White-bellied swiftlets of the Collocalia esculenta complex constitute a radiation of colony-breeding swifts distributed throughout the tropical Indo-Pacific region. Resolution of their taxonomy is challenging due to their morphological uniformity. To analyze the evolutionary history of this complex, we combine new biometric measurements and results from plumage assessment of museum specimens with novel as well as previously published molecular data. Together, this body of information constitutes the largest systematic dataset for white-bellied swiftlets yet compiled, drawn from 809 individuals belonging to 32 taxa for which new molecular, biometric, and/or plumage data are presented. We propose changing the classification of white-bellied swiftlets, for which two species are currently recognized, to elevate eight regional forms to species level, and we also describe two new subspecies. The ten taxa we recommend recognizing at the species level are: Collocalia linchi (Java to Lombok, Sumatran hills), C. dodgei (montane Borneo), C. natalis (Christmas Island), C. affinis (Greater Sundas, including the Thai-Malay Peninsula and Andaman-Nicobar Islands), C. marginata (Philippines), C. isonota (Philippines), C. sumbawae (west Lesser Sundas), C. neglecta (east Lesser Sundas), C. esculenta (Sulawesi, Moluccas, New Guinea, Bismarck Archipelago, Solomon Islands), and C. uropygialis (Vanuatu, New Caledonia). Future molecular and morphological work is needed to resolve questions of speciation and population affinities in the Philippines, Christmas Island, Wallacea and central Melanesia, and to shed light on historic diversification and patterns of gene flow in the complex.
The southern river terrapin, Batagur affinis is one of the world's 25 most endangered freshwater turtle species. The major portion of the global population is currently found in peninsular Malaysia, with the only remnant Indochinese population in southern Cambodia. For more than a decade, wild nests in this remnant Cambodian population have been fenced and hatchlings reared in captivity. Here we amplified 10 microsatellite markers from all 136 captive individuals, obtained 2,658 presumably unlinked and neutral single nucleotide polymorphisms from 72 samples with ddRAD-seq, and amplified 784 bp of mtDNA from 50 samples. Our results reveal that the last Indochinese population comprised only four kinship groups as of 2012, with all offspring sired from <10 individuals in the wild. We demonstrate an obvious decrease in genetic contributions of breeders in the wild from 2006-2012 and identify high-value breeders instrumental for ex-situ management of the contemporary genetic stock of the species.
Island biogeography is one of the most powerful subdisciplines of ecology: its mathematical predictions that island size and distance to mainland determine diversity have withstood the test of time. A key question is whether these predictions follow at a population-genomic level. Using rigorous ancient-DNA protocols, we retrieved approximately 1,000 genomic markers from approximately 100 historic specimens of two Southeast Asian songbird complexes from across the Sunda Shelf archipelago collected 1893-1957. We show that the genetic affinities of populations on small shelf islands defy the predictions of geographic distance and appear governed by Earth-historic factors including the position of terrestrial barriers (paleo-rivers) and persistence of corridors (Quaternary land bridges). Our analyses suggest that classic island-biogeographic predictors may not hold well for population-genomic dynamics on the thousands of shelf islands across the globe, which are exposed to dynamic changes in land distribution during Quaternary climate change.
Wildlife crossings are implemented in many countries to facilitate the dispersal of animals among habitats fragmented by roads. However, the efficacy of different types of habitat corridors remains poorly understood. We used a comprehensive sampling regime in two lowland dipterocarp forest areas in peninsular Malaysia to sample pairs of small mammal individuals in three treatment types: (1) viaduct sites, at which sampling locations were separated by a highway but connected by a vegetated viaduct; (2) non-viaduct sites, at which sampling locations were separated by a highway and not connected by a viaduct; and (3) control sites, at which there was no highway fragmenting the forest. For four small mammal species, the common tree shrew Tupaia glis, Rajah's spiny rat Maxomys rajah, Whitehead's spiny rat Maxomys whiteheadi and dark-tailed tree rat Niviventer cremoriventer, we used genome-wide markers to assess genetic diversity, gene flow and genetic structure. The differences in genetic distance across sampling settings among the four species indicate that they respond differently to the presence of highways and viaducts. Viaducts connecting forests separated by highways appear to maintain higher population connectivity than forest fragments without viaducts, at least in M. whiteheadi, but apparently not in the other species.
Quaternary climate oscillations are a well-known driver of animal diversification, but their effects are most well studied in areas where glaciations lead to habitat fragmentation. In large areas of the planet, however, glaciations have had the opposite effect, but here their impacts are much less well understood. This is especially true in Southeast Asia, where cyclical changes in land distribution have generated enormous land expansions during glacial periods. In this study, we selected a panel of five songbird species complexes covering a range of ecological specificities to investigate the effects Quaternary land bridges have had on the connectivity of Southeast Asian forest biota. Specifically, we combined morphological and bioacoustic analysis with an arsenal of population genomic and modelling approaches applied to thousands of genome-wide DNA markers across a total of more than 100 individuals. Our analyses show that species dependent on forest understorey exhibit deep differentiation between Borneo and western Sundaland, with no evidence of gene flow during the land bridges accompanying the last 1-2 ice ages. In contrast, dispersive canopy species and habitat generalists have experienced more recent gene flow. Our results argue that there remains much cryptic species-level diversity to be discovered in Southeast Asia even in well-known animal groups such as birds, especially in nondispersive forest understorey inhabitants. We also demonstrate that Quaternary land bridges have not been equally suitable conduits of gene flow for all species complexes and that life history is a major factor in predicting relative population divergence time across Quaternary climate fluctuations.
