Convergent evolution of kidney sizes and supraorbital salt glands for birds living in saline habitats.

Only a small number of avian species inhabit salty environments. To understand how they adapted, we examined the evolution of kidney sizes, supraorbital salt glands (SSGs), and the utilization of salty habitats across 230 species spanning 25 avian orders. Phylogenetic analysis indicates that SSGs, large kidneys, and thriving in salty habitats emerged convergently in birds. Transition rate analysis reveals that species possessing SSGs and large kidneys tended to move from low-to high-salinity environments, while others moved in the opposite direction. However, habitat salinity also influenced kidney evolution; lineages residing in high-salinity environments tended to develop larger kidneys than those in low-salinity environments. Our findings suggest that SSGs and large kidneys may have evolved through adaptation to high salinity. Overall, habitat conditions and physiological traits influenced avian adaptation to salty environments in a reciprocal manner. These results shed the new light on the evolutionary mechanisms underlying functional diversity in birds.

Low but highly geographically structured genomic diversity of East Asian Eurasian otters and its conservation implications.

Populations of Eurasian otters Lutra lutra, one of the most widely distributed apex predators in Eurasia, have been depleted mainly since the 1950s. However, a lack of information about their genomic diversity and how they are organized geographically in East Asia severely impedes our ability to monitor and conserve them in particular management units. Here, we re-sequenced and analyzed 20 otter genomes spanning continental East Asia, including a population at Kinmen, a small island off the Fujian coast, China. The otters form three genetic clusters (one of L. l. lutra in the north and two of L. l. chinensis in the south), which have diverged in the Holocene. These three clusters should be recognized as three conservation management units to monitor and manage independently. The heterozygosity of the East Asian otters is as low as that of the threatened carnivores sequenced. Historical effective population size trajectories inferred from genomic variations suggest that their low genomic diversity could be partially attributed to changes in the climate since the mid-Pleistocene and anthropogenic intervention since the Holocene. However, no evidence of genetic erosion, mutation load, or high level of inbreeding was detected in the presumably isolated Kinmen Island population. Any future in situ conservation efforts should consider this information for the conservation management units.

Potential millennial-scale avian declines by humans in southern China.

Mounting observational records demonstrate human-caused faunal decline in recent decades, while accumulating archaeological evidence suggests an early biodiversity impact of human activities during the Holocene. A fundamental question arises concerning whether modern wildlife population declines began during early human disturbance. Here, we performed a population genomic analysis of six common forest birds in East Asia to address this question. For five of them, demographic history inference based on 25-33 genomes of each species revealed dramatic population declines by 4- to 48-fold over millennia (e.g. 2000-5000 thousand years ago). Nevertheless, summary statistics detected nonsignificant correlations between these population size trajectories and Holocene temperature variations, and ecological niche models explicitly predicted extensive range persistence during the Holocene, implying limited demographic consequence of Holocene climate change. Further analyses suggest high negative correlations between the reconstructed population declines and human disturbance intensities and indicate a potential driver of human activities. These findings provide a deep-time and large-scale insight into the recently recognized avifaunal decline and support an early origin hypothesis of human effects on biodiversity. Overall, our study sheds light on the current biodiversity crisis in the context of long-term human-environment interactions and offers a multi-evidential framework for quantitatively assessing the ecological consequences of human disturbance.

Not out of the woods yet: Signatures of the prolonged negative genetic consequences of a population bottleneck in a rapidly re-expanding wader, the black-faced spoonbill Platalea minor.

The long-term persistence of a population which has suffered a bottleneck partly depends on how historical demographic dynamics impacted its genetic diversity and the accumulation of deleterious mutations. Here we provide genomic evidence for the genetic effect of a recent population bottleneck in the endangered black-faced spoonbill (Platalea minor) after its rapid population recovery. Our data suggest that the bird's effective population size, Ne , had been relatively stable (7500-9000) since 22,000 years ago; however, a recent brief yet severe bottleneck (Ne  = 20) which we here estimated to occur around the 1940s wiped out >99% of its historical Ne in roughly three generations. Despite a >15-fold population recovery since 1988, we found that black-faced spoonbill population has higher levels of inbreeding (7.4 times more runs of homozygosity) than its sister species, the royal spoonbill (P. regia), which is not thought to have undergone a marked population contraction. Although the two spoonbills have similar levels of genome-wide genetic diversity, our results suggest that selection on more genes was relaxed in the black-faced spoonbill; moreover individual black-faced spoonbills carry more putatively deleterious mutations (Grantham's score > 50), and may therefore express more deleterious phenotypic effects than royal spoonbills. Here we demonstrate the value of using genomic indices to monitor levels of genetic erosion, inbreeding and mutation load in species with conservation concerns. To mitigate the prolonged negative genetic effect of a population bottleneck, we recommend that all possible measures should be employed to maintain population growth of a threatened species.

