Quaternary land bridges have not been universal conduits of gene flow

Abstract

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 genomewide 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.

Phylogenomics of white-eyes, a ‘great speciator’, reveals Indonesian archipelago as the center of lineage diversity

“…Sundaland, that has facilitated the evolution of much of Southeast Asia's equatorial rainforest fauna (Sarr et al 2019). The east of Sundaland (i.e., Borneo) has constituted a particularly stable part of this subcontinent, remaining above water for the While Borneo's exceptional biodiversity has been appreciated as early as during Alfred R. Wallace's times (Wallace 1962), most of this diversity has traditionally been interpreted as being of a Sundaic element largely shared with Sumatra and peninsular Malaysia, and is only slowly being recognized as having attained species-level depths of differentiation (Cros et al 2020). On the other hand, Borneo is known for hosting a number of deep phylogenetic isolates, such as the enigmatic Bristlehead Pityriasis gymnocephala (Oliveros et al 2019).…”

Gene Flow in Volant Vertebrates: Species Biology, Ecology and Climate Change

“…For example, many bulbuls which can move across large distances in search for fruiting trees were able to utilize these Pleistocene land bridges but the same was not observed for insectivorous understory babblers which are comparatively sedentary in nature (Figs. 1 b and 2 ) 14 . Similarly, in the satellite islands of Sulawesi, Peleng and Taliabu, forest-dependent bird species rarely utilized these land bridges to move between isolated island populations leading to genetic diversification and speciation, whereas edge tolerant species were able to move across the land bridges thereby retaining genetic connectivity and resisting genetic differentiation 23 .…”

“…Further, this same panel of genome-wide markers could also identify a cryptic species of fruit bat from Eastern India and discovered a hybrid zone between two species-level lineages with evidence of gene flow and introgression 11 . NGS data has also helped in identifying various barriers to gene flow like physical features of the Earth (e.g rivers and oceans) as well as species attributes (e.g habitat preferences) 14 , 23 , 41 , 56 . For instance, unexpected fine-scale populations structure was revealed in forest-dependent birds within a small forested region of the island nation of Singapore when thousands of genomic markers were used 15 .…”

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

“…As Quaternary glacial Island Biogeography Revisited . doi:10.1093/molbev/msab340 MBE cycles leave a track record within the genome, patterns of genomic diversity can be used to reconstruct evolutionary history (Lim et al 2017;Ng et al 2017;Papadopoulou and Knowles 2017;Garg et al 2018;Cros, Chattopadhyay, et al 2020;Rheindt et al 2020).…”

“…However, island size and distance to mainland may not provide a complete picture ( Borregaard et al 2016 ; Fernández‐Palacios et al 2016 ; Weigelt et al 2016 ; Whittaker et al 2017 ), with the role of Quaternary glaciations and concomitant sea-level fluctuations also pertinent to island biogeography ( Fernández‐Palacios et al 2016 ; Weigelt et al 2016 ). Cyclical periods of global cooling and warming over the past approximately 2.6 My have not only been an engine of diversification at higher latitudes and altitudes, but also affected gene flow and speciation patterns in shelf-island regions (i.e., islands on continental shelves), especially in Southeast Asia ( Heaney 1986 ; Hewitt 2000 , 2004 ; Moyle et al 2009 ; Lim and Sheldon 2011 ; Brown et al 2013 ; Chattopadhyay et al 2017 ; Ng et al 2017 ; Garg et al 2018 , 2020 ; Cros, Chattopadhyay, et al 2020 ; Rheindt et al 2020 ). Many present-day shelf-islands have been connected by land bridges during cooler Quaternary periods with lower sea levels, allowing for possible dispersal of terrestrial organisms and gene flow ( Lim and Sheldon 2011 ; Lim et al 2011 , 2017 ; Leonard et al 2015 ; Ng et al 2017 ; Garg et al 2018 ; Cros, Chattopadhyay, et al 2020 ).…”