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Evolutionary Lineages in Emballonura and Mosia Bats (Mammalia: Microchiroptera) from the Southwestern Pacific1

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Evolutionary Lineages in Emballonura and Mosia Bats (Mammalia: Microchiroptera) from the Southwestern Pacific1 Evolutionary Lineages in Emballonura and Mosia Bats (Mammalia: Microchiroptera) from the Southwestern Pacific1 D. J. Colgan2,3 and S. Soheili2 Abstract: The microchiropteran bat family Emballonuridae is widely distrib- uted in archipelagos of the southwestern Pacific, with especially strong repre- sentation of genera Emballonura and Mosia. DNA sequences from three segments of the mitochondrial genome were collected from four species of Em- ballonura and from M. nigrescens to investigate the relationship of genetic differ- entiation to archipelago biogeography. Specimens of each species formed monophyletic clades in maximum parsimony and Bayesian analyses. Mosia ni- grescens was genetically distant to the other four species. The other four studied species formed a monophyletic clade composed of the pairs E. beccarii, E. serii and E. raffrayana, E. semicaudata. Clades within species were strongly concor- dant with geography, with only two counterexamples (E. semicaudata in Fiji and E. raffrayana in the Solomon Islands) to the general finding that each island’s population of a species constitutes a monophyletic clade. Genetic results do not agree with current subspecific designations within M. nigrescens. Samples from Woodlark, Alcester, and Manus Islands are phylogenetically closer to Papuan mainland samples than to Solomon Islands and New Ireland samples supposedly belonging to the same subspecies. Results suggest that Emballonura can establish populations across wide water barriers but does so infrequently. The isolating effect of water barriers is exemplified by the substantial genetic distinctiveness of Solomon Islands and New Ireland populations of both E. raf- frayana and M. nigrescens. Absence from New Britain of E. beccarii, E. raffrayana, and E. serii (all known from New Ireland) may also reflect effects of water bar- riers if not due to collecting artifacts. Bats are the most widespread of the en- lopex, Macroglossus, Melonycteris, Notopteris, demic mammals of the western Pacific. Na- Nyctimene, Dobsonia, Rousettus, Syconycteris, tive marsupials and rodents are found in the and Mirimiri (Koopman 1984, Nowak 1994, Bismarck Archipelago, but the former do not Flannery 1995a,b, Bonaccorso 1998, Carvajal extend east of this and the latter are not and Adler 2005, Helgen 2005). Five families found beyond the Solomon Islands (Carvajal of Microchiroptera (Emballonuridae, Hippo- and Adler 2005). Ten genera of Megachirop- sideridae, Rhinolophidae, Vespertilionidae, tera are found in the region: Pteropus, Ptera- and Molossidae) have members with ranges extending east of Papua New Guinea (Nowak 1994, Flannery 1995b, Bonaccorso 1 The Winifred Violet Scott Estate and the Australian 1998, Carvajal and Adler 2005). Museum financially supported this research. Manuscript Achieving such wide oceanic distributions accepted 2 July 2007. 2 Research Branch, Australian Museum, 6 College has probably been greatly assisted by flight. Street, Sydney, New South Wales 2010, Australia. Geographic barriers may, however, have dis- 3 Corresponding author: (phone: 612-9320-6030; fax: cernible effects on biogeographic structure 612-9320-6020; e-mail: [email protected]). within species despite this capacity (Heaney 2000). For example, close examination of Pacific Science (2008), vol. 62, no. 2:219–232 phylogenetic lineages in relation to geogra- : 2008 by University of Hawai‘i Press phy often suggests that the present-day dis- All rights reserved tributions of flighted vertebrates within 219 220 PACIFIC SCIENCE . April 2008 archipelagos are substantially influenced by specific phylogeographic structuring in the the extent and persistence of water barriers genus (compared with that observed in Me- between islands (Diamond et al. 1976, Mayr lonycteris). The monospecific genus Mosia and Diamond 2001, Campbell et al. 2004, (species nigrescens) was also included in the Carstens et al. 2004, Heaney et al. 2005, study because specimens were available from Roberts 2006). The effects of water barriers multiple archipelagos. vary between species. Carstens et al. (2004) The family Emballonuridae has approxi- found marked differences in phylogeographic mately 51 species in 13 genera (Simmons patterns in three microchiropteran species 2005). The family is widely distributed in in the family Phyllostomidae in the Lesser tropical and subtropical regions. Nine of the Antilles. Heaney et al. (2005) found that dif- genera are restricted to the Americas, and ferences in species’ ecologies were important four are found in Africa, Asia, and the Pacific in determining how genetic differentiation islands, extending east to Fiji and