Phylogeny and biogeography of Chinese sisorid catfishes re-examined using mitochondrial cytochrome b and 16S rRNA gene sequences

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Abstract

The family Sisoridae is one of the largest and most diverse Asiatic catfish families, most species occurring in the water systems of the Qinhai-Tibetan Plateau and East Himalayas. To date published morphological and molecular phylogenetics hypotheses of sisorid catfishes are part congruent, and there are some areas of significant disagreement with respect to intergeneric relationships. We used mitochondrial cytochrome b and 16S rRNA gene sequences to clarify existing gaps in phylogenetics and to test conflicting vicariant and dispersal biogeographical hypotheses of Chinese sisorids using dispersal–vicariance analysis and weighted ancestral area analysis in combination with palaeogeographical data as well as molecular clock calibration. Our results suggest that: (1) Chinese sisorid catfishes form a monophyletic group with two distinct clades, one represented by (Gagata (Bagarius, Glyptothorax)) and the other by (glyptosternoids, Pseudecheneis); (2) the glyptosternoid is a monophyletic group and Glyptosternum, Glaridoglanis, and Exostoma are three basal species having a primitive position among it; (3) a hypothesis referring to Pseudecheneis as the sister group of the glyptosternoids, based on morphological evidence, is supported; (4) the genus Pareuchiloglanis, as presently defined, is not monophyletic; (5) congruent with previous hypotheses, the uplift of Qinghai-Tibetan Plateau played a primary role in the speciation and radiation of the Chinese sisorids; and (6) an evolutionary scenario combining aspects of both vicariance and dispersal theory is necessary to explain the distribution pattern of the glyptosternoids. In addition, using a cytochrome b substitution rate of 0.91% per million years and 0.23% for 16S rRNA, we tentatively date that the glyptosternoids most possibly originated in Oligocene–Miocene boundary (19–24Myr), and radiated from Miocene to Pleistocene, along with a center of origin in the Irrawaddy–Tsangpo drainages and several rapid speciation in a relatively short time.

Introduction

The family Sisoridae, established by Regan (1911), is one of the largest and most diverse Asiatic families, quite a few sisorid species inhabiting in basins around the Qinghai-Tibetan Plateau and East Himalayas. The main basins in which these fishes live include: Yaluzangbujiang (Tsangpo), Irrawady, Nujiang (Salween), Lancangjiang (Mekong River), Jingshajiang (Upper Yangtze), Yuanjiang (Red River), Nanpanjiang (Upper Pearl River), and Brahmaputra basin. They are highly adaptive to torrential environment. Its special distribution and phylogenetic interpretation would be helpful in determining the development of water systems in this area. It is assumed that speciation events within this group are linked to historical changes in the geography of their main distribution habitat, which have been severely affected by several uplift events along the Qinhai-Tibetan Plateau. These geological processes have been considered to play a fundamental vicariant role in species of many other vertebrates endemic to this region (Luo et al., 2004, Pang et al., 2003, Rüber et al., 2004). Thus, we wanted to test whether the uplift of the Qinghai-Tibetan Plateau also facilitated speciation and adaptation process of the sisorids.

The currently accepted taxonomy of the sisorid catfishes is outlined in Table 1. The revision by de Pinna (1996), based on morphology, divided the family Sisoridae into two subfamilies: Sisorinae and Glyptosterninae. The Sisoridae (sensu stricto) is composed of two major lineages, one represented by (Bagarius (Sisor (Nangra, Gagata))) and the other by (Glyptothorax (Pseudecheneis, “glyptosternoids”)). There are 12 genera of sisorids found in China, including genera Glyptothorax, Gagata, Bagarius, and Pseudecheneis as well as eight genera of glyptosternoids, i.e., Glyptosternum, Exostoma, Pseudexostoma, Oreoglanis, Pareuchiloglanis, Euchiloglanis, Parachiloglanis, and Glaridoglanis. The other genus Myersglanis is only found in India. And most of the eight genera glyptosternoids are highly specialized, with strongly depressed heads and bodies, and greatly enlarged pectoral and pelvic fins modified to form an adhesive apparatus (e.g., Fig. 1).