The red junglefowl Gallus gallus is the ancestor of the domestic chicken and arguably the most important bird species on Earth. Continual gene flow between domestic and wild populations has compromised its gene pool, especially since the last century when human encroachment and habitat loss would have led to increased contact opportunities. We present the first combined genomic and morphological admixture assessment of a native population of red junglefowl, sampled from recolonized parts of its former range in Singapore, partly using whole genomes resequenced from dozens of individuals. Crucially, this population was genomically anchored to museum samples from adjacent Peninsular Malaysia collected ~110-150 years ago to infer the magnitude of modern domestic introgression across individuals. We detected a strong feral-wild genomic continuum with varying levels of domestic introgression in different subpopulations across Singapore. Using a trait scoring scheme, we determined morphological thresholds that can be used by conservation managers to successfully identify individuals with low levels of domestic introgression, and selected traits that were particularly useful for predicting domesticity in genomic profiles. Our study underscores the utility of combined genomic and morphological approaches in population management and suggests a way forward to safeguard the allelic integrity of wild red junglefowl in perpetuity.
Impending anthropogenic climate change will severely impact coastal organisms at unprecedented speed. Knowledge on organisms' evolutionary responses to past sea-level fluctuations and estimation of their evolutionary potential is therefore indispensable in efforts to mitigate the effects of future climate change. We sampled tens of thousands of genomic markers of ~300 individuals in two of the four extant horseshoe crab species across the complex archipelagic Singapore Straits. Carcinoscorpius rotundicauda Latreille, a less mobile mangrove species, has finer population structure and lower genetic diversity compared with the dispersive deep-sea Tachypleus gigas Müller. Even though the source populations of both species during the last glacial maximum exhibited comparable effective population sizes, the less dispersive C. rotundicauda seems to lose genetic diversity much more quickly because of population fragmentation. Contra previous studies' results, we predict that the more commonly sighted C. rotundicauda faces a more uncertain conservation plight, with a continuing loss in evolutionary potential and higher vulnerability to future climate change. Our study provides important genomic baseline data for the redirection of conservation measures in the face of climate change and can be used as a blueprint for assessment and mitigation of the adverse effects of impending sea-level rise in other systems.
Habitat fragmentation is a major extinction driver. Despite dramatically increasing fragmentation across the globe, its specific impacts on population connectivity across species with differing life histories remain difficult to characterize, let alone quantify. Here, we investigate patterns of population connectivity in six songbird species from Singapore, a highly fragmented tropical rainforest island. Using massive panels of genome-wide single nucleotide polymorphisms across dozens of samples per species, we examined population genetic diversity, inbreeding, gene flow and connectivity among species along a spectrum of ecological specificities. We found a higher resilience to habitat fragmentation in edge-tolerant and forest-canopy species as compared to forest-dependent understorey insectivores. The latter exhibited levels of genetic diversity up to three times lower in Singapore than in populations from contiguous forest elsewhere. Using dense genomic and geographic sampling, we identified individual barriers such as reservoirs that effectively minimize gene flow in sensitive understorey birds, revealing that terrestrial forest species may exhibit levels of sensitivity to fragmentation far greater than previously expected. This study provides a blueprint for conservation genomics at small scales with a view to identifying preferred locations for habitat corridors, flagging candidate populations for restocking with translocated individuals and improving the design of future reserves.
There is an urgent need for reliable data on the impacts of deforestation on tropical biodiversity. The city-state of Singapore has one of the most detailed biodiversity records in the tropics, dating back to the turn of the 19th century. In 1819, Singapore was almost entirely covered in primary forest, but this has since been largely cleared. We compiled more than 200 y of records for 10 major taxonomic groups in Singapore (>50,000 individual records; >3,000 species), and we estimated extinction rates using recently developed and novel statistical models that account for "dark extinctions," i.e., extinctions of undiscovered species. The estimated overall extinction rate was 37% (95% CI [31 to 42%]). Extrapolating our Singapore observations to a future business-as-usual deforestation scenario for Southeast Asia suggests that 18% (95% CI [16 to 22%]) of species will be lost regionally by 2100. Our extinction estimates for Singapore and Southeast Asia are a factor of two lower than previous estimates that also attempted to account for dark extinctions. However, we caution that particular groups such as large mammals, forest-dependent birds, orchids, and butterflies are disproportionately vulnerable.