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The Use of Molecular Phylogenetic and Morphological The Use of Molecular Phylogenetic and Morphological Tools to Identify Cryptic and Paraphyletic Species: Examples from the Diminutive Long-fingered Bats (Chiroptera: Miniopteridae: Miniopterus) on Madagascar Author(s): Steven M. Goodman, Claudette P. Maminirina, Helen M. Bradman, Les Christidis, and Belinda Appleton Source: American Museum Novitates, :1-34. Published By: American Museum of Natural History DOI: http://dx.doi.org/10.1206/652.1 URL: http://www.bioone.org/doi/full/10.1206/652.1 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. 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PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024 Number 3669, 34 pp., 11 figures, 7 tables November 30, 2009 The Use of Molecular Phylogenetic and Morphological Tools to Identify Cryptic and Paraphyletic Species: Examples from the Diminutive Long-fingered Bats (Chiroptera: Miniopteridae: Miniopterus) on Madagascar STEVEN M. GOODMAN,1,2 CLAUDETTE P. MAMINIRINA,2,3 HELEN M. BRADMAN,4 LES CHRISTIDIS,4,5 AND BELINDA APPLETON4 ABSTRACT Based on nearly complete (1125 bp) cytochrome-b sequence data and morphological characters, two new endemic species of Miniopterus are described from Madagascar that were previously identified as M. manavi. Using phylogenetic analysis, the basal nodes of major lineages in the Malagasy members of this genus are weakly supported, while, in most cases, the branches leading to each of the clades are well resolved. Miniopterus mahafaliensis, new species, occurs in the southwestern semidesert areas and M. brachytragos, new species, has a broad distribution across the northern half of the island, ranging across several different biomes. Phylogenetic inference indicates that these two new taxa are not closely related to M. manavi sensu stricto, with average genetic distances of 9.2% and 5.7% from this taxon, respectively. On the basis of this and previous revisions, the former M. manavi complex is now recognized to represent at least five taxa, which do not form a monophyletic group with respect to one another, and represent extraordinary examples of convergent evolution. Miniopterus brachytragos is closely related to the recently named M. 1 Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History; Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605 USA ([email protected] and sgoodman@ vahatra.mg). 2 Vahatra, BP 3972, Antananarivo (101), Madagascar. 3 De´partement de Biologie Animale, Faculte´ des Sciences, Universite´ d’Antananarivo, BP 906, Antananarivo (101), Madagascar ([email protected]). 4 Department of Genetics, The University of Melbourne, Victoria 3010, Australia ([email protected]). 5 Australian Museum, 6 College Street Sydney, NSW 2010, Australia ([email protected]). Copyright E American Museum of Natural History 2009 ISSN 0003-0082 2 AMERICAN MUSEUM NOVITATES NO. 3669 aelleni, while M. mahafaliensis is not closely associated with any of these species. Molecular phylogenetic analysis was imperative to resolve the species limits of these taxa and morphology then provided the means to corroborate the recovered clades. There are localities on the island, specifically limestone karstic zones, where four species of the former M. manavi sensu lato complex occur in strict sympatry. These species often use the same day-roost caves and have similar external and craniodental measurements. This raises intriguing questions as to how these animals divide their worlds with regard to dietary regimes and foraging strategies, as well as their speciation history. INTRODUCTION vealed considerable fixed genetic differences and, as of September 2008, at least 19 species With the advent of molecular phylogenetic are proposed that are phenotypically similar techniques, nearly two decades ago, new to one another (Rasoloarison et al., 2000; means became available to classify groups of Kappeler et al., 2005; Andriantompohavana et animals that are morphologically similar to al., 2006; Louis et al., 2006, 2008; Olivieri et one another, but sufficiently genetically dis- al., 2007; Radespiel et al., 2008). tinct to be considered separate species (Yoder Herein, we explore the species limits of et al., 2005; Bickford et al., 2006; Pfenninger another group of Malagasy vertebrates, long- and Schwenk, 2007). This