Despite considerable studies, the phylogenetic and taxonomic relationships within the sisorids, and the deeper relationships of the glyptosternoids, remain controversial (various hypotheses are illustrated in Fig. 2). In particular, considering disagreement surrounds the phylogenetic affinities of the genus Pseudecheneis. Early studies demonstrated similarities and differences between the genus Pseudecheneis and various “glyptosternoid sisorids” but were not conclusive about their possible phylogenetic affinities (Hora, 1952, Hora and Silas, 1952a, Hora and Silas, 1952b). Hora (1952) implied that the glyptosternoids, in addition to the genus Pseudecheneis, formed a monophyletic group. Chu (1982) focused exclusively on the monophyletic origin of Pseudecheneis, but without addressing which group is most closely related. Tilak (1976) proposed a close relationship between Pseudecheneis and the glyptosternoids, mainly on the basis of an overall similarity in their pectoral spine morphology as well as a study of the adhesive thoracic apparatus. In support of Tilak’s view, de Pinna (1996) suggested that Pseudecheneis is the sister group of the glyptosternoids on the basis of a large set of synapomorphies. But his work did not cover the intrarelationships of the glyptosternoids. He’s work (1996) showed us a “full known” of intrarelationship of the glyptosternoids based on 60 osteological characters. Peng et al. (2004) first verified the monophyly of glyptosternoids and proposed different phylogenetic relationships based on the analysis of mitochondrial DNA cytochrome b gene sequences. However, Peng et al. (2004) did not resolve the placement of genus Pseudecheneis. Strikingly, Guo et al. (2004) did not agree with that of Peng et al. (2004) as for the monophyly of glyptosternoids and the placement of Pseudecheneis based on the analysis of mitochondrial 16S rRNA sequences. Such a perspective is therefore still far from clear promoting us to pursue further studies of the molecular phylogenetics of the sisorid catfishes.

It has long been recognized that paleo-drainages of major continental East Asian Rivers, draining the south-eastern Tibet plateau margin, differed markedly from their current drainage patterns (Brookfield, 1998, Clark et al., 2004, Gregory, 1925, Gregory and Gregory, 1923, Hallet and Molnar, 2001, Métivier et al., 1999, Seeber and Gornitz, 1983, Zeitler et al., 2001). In a recent study, Clark et al. (2004) suggested that these rivers were once tributaries to a single southward flowing system, which drained into the South China Sea (Fig. 3A). Subsequent reorganization into modern major river drainages was primarily caused by river capture and reversal events associated with the initiation of Miocene uplifts in eastern Tibet (Clark et al., 2004). Although large-magnitude tectonic shear, prompted by the Indian–Asian collision around the eastern Himalayan syntaxis (especially in the “Three River” area where the Salween, Mekong, and Yangtze rivers run parallel, see Fig. 3), river capture and reversal events cannot be ruled out as an additional factor influencing these large-scale changes in drainage patterns (Clark et al., 2004, Hallet and Molnar, 2001). As reviewed by Rüber et al. (2004), the evolution of drainage systems in Asia can be summarized in four stages (Fig. 3, Clark et al., 2004). (a) Upper Yangtze, Middle Yangtze, Upper Mekong, and Upper Salween rivers drained into the South China Sea through the paleo Red River (Fig. 3A). (b) Capture/reversal of the Middle Yangtze river redirected drainage away from the Red River and into the East China Sea through the Lower Yangtze river (Fig. 3B). (c) Capture of the Upper Yangtze River into the Lower Yangtze River, and of the Upper Mekong and Upper Salween rivers into their modern drainage position. The Tsangpo River was also captured to the south through the Irrawaddy River (Fig. 3C). (d) Capture of the Tsangpo river through the Brahmaputra river into its modern drainage position (Fig. 3D).

