Evolutionary dynamics of bird populations in Southeast Asia

A confluence of factors determines the biological diversity we observe today. Here, I conducted three investigations of the historic, geographic and ecological factors that shaped the morphological and genetic diversity of rainforest birds in Southeast Asia. (1) In the Oriental Dwarf Kingfisher (Ceyx erithaca) complex, the birds are highly polymorphic in plumage. Quantitative analysis of this variation indicated that a large proportion of birds in Sumatra, the Malay Peninsula and Borneo have plumages intermediate between the northerly black form from mainland Asia and the southerly rufous form from Java. Phylogenetic analyses indicated that birds from continental Southeast Asia (north of the Malay Peninsula) were well differentiated from those from insular Southeast Asia. This genetic distinction correlates well with a fixed plumage difference (mantle coloration). Coalescent analyses showed that the plumage polymorphism was caused by past genetic introgression between the two parental forms. (2) I sampled 16 lowland rainforest bird species primarily from the Malay Peninsula and Borneo to test the long-standing hypothesis that animals on different Sundaic landmasses intermixed extensively when low sea-levels during the Last Glacial Maximum (LGM) exposed land-bridges. This hypothesis was rejected in all but five species through coalescent simulations. Environmental niche modeling showed that the presence of unsuitable habitats between western and eastern Sundaland during the LGM coincided with deeper inter-population genetic divergences. The distinctiveness of the northeastern Borneo populations of some species may be underlain by a combination of factors that included riverine barriers, LGM expansion of montane forests and regional physiography. (3) I further investigated the population divergence and demographic histories of three bird species that possessed disparate ecological characteristics. Multilocus analyses revealed changes in effective population sizes that were driven by long-term changes in the environment, instead of high-frequency glacial cycles. Populations from Borneo exhibited stronger demographic growth than those from mainland Southeast Asia, suggesting regional differences in environmental changes or directional colonization. The species with the widest habitat breadth also showed the greatest amount of inter-landmass gene flow. This adds to the growing body of empirical work indicating an association between a species’ ecological characteristics and its population connectivity over evolutionary time-scales

Do insectivorous bird communities decline on land-bridge forest islands in Peninsular Malaysia?

To assess the impact of habitat fragmentation on tropical avian communities, we sampled lowland forest birds on six land-bridge islands and two mainland forest sites in Lake Kenyir, Peninsular Malaysia using timed point counts, hypothesizing that insectivorous birds are the worst affected guild. We used an information-theoretic approach to evaluate the effects of area, isolation, primary dietary guild (omnivore, frugivore and insectivore) and their interactions in predicting species richness, abundance and diversity. Our analysis showed that a model that considered the effects of area, dietary guild and their interaction best explained observed patterns of species richness. But a model considering both area and dietary guild best explained the variation in abundance. Notably, insectivorous birds were singled out as the dietary guild most sensitive to fragmentation, followed by frugivorous and omnivorous birds and hence provide support for our hypothesis. Assemblages of insectivorous birds were clearly depauperate on anthropogenic forest islands in Lake Kenyir and are consistent with forest fragmentation studies in the Neotropics. Given their specialized foraging ecology and diversity, conservation of intact communities of insectivorous bird guilds in Malaysia will be critical for maintaining predator-prey interactions in lowland tropical forest

Divergence history of the Rufous-tailed Tailorbird (Orthotomus sericeus) of Sundaland: Implications for the biogeography of Palawan and the taxonomy of island species in general

The Rufous-tailed Tailorbird (Orthotomus sericeus)—a Sunda endemic—is divided into 3 morphologically based subspecies: one in western Sundaland (Malay Peninsula, Sumatra, and associated islands), one from the Natuna Islands in the South China Sea, and one on Borneo, Palawan, and smaller islands of the Sunda continental shelf east of Borneo. Previous study, however, suggested that these subspecies do not conform to molecular genetic subdivisions of the species. We reexamined the morphology and performed molecular phylogeographic and multi-locus coalescent analysis of two subspecies of Rufous-tailed Tailorbird comprising populations on the Malay Peninsula, Sumatra, Borneo, and Palawan. We found (1) little morphological difference among the two subspecies, (2) no substantial genetic differences between the Borneo and western Sunda populations, but (3) marked genetic divergence between the Palawan and other populations. We conclude that the Bornean and western Sunda populations interbred extensively during Quaternary glacio-eustatic land connections, whereas the Bornean and Palawan populations did not. Unlike the other Greater Sunda Islands, Palawan has not been attached by a land bridge to the rest of Sundaland for at least one million years, and its relative isolation has prevented extensive intermixing between Palawan's and other Sunda populations. Thus, the Palawan population appears to be on its own evolutionary trajectory. The ability to demonstrate extensive interbreeding among some Sunda island populations, but not others, illustrates the practicality of testing Gill's (2014) “null hypothesis” that morphologically distinct populations on different islands are different species unless a compelling argument can be made to the contrary. In this case, Rufous-tailed Tailorbird morphology provided little or misleading evidence of the extent of interbreeding, whereas modern genetic analysis provided a clear view

