Ancient divergence time estimates inEutropis rugiferasupport the existence of Pleistocene barriers on the exposed Sunda Shelf

Abstract

Episodic sea level changes that repeatedly exposed and inundated the Sunda Shelf characterize the Pleistocene. Available evidence points to a more xeric central Sunda Shelf during periods of low sea levels, and despite the broad land connections that persisted during this time, some organisms are assumed to have faced barriers to dispersal between land-masses on the Sunda Shelf. Eutropis rugifera is a secretive, forest adapted scincid lizard that ranges across the Sunda Shelf. In this study, we sequenced one mitochondrial (ND2) and four nuclear (BRCA1, BRCA2, RAG1, and MC1R) markers and generated a time-calibrated phylogeny in BEAST to test whether divergence times between Sundaic populations of E. rugifera occurred during Pleistocene sea-level changes, or if they predate the Pleistocene. We find that E. rugifera shows pre-Pleistocene divergences between populations on different Sundaic land-masses. The earliest divergence within E. rugifera separates the Philippine samples from the Sundaic samples approximately 16 Ma; the Philippine populations thus cannot be considered conspecific with Sundaic congeners. Sundaic populations diverged approximately 6 Ma, and populations within Borneo from Sabah and Sarawak separated approximately 4.5 Ma in the early Pliocene, followed by further cladogenesis in Sarawak through the Pleistocene. Divergence of peninsular Malaysian populations from the Mentawai Archipelago occurred approximately 5 Ma. Separation among island populations from the Mentawai Archipelago likely dates to the Pliocene/Pleistocene boundary approximately 3.5 Ma, and our samples from peninsular Malaysia appear to coalesce in the middle Pleistocene, about 1 Ma. Coupled with the monophyly of these populations, these divergence times suggest that despite consistent land-connections between these regions throughout the Pleistocene E. rugifera still faced barriers to dispersal, which may be a result of environmental shifts that accompanied the sea-level changes.

Ancient Divergence Driven by Geographic Isolation and Ecological Adaptation in Forest Dependent Sundaland Tree Squirrels

“…This does not support the Pleistocene speciation-pump hypothesis as the main driver behind the high levels of diversity found in Sundaland (Brown et al, 2013;Husson et al, 2019). The ancient patterns of divergence that we found in Sunda squirrels are consistent with those found in other small vertebrates and invertebrates (Klaus et al, 2013;Grismer et al, 2017;Karin et al, 2017;Manawatthana et al, 2017). This is particularly interesting in light of recent geological work suggesting that the Sunda shelf was continuously exposed until 400 ka (Husson et al, 2019).…”

“…The intermediate phenotype of the Siberut population, the closest Mentawai island to the Batu archipelago, which externally resembles Robinson's squirrel but is clustered within the craniodental variation of the Fraternal squirrel would also support this. In accordance with this peninsular dispersal corridor, Karin et al (2017) suggest a divergence of ∼2.60 Mya among skink populations of Nias (Batu Islands) and Siberut (Mentawai Islands) which would be slightly after to the divergence among Mentawai and Malay Peninsula squirrels. Given that western Sumatra and Mentawai have been suggested to be a forest refuge (Morley, 2000;Lim et al, 2010) it is not straight-forward to assess the direction of the potential dispersal events.…”

“…The endemic fraternal squirrel became isolated from Robinson's squirrel, which was distributed across Sumatra and the Malay Peninsula in the Pliocene. This level of deep divergence between taxa on Mentawai and sister taxa elsewhere in Sundaland has also been identified in other taxa such as gibbons, civets and skinks (Chan et al, 2010;Patou et al, 2010;Karin et al, 2017) and even deeper divergence was found in macaques (Evans et al, 2017). This sister relationship between Mentawai and Sumatra-Malay Peninsula populations (Meijaard and Groves, 2004;Chan et al, 2010;Patou et al, 2010;Arifin et al, 2018) however, is not the most common in mammals (Wilting et al, 2012).…”

“…These common patterns could be due to dispersal barriers following the development of the Bornean highlands and river systems into their more modern representation by ∼8-10 Mya (Hall, 2013;Mason et al, 2011;Yang and Rannala, 2010). Alternatively, vicariance during fragmentation of the Sunda shelf /oceanic dispersal between islands during periods of high sea-levels by ∼5-6 Mya (Karin et al, 2017) if there were early inundations, could also explain this pattern.…”

“…At about the same time the western high elevation Sunda squirrels (S. tahan and S. altitudinis) diverged from the western slender and Jentink's squirrels. This period was also characterized by diversification across Sundaland in semiarboreal rough-skinned skinks, bulbuls, barbets and Sundaic freshwater crabs (Den Tex et al, 2010;Klaus et al, 2013;Karin et al, 2017;Manawatthana et al, 2017). These common patterns could be due to dispersal barriers following the development of the Bornean highlands and river systems into their more modern representation by ∼8-10 Mya (Hall, 2013;Mason et al, 2011;Yang and Rannala, 2010).…”