Journal of Mammalogy

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Journal of Mammalogy 86(6):1121-1135. 2005
doi: 10.1644/05-MAMM-A-021R1.1

GENETIC AND PHENOTYPIC DIFFERENCES BETWEEN SOUTH AFRICAN LONG-FINGERED BATS, WITH A GLOBAL MINIOPTERINE PHYLOGENY

Cassandra M. Miller-Butterworth*abd, Geeta Eickace, David S. Jacobsab, M. Corrie Schoemanab, and Eric H. Harleyab

aDepartment of Zoology, University of Cape Town, Private Bag, Rondebosch, 7701, South Africa (CMM-B, DSJ, MCS)

bDivision of Chemical Pathology, University of Cape Town Medical School, Observatory, 7925, South Africa (CMM-B, EHH)

cEvolutionary Genomics Group, Department of Botany and Zoology, University of Stellenbosch, Private Bag X1, Matieland, Stellenbosch, 7602, South Africa (GE)

dPresent address of CMM-B: Department of Human Genetics, University of Pittsburgh, 130 DeSoto Street, Pittsburgh, PA 15261, USA

ePresent address of GE: TMP202, Department of Surgery, Yale Medical School, 333 Cedar Street, New Haven, CT 06520, USA

*Correspondent:

Abstract

The Natal long-fingered bat (Miniopterus natalensis) and lesser long-fingered bat (M. fraterculus) are morphologically almost indistinguishable and occur sympatrically over much of their southern African range. This raises the possibility that they are sister taxa. We employed a multidisciplinary approach to examine their taxonomic relationship to one another and to other Miniopterus species, whose global phylogeny requires review. We examined echolocation, morphological, and dietary differences between M. natalensis and M. fraterculus, as well as both nuclear and mitochondrial DNA variation between them in the context of a phylogeny incorporating 13 Miniopterus species and subspecies. Despite similarities in their morphology and distribution, M. natalensis and M. fraterculus echolocate at peak frequencies separated by 12 kHz, and both nuclear and mitochondrial DNA markers confirm they are distinct species. Analysis of cytochrome-b (Cytb) sequences further indicates that M. fraterculus and M. natalensis are not sister taxa; M. fraterculus appears to be more closely related to the greater long-fingered bat (M. inflatus). Examination of the global taxonomy of Miniopterus confirms that Schreibers's long-fingered bat (M. schreibersii) forms a paraphyletic species complex. Furthermore, the miniopterine bats are divided into 2 geographically isolated monophyletic groups, one containing African and European species, and the other taxa from Australasia and Asia. Cytb sequence divergence also suggests that M. natalensis is distinct from the European M. schreibersii. These results support the elevation of M. natalensis to full species rank.

submittedJanuary 21, 2004; Accepted: April 4, 2005

Keywords: Chiroptera, cytochrome b, echolocation, microsatellite, Miniopterus, morphology, phylogeny



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Appendix I






Specimens examined

The following are listed for each species included in this study: collection locality, source of material, the number of samples included in the microsatellite (M) and cytochrome b (Cytb) components, and, where applicable, identification of Cytb haplotypes (A–H) and institution or GenBank accession number of samples used for Cytb sequencing. Geographic locations of South African collection localities (sites 1–12) are shown in Fig. 1. Specimens for which vouchers were taken are indicated by an asterisk (*). DSJ indicates specimen was contributed by D. S. Jacobs. GenBank accession numbers for microsatellite primer sequences of Miniopterus are AY056588–AY056592, and for the Cytb sequences generated in this study are AY614732–AY614755 and AY675219–AY675220.