Opening the door to greater phylogeographic inference in Southeast Asia: Comparative genomic study of five codistributed rainforest bird species using target capture and historical DNA

Indochina and Sundaland are biologically diverse, interconnected regions of Southeast Asia with complex geographic histories. Few studies have examined phylogeography of bird species that span the two regions because of inadequate population sampling. To determine how geographic barriers/events and disparate dispersal potential have influenced the population structure, gene flow, and demographics of species that occupy the entire area, we studied five largely codistributed rainforest bird species: Arachnothera longirostra, Irena puella, Brachypodius atriceps, Niltava grandis, and Stachyris nigriceps. We accomplished relatively thorough sampling and data collection by sequencing ultraconserved elements (UCEs) using DNA extracted from modern and older (historical) specimens. We obtained a genome-wide set of 753–4,501 variable loci and 3,919–18,472 single nucleotide polymorphisms. The formation of major within-species lineages occurred within a similar span of time (0.5–1.5 mya). Major patterns in population genetic structure are largely consistent with the dispersal potential and habitat requirements of the study species. A population break across the Isthmus of Kra was shared only by the two hill/submontane insectivores (N. grandis and S. nigriceps). Across Sundaland, there is little structure in B. atriceps, which is a eurytopic and partially frugivorous species that often utilizes forest edges. Two other eurytopic species, A. longirostra and I. puella, possess highly divergent populations in peripheral Sunda Islands (Java and/or Palawan) and India. These species probably possess intermediate dispersal abilities that allowed them to colonize new areas, and then remained largely isolated subsequently. We also observed an east–west break in Indochina that was shared by B. atriceps and S. nigriceps, species with very different habitat requirements and dispersal potential. By analyzing high-throughput DNA data, our study provides an unprecedented comparative perspective on the process of avian population divergence across Southeast Asia, a process that is determined by geography, species characteristics, and the stochastic nature of dispersal and vicariance events

Diversification of an Endemic Southeast Asian Genus: Phylogenetic Relationships of the Spiderhunters (Nectariniidae: Arachnothera)

This is the publisher's version, also available at http://www.bioone.org/doi/abs/10.1525/auk.2011.11019The phylogeny of spiderhunters (Nectariniidae: Arachnothera) was reconstructed by comparing mitochondrial and nuclear DNA sequences of all currently recognized species and with broad geographic sampling of two particularly variable species complexes, the Little Spiderhunter (Arachnothera longirostra) and the streaky spiderhunters (A. modesta and A. affinis). It appears to be a relatively old group, whose diversification was not caused by recent sea-level changes. However, the modern, highly sympatric distribution of the large species in the Sunda lowlands was probably a result of dispersal via recent land bridges. Within the highly variable A. longirostra group, there are substantially diverged taxa in the Philippines that should be considered different species. Within the A. affinis—modesta complex, there are three distinct species and a closely related fourth, which describe a clear allopatric distribution: A. affinis in Java, A. modesta in the rest of the Sunda lowlands (except Sabah), A. magna in the Malayan highlands and mainland Southeast Asia, and A. everetti in the Bornean highlands and Sabah. Depending on whether mitochondrial or nuclear genes were compared, monophyly of the genus was disrupted by a single outgroup sunbird (Hypogramma hypogrammicum) or by all outgroup sunbirds included in the study. The discrepancy between nuclear and mitochondrial results is probably a case of deep coalescence and will require additional markers for resolution

Phylogeography of three endemic birds of Maratua Island, a potential archive of Bornean biogeography

Maratua is an oceanic island ca. 50 km off the east coast of Borneo and home to several endemic taxa of birds and mammals. To determine the phylogeographic relationships of three of Maratua’s most distinctive avian endemics—a shama Copsychus stricklandii barbouri, a bulbul Pycnonotus atriceps hodiernus, and a monarch Hypothymis azurea aeria—we compared their mitochondrial ND2 sequences with those of putatively closely related Southeast Asian populations. We found that Maratua’s shama and bulbul are substantially differentiated from populations on Borneo and elsewhere in Southeast Asia, whereas Maratua’s monarch is not. The shama’s phylogeographic tree indicates a sister relationship between C. s. barbouri and C. s. stricklandii of northeast Borneo, both of which have white crowns (ND2 distance ~2%). These two taxa, in turn, are >3% divergent from C. malabaricus populations, which have black crowns. The relative morphological and genetic similarity of C. s. barbouri and C. s. stricklandii suggests that C. stricklandii had a broader distribution in eastern Borneo in the mid-Pleistocene and that C. s. stricklandii has more recently moved or been restricted to its current position in northeast Borneo. Maratua has thus acted as a biogeographic “museum”, preserving evidence of C. stricklandii’s former distribution. The Maratuan P. atriceps is about equidistant genetically from other P. atriceps populations. It is distinguished by an overall grey body plumage, whereas P. atriceps elsewhere is mostly yellow (with grey morphs appearing only rarely). The universality of grey birds on Maratua is likely the result of a founder effect. The Maratuan monarch’s genetic similarity to the mainland Bornean population suggests either that it is a recent invader or that substantial gene flow occurs between Borneo and Maratua in this species. The genetic and morphological distinctiveness of the shama and bulbul are adequate to consider them both as full species