Only a few studies have recognized the potential importance of changes in drainage basin morphology in understanding biogeographic patterns of the South East Asian Ichthyofauna (e.g., Kottelat, 1989, Rüber et al., 2004). Hora (1952) hypothesized that the glyptostenoids originated in Yunnan of China and radiated due to tectonic uplifting and movements in the region. Hora and Silas (1952a) also hypothesized that the glyptosternoids achieved their current distribution by means of dispersal, based on the geological hypothesis proposed by Gregory and Gregory (1923) and Gregory (1925), in which it is considered that, due to regional subsidence, some rivers of this area changed their direction by river-capture. They also considered that the orogenic movements of the Himalayan mountain range formed a highway, which supported the dispersal of the glyptisternoids. However, recent historical biogeography study (He, 1995), based on morphology, provided an alternative explanation for the distribution pattern of the glyptosternoids, and hypothesized that the speciation of this group has a direct relationship with three uplifting events of the Qinhai-Tibetan Plateau. In addition, to our knowledge, thus few molecular phylogenetic studies have been conducted to test underlying vicariant/dispersed speciation hypotheses.

16S rRNA gene evolves at a slower rate than mitochondrial DNA cytochrome b gene, so the two genes were selected to recover the maximum phylogenetic information for the terminal nodes at the base of the tree. Drawing on the combined molecular data, the goals of this study were: (1) to elucidate existing gaps in the phylogenetic relationships among the Chinese sisorids; (2) to use molecular calibrations to investigate if the divergence events within the sisorids are correlated with the uplift events of the Qinhai-Tibetan Plateau; (3) to resolve the biogeographic (dispersal/vicariance) controversy surrounding the Qinhai-Tibetan Plateau distribution of the glyptosternoids. To achieve the final aim, we attempted to reconstruct the ancestral distributions in the phylogeny of the glyptosternoids.

Section snippets

Sample collection

The specimens used in this study, including 32 individuals from 17 sisorid catfish species and five non-sisorids, following the system of Chu et al. (1999), were collected from a variety of locations in China (Table 2, Fig. 4). Due to difficulties of sampling, Myserglanis and Parachiloglanis were not included in this study. Muscle tissue used was preserved in 95% ethanol, and most specimens were deposited in the Fish Collection of the Institute of Hydrobiology of the Chinese Academy of

Cytochrome b

For eight individuals, we sequenced the complete cytochrome b gene and identified six haplotypes (see Table 2). The other 17 complete cytochrome b sequences (with the exception of Pseudobagrus kyphus, 1132 bp) were obtained from GenBank. A total of 1138 positions were analyzed, of which 564 characters were variable, and 458 of these characters were phylogenetically informative (49.5 and 40.2%, respectively). Levels of sequence divergence (uncorrected distance) between the outgroup and ingroup

Intrarelationships of the Chinese sisorids

The Sisoridae has been consistently recognized as a natural group (de Pinna, 1996, Diogo et al., 2002) based on morphology. Despite the low support for this node in ML, MP, and NJ analysis, these results are congruent with morphology, which further lends support to the hypothesis of monophyletic sisorids. Moreover, Bayesian tree indicates a robust node support (PP = 97%). In support of Guo et al. (2004), our result indicates that Chinese sisorid catfishes are composed of two major lineages, one

Acknowledgments

We extend our sincerest gratitude to Mrs. Sheng-hong Zhou, Zhen-quan Ye, and Dr. Zuo-gang Peng for assistance in collecting specimens or providing tissues in their care, and Dr. C. Smith (University of Leicester) for helpful suggestions. This work was supported by the Chinese Academy of Sciences (KSCX2-SW-101B), the Innovation Program (220101) of the Institute of Hydrobiology of Chinese Academy of Sciences to S.P. He. Insightful comments from the anonymous reviewers improved the clarity and

References (74)

  • Z. An et al.

    Evolution of Asian monsoons and phased uplift of the Himalayas–Tibetan Plateau since Late Miocene times

    Nature

    (2001)
  • D.R. Brooks et al.

    How to do BPA, really

    J. Biogeogr.

    (2001)
  • T.R. Buckley et al.