Parallel genomic responses to historical climate change and high elevation in East Asian songbirds.

Parallel evolution can be expected among closely related taxa exposed to similar selective pressures. However, parallelism is typically stronger at the phenotypic level, while genetic solutions to achieve these phenotypic similarities may differ. For polygenic traits, the availability of standing genetic variation (i.e., heterozygosity) may influence such genetic nonparallelism. Here, we examine the extent to which high-elevation adaptation is parallel-and whether the level of parallelism is affected by heterozygosity-by analyzing genomes of 19 Paridae species distributed across East Asia with a dramatic east-west elevation gradient. We find that western highlands endemic parids have consistently lower levels of heterozygosity-likely the result of late-Pleistocene demographic contraction-than do parids found exclusively in eastern lowlands, which remained unglaciated during the late Pleistocene. Three widespread species (east to west) have high levels of heterozygosity similar to that observed in eastern species, although their western populations are less variable than eastern ones. Comparing genomic responses to extreme environments of the Qinghai-Tibet Plateau, we find that the most differentiated genomic regions between each high-elevation taxon and its low-elevation relative are significantly enriched for genes potentially related to the oxygen transport cascade and/or thermogenesis. Despite no parallelism at particular genes, high similarity in gene function is found among comparisons. Furthermore, parallelism is not higher in more heterozygous widespread parids than in highland endemics. Thus, in East Asian parids, parallel functional response to extreme elevation appears to rely on different genes, with differences in heterozygosity having no effect on the degree of genetic parallelism.

Morphological variations in a widely distributed Eastern Asian passerine cannot be consistently explained by ecogeographic rules.

Ecogeographic rules that describe quantitative relationships between morphologies and climate might help us predict how morphometrics of animals was shaped by local temperature or humidity. Although the ecogeographic rules had been widely tested in animals of Europe and North America, they had not been fully validated for species in regions that are less studied. Here, we investigate the morphometric variation of a widely distributed East Asian passerine, the vinous-throated parrotbill (Sinosuthora webbiana), to test whether its morphological variation conforms to the prediction of Bergmann's rule, Allen's rules, and Gloger's rule. We at first described the climatic niche of S. webbiana from occurrence records (n = 7838) and specimen records (n = 290). The results of analysis of covariance (ANCOVA) suggested that the plumage coloration of these parrotbills was darker in wetter/warmer environments following Gloger's rule. However, their appendage size (culmen length, beak volume, tarsi length) was larger in colder environments, the opposite of the predictions of Allen's rule. Similarly, their body size (wing length) was larger in warmer environments, the opposite of the predictions of Bergmann's rule. Such disconformity to both Bergmann's rule and Allen's rule suggests that the evolution of morphological variations is likely governed by multiple selection forces rather than dominated by thermoregulation. Our results suggest that these ecogeographic rules should be validated prior to forecasting biological responses to climate change especially for species in less-studied regions.

Genomic Consequences of Long-Term Population Decline in Brown Eared Pheasant.

Population genetic theory and empirical evidence indicate that deleterious alleles can be purged in small populations. However, this viewpoint remains controversial. It is unclear whether natural selection is powerful enough to purge deleterious mutations when wild populations continue to decline. Pheasants are terrestrial birds facing a long-term risk of extinction as a result of anthropogenic perturbations and exploitation. Nevertheless, there are scant genomics resources available for conservation management and planning. Here, we analyzed comparative population genomic data for the three extant isolated populations of Brown eared pheasant (Crossoptilon mantchuricum) in China. We showed that C. mantchuricum has low genome-wide diversity and a contracting effective population size because of persistent declines over the past 100,000 years. We compared genome-wide variation in C. mantchuricum with that of its closely related sister species, the Blue eared pheasant (C. auritum) for which the conservation concern is low. There were detrimental genetic consequences across all C. mantchuricum genomes including extended runs of homozygous sequences, slow rates of linkage disequilibrium decay, excessive loss-of-function mutations, and loss of adaptive genetic diversity at the major histocompatibility complex region. To the best of our knowledge, this study is the first to perform a comprehensive conservation genomic analysis on this threatened pheasant species. Moreover, we demonstrated that natural selection may not suffice to purge deleterious mutations in wild populations undergoing long-term decline. The findings of this study could facilitate conservation planning for threatened species and help recover their population size.

