Phylogeny of spiny frogs Nanorana (Anura: Dicroglossidae) supports a Tibetan origin of a Himalayan species group.

Sylvia Hofmann,Spartak N Litvinchuk,Joachim Schmidt,Georg Miehe,Jia-Tang Li,Chitra B Baniya

doi:10.1002/ece3.5909

Abstract

Recent advances in the understanding of the evolution of the Asian continent challenge the long‐held belief of a faunal immigration into the Himalaya. Spiny frogs of the genus Nanorana are a characteristic faunal group of the Himalaya–Tibet orogen (HTO). We examine the phylogeny of these frogs to explore alternative biogeographic scenarios for their origin in the Greater Himalaya, namely, immigration, South Tibetan origin, strict vicariance. We sequenced 150 Nanorana samples from 62 localities for three mitochondrial (1,524 bp) and three nuclear markers (2,043 bp) and complemented the data with sequence data available from GenBank. We reconstructed a gene tree, phylogenetic networks, and ancestral areas. Based on the nuDNA, we also generated a time‐calibrated species tree. The results revealed two major clades (Nanorana and Quasipaa), which originated in the Lower Miocene from eastern China and subsequently spread into the HTO (Nanorana). Five well‐supported subclades are found within Nanorana: from the East, Central, and Northwest Himalaya, the Tibetan Plateau, and the southeastern Plateau margin. The latter subclade represents the most basal group (subgenus Chaparana), the Plateau group (Nanorana) represents the sister clade to all species of the Greater Himalaya (Paa). We found no evidence for an east–west range expansion of Paa along the Himalaya, nor clear support for a strict vicariance model. Diversification in each of the three Himalayan subclades has probably occurred in distinct areas. Specimens from the NW Himalaya are placed basally relative to the highly diverse Central Himalayan group, while the lineage from the Tibetan Plateau is placed within a more terminal clade. Our data indicate a Tibetan origin of Himalayan Nanorana and support a previous hypothesis, which implies that a significant part of the Himalayan biodiversity results from primary diversification of the species groups in South Tibet before this part of the HTO was uplifted to its recent heights.

Highlights

We examine the phylogeny of these frogs to explore alternative biogeographic scenarios for their origin in the Greater Himalaya, namely, immigration, South Tibetan origin, strict vicariance
Our data indicate a Tibetan origin of Himalayan Nanorana and support a previous hypothesis, which implies that a significant part of the Himalayan biodiversity results from primary diversification of the species groups in South Tibet before this part of the Himalaya–Tibet orogen (HTO) was uplifted to its recent heights
The key to disentangling the paleoclimatology and biogeography of the HTO lies in the Himalaya (Molnar, 1986; Searle, 2013) for the following reasons: i) Most of the modern geological models differ with respect to the uplift history of this part of the mountain system (Schmidt, Opgenoorth, & Miehe, 2016, and refs. therein), ii) the uplift of the Greater Himalaya markedly influences the climate in the interior of High Asia and on a global scale (Boos & Kuang, 2010; Hodges, Hurtado, & Whipple, 2001; Sanwal et al, 2013), and iii) South Tibet may have been an important evolutionary center during the Cenozoic, which impacted the modern faunas of Central and East Asia (Schmidt, Opgenoorth, Holl, & Bastrop, 2012; Weigold, 2005)

Summary

| INTRODUCTION

For the past 45 ± 5 million years, the Earth has experienced one of the most dramatic continental collisions, when India collided with and was subducted beneath Asia (Gibbons, Zahirovic, Müller, Whittaker, & Yatheesh, 2015; Li et al, 2015; Lippert, van Hinsbergen, & DupontNivet, 2014; Molnar, Boos, & Battasti, 2010). A similar explanation has been proposed for the evolution of highly isolated non-wind-dispersed Himalayan alpine plants (Miehe et al, 2015) This Tibetan-origin scenario postulates that during the early phase of mountain uplift, South Tibet was an independent center of evolution that was well separated from other mountainous regions (Schmidt, 2006; Schmidt et al, 2012). Spiny frogs of the genus Nanorana, subfamily Dicroglossinae, are a characteristic species group of the HTO, living mostly in swift boulder-strewn streams (Dubois, 1975) These frogs are found across the Himalayan arc from northern Pakistan and northern India, through Nepal, Sikkim, and Bhutan, to western China (Hengduan Shan), Myanmar, Thailand, Laos, northern Vietnam, and to montane southern China (Frost, 2019). Under the Tibetan-origin scenario, endemic Himalayan lineages are expected to show disjunct distribution with no close relationships to lineages occurring in adjacent parts of the mountain system, and which are of greater phylogenetic age.

| MATERIALS AND METHODS

| DISCUSSION

Findings

| Conclusions