Evolutionary and biogeographic patterns of the Badidae (Teleostei: Perciformes) inferred from mitochondrial and nuclear DNA sequence data

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Abstract

We reconstructed phylogenetic relationships of the family Badidae using both mitochondrial and nuclear nucleotide sequence data to address badid systematics and to evaluate the role of vicariant speciation on their evolution and current distribution. Phylogenetic hypotheses were derived from complete cytochrome b (1140 base pairs) sequences of 33 individuals representing 13 badid species, and using three species of Nandidae as outgroups. Additionally, we sequenced the nuclear RAG1 (1473 base pairs) and Tmo-4C4 (511 base pairs) genes from each of the badid species and one representative of the outgroup. Our molecular data provide the first phylogenetic hypothesis of badid intrarelationships. Analysis of the mitochondrial and nuclear nucleotide sequence data sets resulted in well-supported trees, indicating a basal split between the genera Dario and Badis, and further supporting the division of the genus Badis into five species groups as suggested by a previous taxonomic revision of the Badidae. Within the genus Badis, mitochondrial and nuclear phylogenies differed in the relative position of B. kyar. We also used our molecular phylogeny to test a vicariant speciation hypothesis derived from geological evidence of large-scale changes in drainage patterns in the Miocene affecting the Irrawaddy– and Tsangpo–Brahmaputra drainages, in the southeastern Himalaya. Within both genera, Badis and Dario, we observed a divergence into Irrawaddy– and Tsangpo–Brahmaputra clades. Using a cytb substitution rate of 8.2 × 10−9 (substitutions × base pair−1 × year−1), we tentatively date this vicariant event at the Oligocene–Miocene boundary (19–24 Myr). It is concordant with a hypothesized paleo connection of the Tsangpo river with the Irrawaddy drainage that was most likely interrupted during Miocene orogenic events through tectonic uplifts in eastern Tibet. Our data, therefore, indicate a substantial role of vicariant-based speciation shaping the current distribution patterns of badids.

Introduction

The freshwater ichthyofauna of tropical Asia with around 2100 valid species, and an estimated total number of 3000 species is still poorly known (Lundberg et al., 2000). Recent research efforts that focused on new collections from previously un- or underexplored regions have added considerably to species numbers and towards a better understanding of the biodiversity of this highly endangered fauna (e.g., Kottelat, 2001). For example, until recently, the Indo-Burmese family Badidae (Teleostei, Perciformes) was considered to contain one single genus, and one to three species. New collections, and a taxonomic revision revealed that the family Badidae currently comprises 15 species, assigned to two genera Badis and Dario (Kullander and Britz, 2002).

In the past, the genus Badis was generally treated as a member of the family Nandidae (leaffishes) together with the genera Nandus, Polycentrus, Monocirrhus, Afronandus, and Polycentropsis (the genus Pristolepis had also occasionally been included in the nandids). Nandids are usually classified as a Percoidei family, although close relationships to the Anabantoidei (labyrinth fishes) or the Channoidei (snakeheads) have been postulated (Gosline, 1968, Gosline, 1971; Nelson, 1969; Rosen and Patterson, 1990). Based on morphological and behavioral data, a separate family, Badidae for Badis alone was erected by Barlow et al. (1968). Following Kullander and Britz (2002), the family Nandidae is now restricted to the genus Nandus and the genera Polycentrus, Monocirrhus, Afronandus, and Polycentropsis, formerly assigned to the Nandidae, are classified in the Polycentridae. Kullander and Britz (2002) hypothesized a sistergroup relationship of badids and nandids based on a uniquely shared derived character of the caudal skeleton.

Kullander and Britz (2002) based on external morphological characters, but mostly on information derived from color patterns, assigned the Badis species to five species groups: B. assamensis species group (B. assamensis and B. blosyrus), B. badis species group (B. badis, B. kanabos, B. chittagongis, and B. ferrarisi), B. corycaeus species group (B. corycaeus and B. pyema), B. ruber species group (B. ruber, B. siamensis, and B. khwae), and B. kyar. In their revision of the Badidae, Kullander and Britz (2002) also erected a new genus Dario with three species (D. dario, D. hysginon, and D. dayingensis) for small badid fishes with adult size below 25 mm, which are morphologically clearly distinct from Badis. Nevertheless, the phylogenetic relationships among the badid species, and species groups still remain unresolved.