south to between populations and variation within Australia. Taphozous, Saccolaimus, Emballonura, them respond to a common historical influ- and Mosia are found in the southwestern Pa- ence. cific region. Emballonura itself has 11 species, The existence and persistence of water 10 recorded in Nowak (1994) and the re- barriers has been a principal determinant of cently described E. tiavato (Goodman et al. the systematic status of birds in northern 2006). This species and E. atrata are found Melanesia (Diamond and Mayr 1976, Dia- in Madagascar. The other species occur in mond et al. 1976, Mayr and Diamond 2001). Malaya and eastward. Emballonura beccarii, E. The influence of water barriers on species’ dianae, E. furax, and E. raffrayana are found distributions has also been observed in in New Guinea (Flannery 1995a, Bonaccorso megachiropteran blossom bats (genera Mac- 1998). All of these species except E. furax roglossus, Syconycteris, and Melonycteris) in the occur in the Bismarck Archipelago. The New region (Bonaccorso and McNab 1997). In Ireland fauna also contains E. serii, a species Melonycteris, there is a high correlation of ge- related to E. furax but distinct (Flannery netic divergence and the historical extent of 1994). The New Britain emballonurid fauna water barriers (Pulvers and Colgan 2007). is limited, with only E. dianae and M. nigres- The deepest phylogenetic divergence in the cens being recorded from the island (Bonac- genus, which occurs between populations corso 1998). Emballonura dianae, E. raffrayana, from the Bismarck Archipelago and the Solo- and M. nigrescens have been recorded from mon Islands, coincides with the widest water the Solomon Islands (Sanborn and Beecher barrier within its range. The genetically clos- 1947, Hill 1971, Flannery 1995b). Emballo- est pairs of populations are found on present- nura semicaudata is widely distributed in the day islands that were connected by Pleisto- islands of the western Pacific, ranging from cene land bridges. Belau to Samoa (Koopman 1997). The con- In this investigation we report a study of servation of this species is of particular con- phylogeographic patterns in two genera of cern because there have been dramatic or the microchiropteran family Emballonuridae catastrophic reductions in population num- that was undertaken to allow comparison bers in many parts of its range, including the with the results for Melonycteris and assess Mariana Islands (Lemke 1986), Samoa (Grant the generality of the influence of geographic et al. 1994, Tarburton 2002), and Fiji (Flan- history on bat phylogeography in the western nery 1995b), although it remained quite Pacific. Emballonura was selected for the com- abundant in Belau as late as the mid-1990s parison because it is widely distributed in the (Wiles et al. 1997). region and has broad overlaps in species’ ranges, in contrast to the strict allopatry of materials and methods species found in Melonycteris. The overlaps suggest that at least some of the species have The provenance of the 43 chiropteran sam- strong migratory capabilities, leading to the ples used in this study is indicated in the Ap- hypothesis that there would be reduced intra- pendix and Figure 1. DNA was extracted Evolutionary Lineages in Emballonura . Colgan and Soheili 221 Figure 1. Map of the western Pacific showing sample locations. Localities are indicated by filled circles. Species sampled are specified by the following abbreviations: Emballonura beccarii, Eb; E. raffrayana, Er; E. semicaudata, Esem; E. serii, Es; and Mosia nigrescens, Mn. Names of subspecies of E. semicaudata appear next to island or archipelago names. The inset shows linkages between the various populations of Mosia nigrescens. Lines connect those populations with Kimura 2 parameter average pairwise genetic distances less than 0.06. The two localities in each of Santa Isabel and New Georgia were pooled for this illustration. from these specimens by the CTAB method CytBR: 50-AAACTGCAGCCCCTCA- (Saghai-Maroof et al. 1984). Approximately GAATGATATTTGTCCTCA-3 0 100 mg of tissue was used and the extracted The universal primers of Folmer et al. DNA was resuspended in 200 ml of water. (1994) were used to amplify part of cyto- This stock DNA was diluted as required chrome c oxidase subunit I (COI): (generally 1 in 8) for amplification by the polymerase chain reaction (PCR). 1490F: 50-GGTCAACAAATCATAAA- Mitochondrial cytochrome b (Cytb) and GATATTGG-3 0 and 12S ribosomal RNA (12S rRNA) gene seg- 2198R: 50-TAAACTTCAGGGTGAC- ments were amplified from Emballonura DNA CAAAAAATCA-3 0 by the Kocher et al. (1989) ‘‘universal’’ PCR was performed using 0.5 to 1 unit of primers: BIOTAQ (Bio-Line, London, United King- 12SF: 50-AAAAAGCTTCAAACTGG- dom) DNA polymerase, 0.05 mM dNTPs, 0 GATTAGATACCCCACTAT-3 and 3.5 mM MgCl2, 12.5 pmol of each primer, 12S R: 50-TGACTGCAGAGGGTGA- and 1 ml of diluted DNA in a total reaction CGGGCGGTGTGT-30
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