinous-throated parrotbill (Paradoxornis webbianus)

Although Pleistocene glaciations had a major impact on the population genetic patterns of many species in North America and Europe, it remains unclear how these climatic fluctuations contributed to species diversification in East Asia. One reason for this is the difficulty of distinguishing genetic admixture following secondary contact from incomplete lineage sorting, both of which can generate similar patterns of genetic variation. Using a combination of multilocus analyses and coalescent simulation, we explore how these two processes occurred in the Pleistocene evolutionary history of a widespread East Asian bird, the Vinous‐throated parrotbill, Paradoxornis webbianus. Maximum likelihood (ML) tree identified two major mitochondrial lineages, which are geographically separated in most parts of its range, but are sympatric at a few sampling sites. NJ tree and Structure analysis of microsatellite data set revealed an extensive level of admixture and little population structure, suggesting recent admixture between two formerly separated groups. Networks from nuclear DNA data sets, however, did not indicate any geographically isolated groups but rather a panmictic population, thus support incomplete lineage sorting. By using coalescent simulation approaches, we show that both processes did occur, although at different temporal scales. During the Pleistocene glaciations, probably around 0.1–0.5 Ma (the Marine Isotope Stage 6, MIS6), P. webbianus contracted into two separate refugia, and subsequently accumulated genetic divergence. During the interglacial MIS5, the species expanded into previously glaciated areas allowing the once separated groups to come into contact and become admixed. Taken together, our results indicate the current genetic variation within P. webbianus is a combination pattern of widespread distribution in pre‐Pleistocene, then contraction and fragmentation into separated refugia during glacial advance, followed by recently postglacial expansion and admixture.

Genome-wide misexpression of X-linked versus autosomal genes associated with hybrid male sterility

Postmating reproductive isolation is often manifested as hybrid male sterility, for which X-linked genes are overrepresented (the so-called large X effect). In contrast, X-linked genes are significantly under-represented among testis-expressing genes. This seeming contradiction may be germane to the X:autosome imbalance hypothesis on hybrid sterility, in which the X-linked effect is mediated mainly through the misexpression of autosomal genes. In this study, we compared gene expression in fertile and sterile males in the hybrids between two Drosophila species. These hybrid males differ only in a small region of the X chromosome containing the Ods-site homeobox (OdsH) (also known as Odysseus) locus of hybrid sterility. Of genes expressed in the testis, autosomal genes were, indeed, more likely to be misexpressed than X-linked genes under the sterilizing action of OdsH. Since this mechanism of X:autosome interaction is only associated with spermatogenesis, a connection between X:autosome imbalance and the high rate of hybrid male sterility seems plausible.

A phylogenetic analysis of laughingthrushes (Timaliidae: Garrulax) and allies based on mitochondrial and nuclear DNA sequences

The interspecific relationships among extant laughingthrushes have been unclear for a long time and this has resulted in a confusing taxonomic history. Recent advances in molecular methods have greatly improved the resolution of the phylogeny of birds; however, little works has been done on this specific group because of the inaccessibility to many species. This diverse group includes 50 species mostly distributed in South China and South‐east Asia, and were traditionally arranged into the genus Garrulax, for which the non monophyly had been questioned by previous molecular studies. In this study, we infer a phylogeny for 23 Garrulax species and 20 species from close related genera. Mitochondrial data or combined with nuclear sequences both indicate paraphyly of Garrulax, dividing Garrulax species into two groups. Based on these results, we suggest resurrecting the genus name Trochalopteron Blyth, 1843 for one group and retaining Garrulax for the other pending further study. Using dating methods with a secondary calibration point, we develop a profile of the speciation history of laughingthrushes, which suggests that the Hengduan Mountains might not be the centre of origin for these birds as previously suggested.

Interpreting the Process behind Endemism in China by Integrating the Phylogeography and Ecological Niche Models of the Stachyridopsis ruficeps

An area of endemism (AOE) is a complex expression of the ecological and evolutionary history of a species. Here we aim to address the principal drivers of avian diversification in shaping patterns of endemism in China by integrating genetic, ecological, and distributional data on the Red-headed Tree Babbler (Stachyridopsis ruficeps), which is distributed across the eastern Himalayas and south China. We sequenced two mtDNA markers from 182 individuals representing all three of the primary AOEs in China. Phylogenetic inferences were used to reconstruct intraspecific phylogenetic relationships. Divergence time and population demography were estimated to gain insight into the evolutionary history of the species. We used Ecological niche modeling to predict species’ distributions during the Last Glacial Maximum (LGM) and in the present. Finally, we also used two quantitative tests, an identity test and background test to assess the similarity of ecological niche preferences between adjacent lineages. We found five primary reciprocally monophyletic clades, typically separated approximately 0.2–2.27 MYA, of which three were deeply isolated endemic lineages located in the three AOEs. All phylogroups were detected to have undergone population expansion during the past 0.3 MY. Niche models showed discontinuous habitats, and there were three barriers of less suitable habitat during the LGM and in modern times. Ecoclimatic niches may diverge significantly even over recent timescales, as each phylogroup had a unique distribution, and unique niche characteristics. Vicariant events associated with geographical and ecological barriers, glacial refuges and ecological differentiation may be the main drivers forming the pattern of endemism in China.