Molecular systematics and biogeography of the bent-wing bat complex Miniopterus schreibersii (Kuhl, 1817) (Chiroptera: Vespertilionidae)

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Abstract

The complete mitochondrial ND2 gene (1037 bp) was sequenced to examine relationships within the bent-wing bat complex, Miniopterus schreibersii (Family Vespertilionidae). It was found that M. schreibersii is a paraphyletic assemblage comprising several species. Two major lineages were identified, one of which was restricted to the Palearctic–Ethiopian regions and the other to the Oriental–Australasian regions. This pattern of differentiation was mirrored by the genus as a whole. Speciation and differentiation within the genus Miniopterus appears to have a hierarchical geographical pattern. The earliest divergence corresponds to the Ethiopian–Palearctic and the Oriental–Australasian biogeographical zones. This early divergence is then followed by radiations within each of the Ethiopian, Oriental and Australasian regions. The study also revealed that the number of species currently recognized (11 or 13) is a gross underestimate of the number of actual species. The emerging picture is one of a relatively speciose genus with most species having relatively restricted distributions; few, if any, occur in more than one biogeographical region.

Introduction

The bent-winged bat genus Miniopterus Bonaparte, 1837 is distributed throughout most of Africa, Europe, Asia, New Guinea, Australia, and the Pacific (Nowak, 1999). The various species are often difficult to identify morphologically. The principal distinguishing features are overall size and relative length of the wings, but many of the species descriptions have overlapping linear measurements (e.g., Corbet and Hill, 1992; Dobson, 1878; Tate, 1941; Thomas, 1905, Thomas, 1907, Thomas, 1922). Although pelage color can differ between some species (Harrison, 1956; Thomas, 1906, Thomas, 1907; Thomas and Schwann, 1906), there is also wide variation within species (Lewis and Harrison, 1962). Consequently, the validity of recognizing species solely on pelage color (e.g., Harrison, 1956) has been questioned (Etemad, 1967).

Given the difficulties in discerning unambiguous diagnostic characters, the number of species recognized in Miniopterus has ranged from 10 to 39 (e.g., Hill, 1971, Hill, 1983; Koopman, 1993, Koopman, 1994; Maeda, 1982; Nowak, 1999; Tate, 1941). These various classifications have been constantly reviewed and changed over the years, with no two reviews congruent. Tate (1941) believed that many of the species recognized at the time were actually part of a large Miniopterus schreibersii complex. The most recent syntheses of Koopman (1994) and Nowak (1999) listed 13 and 11 species, respectively, with M. schreibersii seen as a single wide ranging polytypic species. Koopman (1994) included M. medius in M. fuscus whereas Nowak (1999) kept them separate.

Koopman (1994) tentatively divided Miniopterus into five subgroups but stopped short of treating them as subgenera (contra to the assertion by Jones et al., 2002). The five groups were: (1) australis, minor, manavi, paululus and pusillus; (2) fuscus and fraterculus; (3) schreibersii and natalensis; (4) inflatus and magnater; and (5) tristis and robustior.

The species of Miniopterus are generally restricted to one or two biogeographical regions. For example, tristis, australis, pusillus, and magnater occur in the Oriental and Australasian regions, whereas fraterculus, minor, and inflatus are restricted to the Ethiopian region. The exception to this pattern is schreibersii which purportedly occurs in the Palearctic, Ethiopian, Oriental, and Australasian regions and is apparently sympatric with most other species in the genus.

The present study used mitochondrial DNA sequence data to investigate whether the atypically wide distribution of the M. schreibersii complex is attributable to wide dispersal ability or incorrect taxonomy. Within this framework we searched for the existence of regional groups within the complex and compared their relationships to other sympatric species of Miniopterus. This provided a test on whether the complex is in fact monophyletic. We do not attempt to correct the untidy taxonomy of the genus. Sample collection from a wider range of localities and which included a complete synthesis of both genetic and morphological analyses would be required in order to achieve that aim.

Section snippets

Samples

Frozen or alcohol preserved material suitable for DNA analysis was obtained from institutions and researchers from around the world. Species nomenclature for the specimens examined was initially based on those names given to the sample by the researchers from whom the material was obtained (Table 1). The species were Miniopterus australis, M. inflatus, M. magnater, M. manavi, M. schreibersii and M. tristis (Table 1). Also included were three individuals of Miniopterus from the Solomon Islands

Sequence variation

A total of 1037 bp of sequence was obtained from each of the 38 samples. All ND2 sequences have been deposited in GenBank with the Accession Nos. AY169435–AY169472.

Comparisons involving the ingroup and outgroup taxa identified 529 variable sites of which 419 were parsimony informative. Removing the outgroup from the comparisons reduced the number of variable and parsimony informative sites to 468 and 415, respectively.

Transitions outnumbered transversions with an overall transition:transversion

Major lineages within miniopterus

The present study has demonstrated that the Miniopterus schreibersii complex as currently defined is not monophyletic and comprises several species. While it has sometimes been argued that the complex should be divided into further species (e.g., Maeda, 1982; Stebbings and Griffith, 1986), most workers have still assumed that the component taxa would comprise a monophyletic group relative to other members of the genus (Corbet and Hill, 1992; Hill, 1983). The present study is the first to

Conclusions

The present study has conclusively demonstrated that Miniopterus schreibersii is a paraphyletic assemblage comprising at least three species groups centred in the Palearctic, Ethiopian, and Oriental–Australasian regions. The widespread distribution of Miniopterus schreibersii is clearly due to incorrect taxonomy and not exceptional dispersal ability.

The pattern of differentiation observed in the Miniopterus schreibersii complex is mirrored by the genus as a whole. Speciation and differentiation

Acknowledgments

We thank the many individuals and institutions that provided the samples used in this study: Bill Stanley and Lawrence Heaney (Field Museum of Natural History, Chicago), Masashi Harada (The Osaka City University Medical School), Javier Juste (Estacion Biologica de Donana, Spain), Cassandra Miller-Butterworth (University of Cape Town, South Africa), Teadora Ivanova (National Museum of Natural History, Bulgaria), Norah Cooper and Rick How (Western Australia Museum), Terry Reardon (South

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