Strict allopatric speciation of sky island Pyrrhula erythaca species complex.

Increasing evidence of post-divergence gene flow between taxa is shifting our understanding on the mode of speciation. A fundamental question arises concerning the circumstances under which strict allopatric speciation still holds true. Sky island populations might undergo reduced gene flow by niche conservatism to highland habitats and follow divergence in an allopatric manner. In this study, we tested this hypothesis in the sky island Grey-headed Bullfinch (Pyrrhula erythaca) species complex via statistical analyses of both genetic and ecological data. Results of coalescent-based analysis of multiple nuclear loci suggested that P. e. owstoni likely colonized Taiwan island during the severe mid-Pleistocene glacial climate followed by strictly allopatric divergence from P. e. erythaca distributed in Himalayas-Hengduan mountains and central North China. Results of ecological niche modeling suggested that their speciation may be attributed to the niche conservatism of these birds and the lack of a suitable ecological corridor during subsequent milder glacial episodes. In addition, we delimited the traditionally defined P. erythaca into two full species, P. erythaca in the Asian mainland and P. owstoni on the island of Taiwan, based on both genetic and behavioural evidences. These results suggest that ecology can have a dynamic role in allowing highland populations to expand their ranges and isolated by habitat barriers to diversify in a strictly allopatric manner.

Disentangling the evolutionary history and biogeography of hill partridges (Phasianidae, Arborophila) from low coverage shotgun sequences.

The advent of the phylogenomic era has significantly improved our understanding of the evolutionary history and biogeography of Southeast Asia's diverse avian fauna. However, the taxonomy and phylogenetic relationships of many Southeast Asian birds remain poorly resolved, especially for those with large geographic ranges, which might have experienced both ancient and recent geological and environmental changes. In this study, we examined the evolutionary history and biogeography of the hill partridges (Galliformes: Phasianidae: Arborophila spp.), currently the second most speciose galliform genus, and thought to have colonized Southeast Asia from Africa. We present a well-resolved phylogeny of 14 Arborophila species inferred from ultra-conserved elements, exons, and mitochondrial genomes from both fresh and museum samples, which representing almost complete coverage of the genus. Our fossil-calibrated divergence time estimates and biogeographic modeling showed the ancestor of Arborophila arrived in Indochina during the early Miocene, but the initial divergence within Arborophila did not occur until ~10 Ma when global cooling intensified. Subsequent dispersal and diversification within Arborophila were driven by several tectonic and climatic events. In particular, we found evidence of rapid radiation in Indochinese Arborophila during the Pliocene global cooling and extensive dispersal and speciation of Sundaic Arborophila during the Pleistocene sea-level fluctuations. Taken together, these results suggest that the evolutionary history and biogeography of Arborophila were influenced by complex interactions among historical, geological and climatic events in Southeast Asia.

Standing genetic variation as the predominant source for adaptation of a songbird.

What kind of genetic variation contributes the most to adaptation is a fundamental question in evolutionary biology. By resequencing genomes of 80 individuals, we inferred the origin of genomic variants associated with a complex adaptive syndrome involving multiple quantitative traits, namely, adaptation between high and low altitudes, in the vinous-throated parrotbill (Sinosuthora webbiana) in Taiwan. By comparing these variants with those in the Asian mainland population, we revealed standing variation in 24 noncoding genomic regions to be the predominant genetic source of adaptation. Parrotbills at both high and low altitudes exhibited signatures of recent selection, suggesting that not only the front but also the trailing edges of postglacial expanding populations could be subjected to environmental stresses. This study verifies and quantifies the importance of standing variation in adaptation in a cohort of genes, illustrating that the evolutionary potential of a population depends significantly on its preexisting genetic diversity. These findings provide important context for understanding adaptation and conservation of species in the Anthropocene.