research reveals fingered bats, genus Miniopterus Bonaparte, cases of phylogenetic sister species possessing 1837, of the family Miniopteridae (Hoofer and morphological traits that are so similar that Van Den Bussche, 2003; Miller-Butterworth et they cannot be easily differentiated from one al., 2007). This genus contains a considerable another, and hence are referred to as cryptic number of cryptic species across their Old species. In such examples, the phenotypic World distribution (Cardinal and Christidis, characters used in taxonomic classification 2000; Appleton et al., 2004; Stoffberg et al., do not reflect the same level of differentiation 2004; Miller-Butterworth et al., 2005; Juste et as the genetic markers (Baker and Bradley, al., 2007). Peterson et al. (1995) recognized 2006). Further, there are numerous cases four taxa from Madagascar, two of which among mammals, where phenotypically simi- also occurred on the Comoros (M. manavi lar species do not form monophyletic units Thomas, 1906 and M. majori Thomas, 1906), and represent examples of morphological one shared with Africa (M. fraterculus convergence and paraphyly (e.g., Pizzimenti, Thomas and Schwann, 1906), and the fourth 1976; Ruedi and Mayer, 2001; Funk and endemic to the island (M. gleni Peterson et al., Omland, 2003; Gaubert and Veron, 2003). 1995). Recent molecular genetic and morpho- Over the past few years numerous cryptic logical studies have considerably changed this species have been described from around the view, with M. manavi and M. gleni being world and across different biological groups paraphyletic and the Malagasy animals for- (Pfenninger and Schwenk, 2007); Madagascar merly assigned to M. fraterculus representing has produced a remarkable number of exam- two endemic species (Goodman et al., 2007, ples from the animal kingdom including, ants, 2008, 2009a, 2009b; Weyeneth et al., 2008). beetles, amphibians, reptiles, bats, and terres- Among the original four species recognized by trial mammals (e.g., Olson et al., 2004; Vences Peterson et al. (1995), only M. majori shows and Glaw, 2005; Monaghan et al., 2005; Smith no notable genetic variation, based on cur- et al., 2005; Yoder et al., 2005; Goodman et rently available samples, and is not a compos- al., 2007). Perhaps one of the more remarkable ite species (Mamanirina et al., 2009). examples of cryptic animal species is among Malagasy miniopterines show numerous cases lemurs, arguably the best-known group of of morphological similarity, with genetic land vertebrates on the island. The mouse- results demonstrating that certain non-sister- lemurs of the genus Microcebus were thought taxa display convergence in size and body to comprise a single broadly distributed morphology. The subject of this current paper species, until Martin (1972) recommended is to further investigate other previously that a second form should be recognized. unrecognized clades among Malagasy Subsequently, largely molecular studies re- Miniopterus formerly identified as M. manavi, 2009 GOODMAN ET AL.: TWO NEW MINIOPTERUS FROM MADAGASCAR 3 and to describe an additional two species that across zygomatic arches at the widest point; are genetically and morphologically distinct. postorbital breadth (POB), dorsal width at most constricted part of skull; mastoid MATERIAL AND METHODS breadth (MAST), maximum width of skull across mastoid processes; greatest braincase Morphological Comparisons width (GBW), breadth at widest portion of braincase; lachrymal width (LW), greatest In order to resolve the taxonomic identity of different small Miniopterus from Madagascar, width across lachrymal swellings; palatal that have been classically placed within the M. length (PAL), from anterior edge of upper manavi species group, specimens were exam- incisors to posterior edge of palatal with- ined from several different natural history out posterior spike; and mandible length museums: BMNH, the Natural History (MAND), from the posteriormost portion of Museum, London (formerly British Museum the condyles to anteriormost alveoli of lower [Natural History]); FMNH, Field Museum of incisors. The dental measurements include: Natural History, Chicago; MNHN, Muse´um cranial toothrow (I1–M3), length from ante- National d’Histoire Naturelle, Paris; ROM rior alveolar border of incisors to
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