Patterns of avian diversification in Borneo: The case of the endemic Mountain Black-eye (Chlorocharis emiliae)

The Mountain Black-eye (Chlorocharis emiliae) is an endemic white-eye (Zosteropidae) of Borneo with a unique “sky island” distribution. We compared mitochondrial ND2, ND3, Cytb, and control region DNA sequences (2,194 nucleotides) to study the phylogeographic relationships of five populations of this species that span its range: Mounts Kinabalu, Trus Madi, Murud, Mulu, and Pueh. These comparisons showed that black-eyes are divided into two main clades that correspond generally to subspecific morphological groups: one in Sabah, Malaysia (Kinabalu and Trus Madi), and one in Sarawak, Malaysia (Murud, Mulu, and Pueh). The genetic and morphologic subdivision of black-eyes disputes the expected merging of populations during the Last Glacial Maximum (LGM), when montane forest presumably expanded and provided the opportunity for currently isolated populations to intermingle. Instead the genetic aging of black-eye populations indicates they diversified long before the LGM, and either did not expand sufficiently in range during the LGM to reach one another, or were reproductively isolated by the time of the LGM and thus prevented from interbreeding. Moreover, the subdivision between black-eyes in Sabah and Sarawak means that this species (and probably several other montane species) has a phylogeographic structure remarkably similar to Borneo's lowland bird populations, which are presumed to have evolved under different paleo-geographic conditions. The similar phylogeographic pattern found in both montane and lowland species requires that we rethink the causes of bird population diversification on the island of Borneo

Genomics-based re-examination of the taxonomy and phylogeny of human and simian Mastadenoviruses: an evolving whole genomes approach, revealing putative zoonosis, anthroponosis, and amphizoonosis

With the advent of high-resolution and cost-effective genomics and bioinformatics tools and methods contributing to a large database of both human (HAdV) and simian (SAdV) adenoviruses, a genomics-based re-evaluation of their taxonomy is warranted. Interest in these particular adenoviruses is growing in part due to the applications of both in gene transfer protocols, including gene therapy and vaccines, as well in oncolytic protocols. In particular, the re-evaluation of SAdVs as appropriate vectors in humans is important as zoonosis precludes the assumption that human immune system may be na€ıve to these vectors. Additionally, as impor- tant pathogens, adenoviruses are a model organism system for understanding viral pathogen emergence through zoonosis and anthroponosis, particularly among the primate species, along with recombination, host adaptation, and selection, as evidenced by one long-standing human respiratory pathogen HAdV-4 and a recent re-evaluation of another, HAdV-76. The latter reflects the insights on amphizoonosis, defined as infections in both directions among host species including “other than human”, that are pos- sible with the growing database of nonhuman adenovirus genomes. HAdV-76 is a recombinant that has been isolated from human, chimpanzee, and bonobo hosts. On-going and potential impacts of adenoviruses on public health and translational medicine drive this evaluation of 174 whole genome sequences from HAdVs and SAdVs archived in GenBank. The conclusion is that rather than separate HAdV and SAdV phylogenetic lineages, a single, intertwined tree is observed with all HAdVs and SAdVs forming mixed clades. Therefore, a single designation of “primate adenovirus” (PrAdV) superseding either HAdV and SAdV is proposed, or alter- natively, keeping HAdV for human adenovirus but expanding the SAdV nomenclature officially to include host species identifica- tion as in ChAdV for chimpanzee adenovirus, GoAdV for gorilla adenovirus, BoAdV for bonobo adenovirus, and ad libitum

Molecular phylogeny and insular biogeography of the lowland tailorbirds of Southeast Asia (Cisticolidae: Orthotomus)

The lowland tailorbirds of Southeast Asia (Orthotomus) offer an excellent opportunity for comparative biogeography because of their diversity in the Greater Sunda and Philippine islands. We reconstructed the phylogeny of all species in the genus using maximum likelihood, Bayesian, and coalescent methods on DNA sequences of three gene segments: an autosomal intron (TGF), a Z-linked intron (MUSK), and a mitochondrial coding gene (ND2). Although resolution is low in parts of the phylogeny, several well defined clades emerge. When considered in light of distribution, these clades indicate that the Greater Sunda and Philippine islands were occupied early in Orthotomus history by the ancestors of O. sericeus in the Greater Sundas and O. frontalis in the Philippines. Subsequently, tailorbirds diversified further in each island group: O. atrogularis, O. ruficeps, and O. sepium arose in the Greater Sundas, and O. castaneiceps castaneiceps, O. c. chloronotus, O. derbianus, O. samarensis, O. nigriceps, and O. cinereiceps in the Philippines. Among the continental taxa (including Sundaic birds), the older lineages (O. sutorius and O. sericeus) are habitat generalists and the recently evolved taxa are more specialized. In the Philippines, several taxa once considered conspecific with O. atrogularis turn out to be highly divergent species (>9% in ND2). Indeed, all Philippine allospecies are well diverged from one another. This finding supports the recent assertion of higher-than-appreciated bird endemicity in the Philippines