Badids are small freshwater fish including the smallest percoid known so far (Dario dario with a standard length <20 mm). They normally inhabit small streams or hill streams with slow to moderate flow, coastal drainages or ditches with stagnant waters. They are lurking predators probably feeding on small invertebrates (Barlow et al., 1968). The distribution of the Badidae includes the Indian subcontinent, Pakistan, Nepal, Bangladesh, Myanmar, Peninsular Thailand, the Mae Khlong drainage, and part of the Mekong basin in South East Asia as well as the Upper Irrawaddy in southern Yunnan, China (Fig. 1, Table 1). The badid species are largely allopatric in distribution with few cases of sympatry: B. kanabos, B. blosyrus, and D. dario in western Assam, B. badis and B. assamensis in northern Assam, and B. kyar, B. corycaeus, and D. hysginon in northern Myanmar. Allopatric species with adjacent distribution suggest vicariant speciation as the main force underlying badid diversification (Kullander and Britz, 2002).

It has long been recognized that paleo-drainages of major continental East Asian rivers, draining the southeastern 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. 2A). 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. 2), cannot be ruled out as an additional factor influencing these large-scale changes in drainage patterns (Clark et al., 2004; Hallet and Molnar, 2001). The evolution of drainage systems in Asia can be summarized in four stages (Fig. 2, 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. 2A). (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. 2B). (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. 2C). (d) Capture of the Tsangpo river through the Brahmaputra river into its modern drainage position (Fig. 2D).

Only 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). Furthermore, to our knowledge, thus far no phylogenetic studies have been conducted to test underlying vicariant speciation hypotheses. The former connection of the Tsangpo and the Irrawaddy rivers (Fig. 2C) may be important in understanding badid biogeography, and leads to a testable vicariant hypothesis. D. dario, as well as the B. badis and B. assamensis species groups are found in the Tsangpo–Brahmaputra–Ganges drainages, whereas the remaining two Dario species, B. kyar and the B. corycaeus species groups are found in the Upper Irrawaddy drainage (Fig. 1). Based on geological evidence for large-scale changes in drainage systems (Fig. 2, Brookfield, 1998; Clark et al., 2004; Zeitler et al., 2001) we hypothesize an important vicariant event separating badid species found in the Tsangpo–Brahmaputra–Ganges drainage from species found in the Irrawaddy drainage. Unfortunately, neither molecular nor morphological phylogenies of badids exist that may allow to test this hypothesis. Thus, the aims of this study are (1) to establish a robust molecular phylogeny of the Badidae using both mitochondrial and nuclear DNA sequence data, and (2) to test a vicariant speciation hypothesis derived from geological evidence of a former Miocene connection of the Tsangpo river with the Irrawaddy drainage. This will allow us to evaluate the role of vicariance in shaping the current distribution patterns of badids.

Section snippets

DNA sources and extraction

To assess the molecular phylogeny of the Badidae, 33 individuals representing 12 out of 15 described species as well as one possibly undescribed species were utilized (Table 1). We were not able to obtain ethanol preserved material from B. chittagongis, B. ferrarisi (both belonging to the B. badis group) and D. dayingensis. In addition, three representatives of the genus Nandus (Teleostei, Nandidae), the sistergroup of the Badidae as supported by morphological (Kullander and Britz, 2002) and

Phylogenetic analyses

Specifications of the different data sets used for the phylogenetic analyses, evolutionary models applied, as well as ML (non-clock, clock), MP, and ME scores are given in Table 2. No base compositional biases were observed (Table 2). The partition homogeneity test detected significant congruence between all data partitions (cytb vs. RAG1, P = 0.71; cytb vs. Tmo-4C4, P = 0.64; RAG1 vs. Tmo-4C4, P = 1.0; and mtDNA vs. nucDNA, P = 0.12). The alignment of cytb gene nucleotide sequences of 33 Badidae

Intrarelationships of the Badidae

Phylogenetic studies based on multiple loci reveal a more complete picture of the evolutionary history of a group of closely related species than those solely based on a single locus (e.g., Machado and Hey, 2003; Rokas et al., 2003). Here, we studied the phylogenetic history of the family Badidae based upon one mitochondrial (cytb) and two nuclear (RAG1 and Tmo-4C4) genes. Our phylogenetic analyses provided a robust framework for badid intrarelationships. All genes validated with high

Acknowledgments

We are grateful to M. Kottelat (Cornol, Switzerland) and F. Schäfer (Rotgau, Germany) for providing some of the samples. Specimens were collected during field surveys supported by grants to F. Fang from the Hierta-Retzius Foundation (the Royal Swedish Academy of Sciences), the Ax:son Johnson Foundation, and the Riksmusei Vänner, and to SOK from the Swedish Natural Science Research Council (R-RA 04568-316). We are indebted to K. Lahkar (Dibrugarh University), U Win Aung, and U Tun Shwe

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