From the Himalayas to a continental Island: Integrative species delimitation in the Brownish-flanked Bush Warbler Horornis fortipes complex.

As species serve as basic units of study in many fields of biology, assessments of species limits are fundamental for such studies. Here, we used a multilocus dataset and different coalescent-based methods to analyze species delimitation and phylogenetic relationships in the Brownish-flanked Bush Warbler Horornis fortipes complex, which is widespread in the Sino-Himalayan region. We also examined the vocal and morphometric divergence within this complex. Our genetic results suggested that Horornis fortipes is composed of at least three independently evolving lineages, which diverged 1.1-1.8 million years ago. However, these lineages have hardly diverged in song or morphometrics and only very slightly in plumage. Our result indicate that there are three incipient species in Horonis fortipes complex diverged in central Himalayas and Hengduan Mountains, but not between the continent and Taiwan island.

The first set of universal nuclear protein-coding loci markers for avian phylogenetic and population genetic studies.

Multiple nuclear markers provide genetic polymorphism data for molecular systematics and population genetic studies. They are especially required for the coalescent-based analyses that can be used to accurately estimate species trees and infer population demographic histories. However, in avian evolutionary studies, these powerful coalescent-based methods are hindered by the lack of a sufficient number of markers. In this study, we designed PCR primers to amplify 136 nuclear protein-coding loci (NPCLs) by scanning the published Red Junglefowl (Gallus gallus) and Zebra Finch (Taeniopygia guttata) genomes. To test their utility, we amplified these loci in 41 bird species representing 23 Aves orders. The sixty-three best-performing NPCLs, based on high PCR success rates, were selected which had various mutation rates and were evenly distributed across 17 avian autosomal chromosomes and the Z chromosome. To test phylogenetic resolving power of these markers, we conducted a Neoavian phylogenies analysis using 63 concatenated NPCL markers derived from 48 whole genomes of birds. The resulting phylogenetic topology, to a large extent, is congruence with results resolved by previous whole genome data. To test the level of intraspecific polymorphism in these makers, we examined the genetic diversity in four populations of the Kentish Plover (Charadrius alexandrinus) at 17 of NPCL markers chosen at random. Our results showed that these NPCL markers exhibited a level of polymorphism comparable with mitochondrial loci. Therefore, this set of pan-avian nuclear protein-coding loci has great potential to facilitate studies in avian phylogenetics and population genetics.

The effects of food and parasitism on reproductive performance of a wild rodent.

Food and parasitism can have complex effects on small mammal reproduction. In this study, we tested the effects of sex, food, and parasitism on reproductive performance of the Taiwan field mouse (Apodemus semotus). In a field experiment, we increased food availability for a portion of the mice in the population by providing sorghum seeds to a set of food stations. We reduced parasite intensity of randomly chosen mice through ivermectin treatment. We determined the number and quality of offspring for the mice using paternity analysis. We quantified seed consumption with stable carbon isotope values of mouse plasma and parasite intensity with fecal egg counts of intestinal nematodes and cestodes (FEC). In a laboratory experiment, we reduced parasite intensity of randomly chosen mice through ivermectin treatment. We quantified their immune functions by total white blood cell count, percent granulocyte count, and percent lymphocyte count through hematological analyses. We measured the FEC and energy intake of the mice. From the field experiment, the number of offspring in A. semotus increased with increasing seed consumption. Due to the trade-off between number and quality of offspring, the offspring quality decreased with increasing seed consumption for the females. The ivermectin treatment did not affect offspring number or quality. However, the FEC was positively correlated with number of offspring. In the laboratory experiment, the percent lymphocyte/granulocyte count changed with parasite intensity at low energy intake, which was relaxed at high energy intake. This study demonstrated positive effects of food availability and neutral effects of parasitism on A. semotus reproduction. However, the benefits of food availability for the females need to take into account the offspring number-quality trade-off, and at high infection intensity, parasitism might negatively affect offspring quality for the males. We suggest that food availability could mediate the relationships between parasite intensity and immune responses.

Ice age unfrozen: severe effect of the last interglacial, not glacial, climate change on East Asian avifauna.

