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.

Kritika Garg

Department of Biology

Kritika Garg M

Emilie Cros

Suzanne Tomassi

Suzan Benedick

David Edwards P

Frank Rheindt E

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Ashoka University

Molecular Biology and Evolution

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.

Molecular Ecology

Quaternary land bridges have not been universal conduits of gene flow

Background: Quaternary climate fluctuations are an engine of biotic diversification. Global cooling cycles, such as the Last Glacial Maximum (LGM), are known to have fragmented the ranges of higher-latitude fauna and flora into smaller refugia, dramatically reducing species ranges. However, relatively less is known about the effects of cooling cycles on tropical biota. Results: We analyzed thousands of genome-wide DNA markers across an assemblage of three closely related understorey-inhabiting scrubwrens (Sericornis and Aethomyias; Aves) from montane forest along an elevational gradient on Mt. Wilhelm, the highest mountain of Papua New Guinea. Despite species-specific differences in elevational preference, we found limited differentiation within each scrubwren species, but detected a strong genomic signature of simultaneous population expansions at 27-29 ka, coinciding with the onset of the LGM. Conclusion: The remarkable synchronous timing of population expansions of all three species demonstrates the importance of global cooling cycles in expanding highland habitat. Global cooling cycles have likely had strongly different impacts on tropical montane areas versus boreal and temperate latitudes, leading to population expansions in the former and serious fragmentation in the latter.

BMC Evolutionary Biology

Last Glacial Maximum led to community-wide population expansion in a montane songbird radiation in highland Papua New Guinea

Anthropogenic activities have propelled the Earth into a crisis characterized by unprecedented levels of environmental degradation and habitat loss, generating changes in global climatic regimes and initiating the planet's Sixth Extinction Catastrophe [1]. Loss of population genetic diversity is known to be a harbinger of local and global extinction events [2]. However, there is a lack of direct empirical evidence of historic losses of genetic diversity through periods of anthropogenically linked environmental degradation. We present genomic DNA information from a population of Sunda fruit bats (Cynopterus brachyotis) from Singapore, an exceptionally well-studied tropical rainforest island that has undergone substantial environmental degradation and fragmentation through the Anthropocene of the 1930–1950s [3]. As an effective pollinator and seed disperser, C. brachyotis represents an important keystone species in Singapore's ecosystem [4]. Here we show that comparison of historic DNA from individuals collected in 1931 with modern specimens reveals a nearly 30-fold reduction in effective population size and corresponding levels of decline in genetic diversity estimates. Coalescent population models indicate that Singapore's C. brachyotis bats underwent a continuous decline in genetic diversity followed by a stark bottleneck in approximately the 1940s, consistent with the estimated onset of the Anthropocene [5]. C. brachyotis continues to be considered common across Singapore [4], yet our results reveal large-scale impacts of the Anthropocene on biotic communities, even in those species thought to be tolerant to the effects of environmental degradation. Humans have brought about a global environmental crisis. Chattopadhyay et al. compared genomic profiles of historic samples, collected in 1931, with modern samples of a widespread fruit bat in Singapore. They detect a strong Anthropocene crash in genetic diversity, suggesting that modern threats extend even to seemingly unaffected species.

Current Biology

Historic DNA reveals Anthropocene threat to a tropical urban fruit bat

Cyclical periods of global cooling have been important drivers of biotic differentiation throughout the Quaternary. Ice age-induced sea level fluctuations can lead to changing patterns of land connections, both facilitating and disrupting gene flow. In this study, we test if species with differing life histories are differentially affected by Quaternary land connections. We used genome-wide SNPs in combination with mitochondrial gene sequences to analyse levels of divergence and gene flow between two songbird complexes across two Wallacean islands that have been repeatedly connected during glaciations. Although the two bird complexes are similar in ecological attributes, the forest and edge-inhabiting golden whistler Pachycephala pectoralis is comparatively flexible in its diet and niche requirements as compared to the henna-tailed jungle-flycatcher Cyornis colonus, which is largely restricted to the forest interior. Using population-genomic and coalescent approaches, we estimated levels of gene flow, population differentiation and divergence time between the two island populations. We observed higher levels of differentiation, an approximately two to four times deeper divergence time and near-zero levels of gene flow between the two island populations of the more forest-dependent henna-tailed jungle-flycatcher as compared to the more generalist golden whistler. Our results suggest that Quaternary land bridges act as semipermeable agents of gene flow in Wallacea, allowing only certain taxa to connect between islands while others remain isolated. Quaternary land bridges do not accommodate all terrestrial species equally, differing in suitability according to life history and species biology. More generalist species are likely to use Quaternary land connections as a conduit for gene flow between islands whereas island populations of more specialist species may continue to be reproductively isolated even during periods of Quaternary land bridges.

Molecular Phylogenetics and Evolution

Pleistocene land bridges act as semipermeable agents of avian gene flow in Wallacea

The role of Pleistocene Ice Age in tropical diversification is poorly understood, especially in archipelagos, in which glaciation-induced sea level fluctuations may lead to complicated changes in land distribution. To assess how Pleistocene land bridges may have facilitated gene flow in tropical archipelagos, we investigated patterns of diversification in the rarely-collected rusty-bellied fantail Rhipidura teysmanni (Passeriformes: Rhipiduridae) complex from Wallacea using a combination of bioacoustic traits and whole-genome sequencing methods (dd-RADSeq). We report a biogeographic leapfrog pattern in the vocalizations of these birds and uncover deep genomic divergence among island populations despite the presence of intermittent land connections between some. We demonstrate how rare instances of genetic introgression have affected the evolution of this species complex and document the presence of double introgressive mitochondrial sweeps, highlighting the dangers of using only mitochondrial DNA in evolutionary research. By applying different tree inference approaches, we demonstrate how concatenation methods can give inaccurate results when investigating divergence in closely-related taxa. Our study highlights high levels of cryptic avian diversity in poorly-explored Wallacea, elucidates complex patterns of Pleistocene climate-mediated diversification in an elusive montane songbird and suggests that Pleistocene land bridges may have accounted for limited connectivity among montane Wallacean biota.

The effects of Pleistocene climate change on biotic differentiation in a montane songbird clade from Wallacea

Island Biogeography Revisited: Museomics Reveals Affinities of Shelf Island Birds Determined by Bathymetry and Paleo-Rivers, Not by Distance to Mainland

Journal	Molecular Biology and Evolution
ISSN	0737-4038