    Evaluating hypotheses on the origin and evolution of the New Zealand alpine cicadas (Maoricicada) using multiple-comparison tests of tree topology

    Mol. Biol. Evol.

    (2001)
  • X. Chu

    Systematics and evolutionary pedigree of the glyptosternoid fishes (Family Sisoridae)

    Acta Zootaxa. Sinica

    (1979)
  • X. Chu

    Phylogeny of the genus Pseudecheneis (Siluriformes: Sisoridae), with descriptions of two new species

    Acta Zootaxonomica Sinica (in Chinese)

    (1982)
  • X. Chu et al.

    Fauna Sinica, Class Teleostei, Siluriformes (in Chinese)

    (1999)
  • Clark, M.K., Schoenbohm, L.M., Royden, L.H., Whipple, K.X., Burchfiel, B.C., Zhang, X., Tang, W., Wang, E., Chen, L.,...
  • M.C.C. de Pinna

    A phylogenetic analysis of the Asian catfish families Sisoridae, Akysidae, and Amblycipitidae, with a hypothesis on the relationships of the neotropical Aspredinidae (Teleostei: Ostariophysi)

    Fieldiana Zool. (N.S.)

    (1996)
  • P. De Riijk et al.

    Database on the structure of large subunit ribosomal RNA

    Nucleic Acids Res.

    (1999)
  • R. Diogo et al.

    Osteology and myology of the cephalic region and pectoral girdle of Glyptothorax fukiensis (Rendahl, 1925), comparison with other sisorids, and comments on the synapomorphies of the Sisoridae (Teleostei: Siluriformes)

    Belg. J. Zool.

    (2002)
  • X. Fang et al.

    Loess in Kunlun Mountains and its implications on desert development and Tibetan Plateau uplift in West China

    Sci. China (Series D)

    (2002)
  • J.S. Farris et al.

    Testing significance of incongruence

    Cladistics

    (1995)
  • J.P. Felsenstein

    Confidence limits on phylogenies: an approach using the bootstrap

    Evolution

    (1985)
  • X. Ge et al.

    Uplift dynamics of Qinghai–Tibet Plateau and Altun fault

    Geol. China (in Chinese)

    (2002)
  • N. Goldman

    Simple diagnostic statistical tests of models of DNA substitution

    J. Mol. Evol.

    (1993)
  • N. Goldman

    Statistical tests of models of DNA substitution

    J. Mol. Evol.

    (1993)
  • J.W. Gregory

    The evolution of the river system of South-Eastern Asia

    Scottish Geograph. Mag.

    (1925)
  • J.W. Gregory et al.

    The Alps of Chinese Tibet and their geographical relations

    Geograph. J.

    (1923)
  • X. Gu et al.

    Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites

    Mol. Biol. Evol.

    (1995)
  • X. Guo et al.

    Mitochondrial 16S rRNA sequence variations and phylogeny of the Chinese sisorid catfishes

    Chinese Sci. Bull.

    (2004)
  • B. Hallet et al.

    Distorted drainage basins as markers of crustal strain east of the Himalaya

    J. Geophys. Res.

    (2001)
  • B. Hausdorf

    Weighted ancestral area analysis and a solution to the redundant distribution problem

    Syst. Biol.

    (1998)
  • D. He et al.

    Molecular phylogeny of the specialized schizothoracine fishes (Teleostei: Cyprinidae), with their implications for the uplift of the Qinghai-Tibetan Plateau

    Chinese Sci. Bull.

    (2004)
  • S. He

    The analysis of historical biogeography for the glyptosternoid fishes (Teleoste: Siluriformes, Sisoridae)

    Biogeographica

    (1995)
  • S. He

    The phylogeny of the glyptosternoid fishes (Teleostei: Siluriformes, Sisoridae)

    Cybium

    (1996)
  • S. He et al.

    The biogeography of Amphiliidae and Sisoridae (Teleositei: Siluriformes)

    Acta Zootax. Sinica. (in Chinese)

    (1998)
  • D.M. Hillis et al.

    Signal, noise, and reliability in molecular phylogenetic analyses

    J. Heredity

    (1992)
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