Miniopterus natalensis

SOUTH AFRICA: Steenkampskraal (31°36′S, 18°45′E; site 1), DSJ (M: n = 20 [*2 voucher specimens], Cytb: n = 1), E, SKKF1; Die Hel (33°05′S, 19°05′E; site 3), DSJ (M: n = 19, Cytb: n = 1), F, DHLM12; De Hoop Nature Reserve (34°25′S, 20°21′E; site 4), DSJ (M: n = 40, Cytb: n = 1), H, DHPF1; Knysna (33°53′S, 22°59′E; site 5), DSJ (M: n = 2, Cytb: n = 2), D, G, DSJ147, DSJ197; Grahamstown (33°17′S, 26°31′E; site 6), DSJ (M: n = 37, Cytb: n = 1), A, GF6; Maitland Mines (33°59′S, 25°17′E; site 7), DSJ (M: n = 37, Cytb: n = 0); Shongweni Dam (29°52′S, 30°43′E; site 8), DSJ (M: n = 29, Cytb: n = 1), C, SHDF1, and W. White and K. Richardson (M: n = 0, Cytb: n = 3), A and D, M4, M5, and M17; Jozini Dam (27°25′S, 32°04′E; site 9), DSJ (M: n = 28, Cytb: n = 0); Pongola River Bridge (27°01′S, 32°16′E; site 9), Durban Natural Science Museum, South Africa (M: n = 5*, Cytb: n = 0); Sudwala (25°22′S, 30°42′E; site 10), DSJ (M: n = 1, Cytb: n = 1), B, SWF1; Peppercorn Cave (24°08′S, 29°12′E; site 11), DSJ (M: n = 19, Cytb: n = 0); Koegelbeen (28°39′S, 23°20′E; site 12), DSJ (M: n = 40, Cytb: n = 1), E, KBF1.



Miniopterus fraterculus

SOUTH AFRICA: Die Hel (site 3), DSJ (M: n = 1, Cytb: n = 0); Knysna (site 5), DSJ (M: n = 0, Cytb: n = 5), A, B, and C, DSJ179, DSJ193, DSJ183*, DSJ80, DSJ182*; Maitland Mines (site 7), DSJ (M: n = 3, Cytb: n = 1), A, MMM17; Shongweni Dam (site 8), Durban Natural Science Museum, South Africa (M: n = 1, Cytb: n = 1), A, DM6213*, and W. White and K. Richardson (M: n = 0, Cytb: n = 1), A, M19; Sudwala (site 10), DSJ (M: n = 8, Cytb: n = 2), D and E, SWF11 and SWF17; Peppercorn Cave (site 11), DSJ (M: n = 1, Cytb: n = 1), F, PCM2.



Miniopterus (species unknown)

ZAMBIA: Leopard Hill Cave, Lusaka (15°36′S, 28°43′E), DSJ (M: n = 0, Cytb: n = 2), A and B, DSJZM1*, DSJZM4*.



Miniopterus australis

VANATU: Australian Museum, Australia (M: n = 0, Cytb: n = 1), M28191.



Miniopterus inflatus

MALAWI: Likabula Mission, Mulanje Mountain, Northern Flagship Institute, South Africa (M: n = 0, Cytb: n = 1), TM41802.



Miniopterus macrocneme

PAPUA NEW GUINEA: Australian Museum, Australia (M: n = 0, Cytb: n = 1), M19552.



Miniopterus manavi

MADAGASCAR: Ankarana, James Hutcheon (M: n = 0, Cytb: n = 1), A, JMH141; Ranomafana, James Hutcheon (M: n = 0, Cytb: n = 1), B, JMH029.



Miniopterus schreibersii

SPAIN: Ruedi and Mayer (2001), (M: n = 0, Cytb: n = 1), AF376830; JAPAN: L. Tian (M: n = 0, Cytb: n = 1), GI37783851; CHINA: L Tian (M: n = 0, Cytb: n = 1), GI37783847.



M. s. bassanii

AUSTRALIA: Naracoorte, Belinda Appleton (M: n = 0, Cytb: n = 1), NA-1.



M. s. fuliginosus

JAPAN: Kashiwazaki, Niigata Pref., Sakai et al (2003), (M: n = 0, Cytb: n = 1), AB085735.