BACKGROUND: The glacial-interglacial cycles in the Pleistocene caused repeated range expansion and contraction of species in several regions in the world. However, it remains uncertain whether such climate oscillations had similar impact on East Asian biota, despite its widely recognized importance in global biodiversity. Here we use both molecular and ecological niche profiles on 11 East Asian avian species with various elevational ranges to reveal their response to the late Pleistocene climate changes. RESULTS: The ecological niche models (ENM) consistently showed that these avian species might substantially contract their ranges to the south during the Last Interglacial period (LIG) and expanded their northern range margins through the Last Glacial Maximum (LGM), leading to the LGM ranges observed for all 11 species. Consistently, coalescent simulations based on 25-30 nuclear genes retrieved signatures of significant population growth through the last glacial period across all species studied. Climate statistics suggested that high climatic variability during the LIG and a relatively mild climate at the LGM potentially explained the historical population dynamics of these birds. CONCLUSIONS: This is the first study based on multiple species and both lines of ecological niche profiles and genetic data to characterize the unique response of East Asian biota to late Pleistocene climate. The present study highlights regional differences in the evolutionary consequence of climate change during the last glacial cycle and implies that global warming might pose a great risk to species in this region given potentially higher climatic variation in the future analogous to that during the LIG.

Himalayan black bulbuls (Hypsipetes leucocephalus niggerimus) exhibit sexual dichromatism under ultraviolet light that is invisible to the human eye.

Sexual dichromatism is a key proxy for the intensity of sexual selection. Studies of dichromatism in birds may, however, have underestimated the intensity and complexity of sexual selection because they used museum specimens alone without taking colour-fading into account or only measured conspicuous visual traits in live animals. We investigated whether the Himalayan black bulbul (Hypsipetes leucocephalus nigerrimus), which is sexually monomorphic to the human eye, exhibits sexual dichromatism distinguishable by a spectrometer. We measured the reflectance (within both the human visual perceptive and the ultraviolet ranges) of two carotenoid-based parts and eight dull and melanin-based parts for each individual live bird or museum skin sampled. According to an avian model of colour discrimination thresholds, we found that males exhibited perceptibly redder beaks, brighter tarsi and darker plumage than did females. This suggests the existence of multiple cryptic sexually dichromatic traits within this species. Moreover, we also observed detectable colour fading in the museum skin specimens compared with the live birds, indicating that sexual dichromatism could be underestimated if analysed using skin specimens alone.

Incipient speciation with gene flow on a continental island: Species delimitation of the Hainan Hwamei (Leucodioptron canorum owstoni, Passeriformes, Aves).

Because of their isolation, continental islands (e.g., Madagascar) are often thought of as ideal systems to study allopatric speciation. However, many such islands have been connected intermittently to their neighboring continent during recent periods of glaciation, which may cause frequent contact between the diverging populations on the island and continent. As a result, the speciation processes on continental islands may not meet the prerequisites for strictly allopatric speciation. We used multiple lines of evidence to re-evaluate the taxonomic status of the Hainan Hwamei (Leucodioptron canorum owstoni), which is endemic to Hainan, the largest continental island in the South China Sea. Our analysis of mitochondrial DNA and twelve nuclear loci suggests that the Hainan Hwamei can be regarded as an independent species (L. owstoni); the morphological traits of the Hainan Hwamei also showed significant divergence from those of their mainland sister taxon, the Chinese Hwamei (L. canorum). We also inferred the divergence history of the Hainan and Chinese Hwamei to see whether their divergence was consistent with a strictly allopatric model. Our results suggest that the two Hwameis split only 0.2 million years ago with limited asymmetrical post-divergence gene flow. This implies that the Hainan Hwamei is an incipient species and that speciation occurred through ecologically divergent selection and/or assortative mating rather than a strictly allopatric process.

The Genetic Relatedness in Groups of Joint-Nesting Taiwan Yuhinas: Low Genetic Relatedness with Preferences for Male Kin.

The relative importance of direct and indirect fitness and, thus, the role of kinship in the evolution of social behavior is much debated. Studying the genetic relatedness of interacting individuals is crucial to improving our understanding of these issues. Here, we used a seven-year data set to study the genetic structure of the Taiwan yuhina (Yuhina brunneciceps), a joint-nesting passerine. Ten microsatellite loci were used to investigate the pair-wised relatedness among yuhina breeding group members. We found that the average genetic relatedness between same-sex group members was very low (0.069 for male dyads and 0.016 for female dyads). There was also a low ratio of closely-related kin (r>0.25) in the cooperative breeding groups of yuhinas (21.59% and 9.68% for male and female dyads, respectively). However, the relatedness of male dyads within breeding groups was significantly higher than female dyads. Our results suggest that yuhina cooperation is maintained primarily by direct fitness benefits to individuals; however, kin selection might play a role in partner choice for male yuhinas. Our study also highlights an important, but often neglected, question: Why do animals form non-kin groups, if kin are available? We use biological market theory to propose an explanation for group formation of unrelated Taiwan yuhinas.

