Zhangixalus

Dufresnes, Christophe, Ambu, Johanna, Prasad, Vishal Kumar, Borzée, Amaël & Litvinchuk, Spartak N, 2022, A phylogeographical framework for Zhangixalus gliding frogs, with insight on their plasticity of nesting behaviour, Biological Journal of the Linnean Society 135 (1), pp. 40-51 : 46-48

BIOGEOGRAPHY OF ZHANGIXALUS

Our temporally and spatially explicit phylogeogaphy for Zhangixalus was consistent with partial timetrees previously published for some members of the genus. Similarities were expected with the study by Chen et al. (2020), from which we implemented our calibration points, but we also recovered nearly identical divergence times as in independently calibrated molecular clocks (e.g. Pan et al., 2017; Matsui et al., 2019). In agreement with previous studies ( Pan et al., 2017), our phylogenetic analysis suggests the following biogeographical scenario, with respect to the evolution of the climate ( Zachos et al., 2001, 2008; Wan et al., 2007; Jacques et al., 2011; Miller et al., 2011) and landscapes in Asia ( Qin et al., 2004; Sibuet & Hsu, 2004; Ni et al., 2014; Chen et al., 2015; Li et al., 2019).

The Zhangixalus genus was dated to the Late Oligocene (~28 Mya in the study by Chen et al., 2020) and first diversified between Sunda and Asia in the Early Miocene (~20 Mya). At this time, Earth experienced a relatively cold period ( Zachos et al., 2001, 2008), and the ancestors of most tropical amphibians, such as rhacophorids, must have retained essentially meridional distributions. Early Zhangixalus species eventually penetrated northern ranges ( Japan and Central China) during the warmer Mid-Miocene optimum ( Zachos et al., 2001, 2008). The subsequent cooling and drying of the climate within the last 10 Myr ( Miller et al., 2011), accompanied by the establishment and intensification of the East Asian monsoon ( Wan et al., 2007; Jacques et al., 2011), then initiated the diversification of several widespread radiations ( Z. dennysi , Z. chenfui and Z. schlegelii complexes).

In particular, South China featured isolated mountain systems surrounded by wide plains, where the dry climate potentially caused long-term population fragmentation. The ensuing lineages might have continued to survive on the Taiwanese slopes as the island uplifted in the Mio-Pliocene ( Sibuet & Hsu, 2004; Chen et al., 2015). The unresolved relationships among internal branches leading to several Taiwanese ( Z. moltrechti , Z. aurantiventris and Z. taipeianus ) and Japanese ( Z. schlegelii and Z. arboreus ) species groups, in addition to their short timeframe of divergence (all ~7.5 Mya), advocate for simultaneous splits from one or a few common ancestors ( Fig. 1 ). Such Taiwan – Japanese ancestor(s) would then have recolonized the tropical regions of Southeast Asia; they diversified into the Z. omeimontis , Z. puerensis and Z. prasinatus clades by the end of the Miocene (~5–7 Mya), and Z. prasinatus subsequently made it back to Taiwan Island.

Most Zhangixalus species or species groups featured Plio-Pleistocene phylogeographical diversifications that coincided with the climatic fluctuations of the Quaternary ( Fig. 1 ; see also Li et al., 2012b, 2015; Pan et al., 2017). The effects of the glaciations were particularly strong in topographically complex areas (e.g. mainland Japan, Taiwan Island, southern Himalayas and Sichuan Basin), where species retracted into narrow refugia (e.g. valleys and other lowland forests). Allopatric evolution during the prolonged glacials, with only brief episodes of expansion and potential gene flow during the short interglacials, thus generated strong genetic differentiation. Structured amphibians are typical from these regions (e.g. Quasipaa in the Sichuan Basin, Yan et al., 2013; Dryophytes in mainland Japan, Dufresnes et al., 2016; Kurixalus on Taiwan Island, Wu et al., 2016). Moreover, we note the colonization of the southern Ryukyus ( Z. owstoni endemic to the Ishigaki island group) during the Late Pliocene, suggesting that the last connection of the Ryukyus with Taiwan Island and the adjacent mainland occurred soon before the Pleistocene glaciations. This is consistent with the pattern found in other rhacophorids (e.g. Buergeria and Kurixalus ) and amphibians in general (e.g. Fejervarya ), whereby Ishigakijima populations diverged during a similar timeframe that led to vicariant speciation in nearly all studied amphibians (reviewed by Dufresnes & Litvinchuk, in press).

Intriguingly, despite regular land bridge connections during the Quaternary glaciations, the Taiwan Strait did not promote exchanges of Zhangixalus species within the last few millions of years; unrelated lineages are found on either side of the Strait. As suggested above, all five Taiwanese endemics appeared earlier (~6–10 Mya) than the final uplift of the island ( Sibuet & Hsu, 2004; Chen et al., 2015), which contributed to their subsequent survival rather than to their initial divergence. Old endemic lineages, sometimes pre-dating the emergence of Taiwan Island by millions of years, are characteristic of other animals ( He et al., 2018), such as the Hynobius salamanders ( Tang et al., 2015).

Such an enigmatic biogeographical pattern could be explained by the distinctive palaeo-landscapes found between Taiwan Island and the adjacent continent. Quaternary Taiwan retained temperate humid forests that probably acted as a long-term refugium for many tropical species, whereas south-eastern mainland China was mostly covered by dry steppelike environments, unsuitable for the dispersal of forest amphibians ( Qin et al., 2004; Ni et al., 2014; Li et al., 2019). Suitable but disconnected from Taiwan Island during interglacial episodes, connected but unsuitable during glacial episodes, the Chinese mainland is, consequently, inhabited exclusively by Zhangixalus species of continental origin (e.g. Z. dennysi ), while the island retained only its endemics. This pattern is exceptional because many continental species colonized Taiwan Island during the Pleistocene (especially amphibians; Dufresnes & Litvinchuk, in press). Yet these mostly involve lowland organisms acclimatized to open landscapes, which had higher opportunities to palaeo-disperse in the region.

Figures

Figure 1. Time-calibrated phylogeny of Zhangixalus lineages, based on ~4 kb of mitochondrial sequences. Node sizes and darkness are proportional to branch support. Lineages are coloured according to their geographical regions. Undescribed lineages are labelled as ‘cf.’, except for Zhangixalus schlegelii and Zhangixalus arboreus, for which the labels provided by Matsui et al. (2019) are used. The bar graph shows the number of splitting events in the timetree in windows of 1 Myr, overlaid by the evolution of temperatures (as given by δ18O) on Earth (red curve, adapted from Zachos et al., 2008). Photograph: Zhangixalus chenfui (S.N.L.).