Relict groups of spiny frogs indicate Late Paleogene-Early Neogene trans-Tibet dispersal of thermophile faunal elements

Abstract

Background The Himalaya-Tibet orogen (HTO) presents an outstanding geologically active formation that contributed to, and fostered, modern Asian biodiversity. However, our concepts of the historical biogeography of its biota are far from conclusive, as are uplift scenarios for the different parts of the HTO. Here, we revisited our previously published data set of the tribe Paini extending it with sequence data from the most western Himalayan spiny frogs Allopaa and Chrysopaa and using them as an indirect indicator for the potential paleoecological development of Tibet. Methods We obtained sequence data of two mitochondrial loci (16S rRNA, COI) and one nuclear marker (Rag1) from Allopaa samples from Kashmir Himalaya as well as Chrysopaa sequence data from the Hindu Kush available from GenBank to complement our previous data set. A Maximum likelihood and dated Bayesian gene tree were generated based on the concatenated data set. To resolve the inconsistent placement of Allopaa, we performed different topology tests. Results Consistent with previous results, the Southeast Asian genus Quasipaa is sister to all other spiny frogs. The results further reveal a basal placement of Chrysopaa relative to Allopaa and Nanorana with an estimated age of ca. 26 Mya. Based on the topology tests, the phylogenetic position of Allopaa as a sister clade to Chaparana seems to be most likely, resulting in a paraphyletic genus Nanorana and a separation from the latter clade around 20 Mya, although a basal position of Allopaa to the genus Nanorana cannot be entirely excluded. Both, the placements of Chrysopaa and Allopaa support the presence of basal Paini lineages in the far northwestern part of the HTO, which is diametrically opposite end of the HTO with respect to the ancestral area of spiny frogs in Southeast Asia. These striking distributional patterns can be most parsimoniously explained by trans-Tibet dispersal during the late Oligocene (subtropical Chrysopaa) respectively early Miocene (warm temperate Allopaa). Within spiny frogs, only members of the monophyletic Nanorana+Paa clade are adapted to the colder temperate climates, indicating that high-altitude environments did not dominate in the HTO before ca. 15 Mya. Our results are consistent with fossil records suggesting that large parts of Tibet were characterized by subtropical to warm temperate climates at least until the early Miocene. They contradict prevalent geological models of a highly uplifted late Paleogene proto-Plateau.

Morphological and molecular data on tadpoles of the westernmost Himalayan spiny frog Allopaa hazarensis (Dubois & Khan, 1979)

“…Here we report on larvae of the dicroglossid frog Allopaa hazarensis. Our work is based on morphological and DNA data of A. hazarensis tadpoles and previously compiled molecular data sets (Hofmann et al 2019(Hofmann et al , 2021. The study provides the first photographs of A. hazarensis larvae, supporting morphological data, and additional distribution records of the species.…”

“…The latter two genera represent the most western dicroglossid frogs that occur in the Himalayan-Tibetan orogenic belt (HTO). Recently, the phylogenetic placement of Allopaa from Kashmir Himalaya and Chrysopaa from the Hindu Kush has been addressed for the first time (Hofmann et al 2021). This study indicates no close taxonomic relations between the two genera and their geographical neighbouring spiny frogs and suggests a trans-Tibet dispersal during the late Oligocene (Chrysopaa) and early Miocene (Allopaa) from the eastern margin of the HTO.…”

“…We aligned the new sequences (accession numbers 16S: MW723172-MW723173, COI: MW723177-MW723178, Rag1: MW728951-MW728952) to data available from our previous studies (Hofmann et al 2019(Hofmann et al , 2021 by eye; for accession numbers and detailed information of these previous data see supplementary table in Hofmann et al (2021). The 16S sequences were aligned based on secondary structures.…”

On the edge of the Shivaliks: An insight into the origin and taxonomic position of Pakistani toads from the Duttaphrynus melanostictus complex (Amphibia, Bufonidae)

“…Recently, two basic biogeographic scenarios have been hypothesized for the origin of different amphibian taxa distributed in northern Pakistan: i) dispersal of ancestral lineages during the Miocene from East or Southeast China into the far northwestern part of the Himalaya-Tibet orogen along a warm temperate corridor that existed in significant parts of Paleo-Tibet's interior (Hofmann et al 2021), this corridor played probably an important role in the initial diversification process of Himalayan faunal organisms (Schmidt et al 2012), (ii) dispersion on widely distributed species characterized by the low level of genetic divergence that followed Shivalik Hills and the Indo-Gangetic plain and reached the territory of Pakistan (Jablonski et al 2020(Jablonski et al , 2021 as a result of the Pleistocene or Holocene colonisations (see Othman et al 2020). Although these are presumable biogeographic models, the second scenario could be now applied for D. melanostictus from Pakistan.…”

“…Due to the topographic heterogeneity and habitat diversity, it might be plausible that Pakistani amphibian populations of different genera with the Oriental affiliation may hold a different evolutionary history compared to their populations from other parts of South-East Asia. The significance of the far-western part of the Himalaya and the Indo-Gangetic plain for understanding the biogeography of taxa distributed across these geomorphological domains has been recently shown in several species groups (see Allopaa, Chrysopaa, Microhyla, Nanorana, Scutiger, Sphaerotheca;Hofmann et al 2017Hofmann et al , 2019Hofmann et al , 2021Jablonski et al 2020Jablonski et al , 2021. However, except for Khan´s (2001) original work, populations of D. melanostictus from Pakistan, including toads from the type locality where the "hazarensis" population has been described, have not been studied so far in a broader biogeographical context (cf.…”