Phylogeny, evolution, and biogeography of Asiatic Salamanders (Hynobiidae)

Abstract

We sequenced 15 complete mitochondrial genomes and performed comprehensive molecular phylogenetic analyses to study the origin and phylogeny of the Hynobiidae, an ancient lineage of living salamanders. Our phylogenetic analyses show that the Hynobiidae is a clade with well resolved relationships, and our results contrast with a morphology-based phylogenetic hypothesis. These salamanders have low vagility and are limited in their distribution primarily by deserts, mountains, and oceans. Our analysis suggests that the relationships among living hynobiids have been shaped primarily by geography. We show that four-toed species assigned to Batrachuperus do not form a monophyletic group, and those that occur in Afghanistan and Iran are transferred to the resurrected Paradactylodon. Convergent morphological characters in different hynobiid lineages are likely produced by similar environmental selective pressures. Clock-independent molecular dating suggests that hynobiids originated in the Middle Cretaceous [ approximately 110 million years ago (Mya)]. We propose an "out of North China" hypothesis for hynobiid origins and hypothesize an ancestral stream-adapted form. Given the particular distributional patterns and our molecular dating estimates, we hypothesize that: (i) the interior desertification from Mongolia to Western Asia began approximately 50 Mya; (ii) the Tibetan plateau (at least on the eastern fringe) experienced rapid uplift approximately 40 Mya and reached an altitude of at least 2,500 m; and (iii) the Ailao-Red River shear zone underwent the most intense orogenic movement approximately 24 Mya.

Fig. 1.

Traditional relationships among the genera of the family Hynobiidae based on 23 morphological characters (10). The living hynobiids were divided into two groups (Hynobius and Ranodon). The genera Pachyhynobius and Pseudohynobius were not included in that study, and their phylogenetic position relative to the other genera is uncertain.

Fig. 2.

Phylogenetic relationships of living hynobiid salamanders inferred from analyses of mitochondrial genome sequences. Branches with letters have branch support values given below the tree for MP, NJ, unpartitioned Bayesian (UBA), and partitioned Bayesian (PBA) methods. Outgroup species are not shown. Branch lengths were estimated by using ML inference. (Scale bar represents 0.1 substitutions per site.) −, branch was unresolved (i.e., values < 50).

Fig. 3.

Molecular tree topology of hynobiids combined with dating of the phylogenetic nodes. (Upper) Branch lengths are proportional to divergence times. Numbers above the nodes are the mean estimated divergence time (in Mya). Numbers in parentheses represent 95% credibility intervals. The hynobiids originated in the Mid-Cretaceous but began their major diversification after K/T boundary. Three important time points during the evolution of hynobiid are indicated by black triangles. The three geologic events corresponding to these time points are illustrated below the tree. (A) Interior desertification of Asia took place by ≈50 Mya. (B) Tibetan plateau (at least on the east fringe) experienced rapid uplift process ≈40 Mya and reached at least an altitude of 2,500 m. (C) The most intense orogenic movement of the Ailao–Red River shear zone took place 24 Mya.

Fig. 4.

Ancestral state reconstruction for five important traits in hynobiids under the present molecular phylogeny (Cryptobranchidae as outgroup). The five traits are life history (stream-type, blue line; pond-type, pink line), dentition (green circle, transversely oriented; open circle, posteriorly directed), length of larval state (orange moon, long larval state; open moon, short larval state), numbers of eggs laid (blue triangle, less eggs; open triangle, more eggs), and premaxillary fontanelle (red square, present; open square, absent). Numbers along the internodes are posterior probabilities for the five traits under the same order mentioned above. Different living habitats seem to impact the selection of feeding and breeding behaviors among hynobiid adults, causing adaptive convergence to some degree. Ancestral state reconstruction was performed by using mrbayes (Version 3.1) (1,000,000 generations).

Fig. 5.

Current distribution of living hynobiids across the Asian continent. The distribution area of living hynobiids is indicated in green. The locality for related fossil taxa is indicated as a black triangle. North China is hypothesized to be the center for the origin of hynobiids. West China is considered as a secondary diversification center (mainly for mountain-type hynobiids). The Tibetan plateau and its concomitants, loess and deserts, have played important roles in shaping distribution patterns.