Within-island speciation with an exceptional case of distinct separation between two sibling lizard species divided by a narrow stream.

Delimitation of genetic and geographic boundaries between species is a focus of evolutionary biology. In this study, we demonstrated fine-scale differentiation of Takydromus formosanus species complex comprising four insular endemics on Taiwan Island. Phylogeny and ancestral range reconstruction based on mitochondrial DNA sequences of 430 Takydromus lizards (405 lizards of this complex throughout their distribution range, and 25 lizards from 11 other species) indicated that the major branching process occurred within Taiwan, which represented a solid evidence of within-island speciation on this small island. We further demonstrated an exceptional case of a pair of sister species, T. viridipunctatus and T. luyeanus, that were separated by a narrow stream with a width of only 15m. This pattern might be one of the narrowest contact zones ever documented in terrestrial vertebrates. To evaluate the level of genetic introgression between these sister species, a fine-scale collection of another 382 lizards was conducted along a transect line across the stream. A total of 13 microsatellite markers and mtDNA genotyping was used to detect a low proportion of hybrids (5.7-9.9% from STRUCTURE, and 2.3% from DAPC). Our results indicated that the two clades are highly differentiated across this extremely short distance.

Climate niche differentiation between two passerines despite ongoing gene flow.

Niche evolution underpins the generation and maintenance of biological diversity, but niche conservatism, in which niches remain little changed over time in closely related taxa, and the role of ecology in niche evolution are continually debated. To test whether climate niches are conserved in two closely related passerines in East Asia - the vinous-throated (Paradoxornis webbianus) and ashy-throated (P. alphonsianus) parrotbills - we established their potential allopatric and sympatric regions using ecological niche models and compared differences in their climate niches using niche overlap indices in background tests and multivariate statistical analyses. We also used polymorphism data on 44 nuclear genes to infer their divergence demography. We found that these two parrotbills occupy different climate niches, in both their allopatric and potential sympatric regions. Because the potential sympatric region is the area predicted to be suitable for both parrotbills based on the ecological niche models, it can serve as a natural common garden. Therefore, their observed niche differences in this potential sympatry were not simply rendered by phenotypic plasticity and probably had a genetic basis. Our genetic analyses revealed that the two parrotbills are not evolutionarily independent for the most recent part of their divergence history. The two parrotbills diverged c. 856,000 years ago and have had substantial gene flow since a presumed secondary contact c. 290,000 years ago. This study provides an empirical case demonstrating that climate niches may not be homogenized in nascent species in spite of substantial, ongoing gene flow, which in turn suggests a role for ecology in promoting and maintaining diversification among incipient species.

Was the exposed continental shelf a long-distance colonization route in the ice age? The Southeast Asia origin of Hainan and Taiwan partridges.

Research on island biotas has greatly contributed to the development of modern evolutionary and biogeographic theories. Until now, most studies have suggested that continental islands received their biotas directly from the adjacent mainland. However, only a few studies have indicated that species on continental islands might originate from other distantly non-adjacent regions. Here, we used the hill partridges (genus Arborophila) that are widely distributed in the southwest and southeast China mainland, Indochina, Hainan and Taiwan islands to test whether species on continental islands might originate from distant regions rather than the adjacent mainland. Based on molecular phylogenies inferred from three mitochondrial fragments and three nuclear introns, together with ancestral area reconstruction, we found that the ancestors of the endemic Hainan and Taiwan partridges (A. ardens and A. crudigularis) likely originated from Indochina, rather than the nearby southeast China mainland. The divergence time estimates demonstrate that their ancestors likely colonized Hainan and Taiwan islands using the long exposed continental shelf between Indochina, Hainan and Taiwan islands during glacial periods, which had not been demonstrated before. Thus, integrating distribution data with phylogenetic information can shed new lights on the historical biogeography of continental islands and surrounding mainland regions.