M. s. orianae

AUSTRALIA: Kakadu, Belinda Appleton (M: n = 0, Cytb: n = 1), M24153.



M. s. pallidus

ISRAEL: Alma Cave, N. Galilee, Benny Shalmon (M: n = 0, Cytb: n = 1), Alma1.



Cistugo lesueuri

SOUTH AFRICA: Algeria Forestry Station (32°22′S, 19°03′E; site 2); DSJ (M: n = 0, Cytb: n = 1), 8.10.02Ml1(A).



Cynomops paranus

GUYANA: Potaro-Siparuni, Royal Ontario Museum, Canada (M: n = 0, Cytb: n = 1), ROM108466.

Fig. 1.—Known distribution ranges of Miniopterus natalensis, M. fraterculus, and M. inflatus in southern Africa (modified from Taylor [2000] to include our sampling localities). Sites in South Africa at which samples were collected are numbered as follows: 1, Steenkampskraal; 2, Algeria Forestry Station; 3, Die Hel; 4, De Hoop Nature Reserve; 5, Knysna; 6, Grahamstown; 7, Maitland Mines; 8, Shongweni Dam; 9, Jozini Dam and Pongola River bridge; 10, Sudwala; 11, Peppercorn Cave; 12, Koegelbeen. Geographic locations and details of which species were collected at each locality are given in Appendix I

Fig. 2.—Results of an assignment test for Miniopterus natalensis and M. fraterculus, based on microsatellite allele frequencies. The negative log likelihood of each individual belonging to its own species is plotted against the negative log likelihood of it belonging to the other species. The clouds of data points for each species are clearly separated and fall predominantly above or below the diagonal (along which an individual is equally likely to belong to either species)

Fig. 3.—Allele frequency distributions for 6 microsatellite loci genotyped in 309 Miniopterus natalensis and 14 M. fraterculus. Loci Mschreib1–Mschreib5 were designed specifically for M. natalensis (Miller-Butterworth et al. 2002); NCAM is a general mammalian microsatellite locus located in the gene for the neural cell adhesion molecule (Moore et al. 1998)

Fig. 4.—Unrooted neighbor-joining tree generated from microsatellite allele frequencies for Miniopterus natalensis and M. fraterculus, using the modified Cavalli–Sforza distance (Da—Nei et al. 1983). Bootstrap values (1,000 replicates) above 50% are given on the branches. Branch lengths are proportional to the genetic distance indicated by the scale bar. Source localities of individuals from both species are shown (site numbers from Fig. 1 are in parentheses after locality names), as are the 3 South African subpopulations previously identified for M. natalensis (Miller-Butterworth et al. 2003)

Fig. 5.—Single tree recovered from maximum-likelihood analysis of cytochrome-b sequences (lnL = −2,843.02). Nodes that received 100% support from all 4 methods of analysis (parsimony, minimum evolution, Bayesian analysis, and maximum likelihood) are indicated by an asterisk (*). Nodal support values for clades that received support ≥50% from at least 3 of the 4 methods of analyses are provided. Branch lengths are proportional to the number of nucleotide substitutions per site as indicated by the scale bar. Institutional or GenBank accession numbers of specimens included in this analysis are given in Appendix I

Fig. 6.—Power spectra and spectrograms for search-phase echolocation calls of Miniopterus natalensis (left) and M. fraterculus (right). Call durations are 7.8 ms and 5.8 ms, respectively. Call intensity is measured in reference to the average threshold for human hearing, which is set at zero. Calls were recorded from hand-released bats (to ensure specific identity was known) and were selected as typical search-phase calls of good quality, with high signal to noise ratio. They were chosen toward the end of the sequence to ensure they represent search-phase calls

table

Table 1.—Average cytochrome-b sequence divergences between species or subspecies of Miniopterus and outgroups. Where available, average intraspecific distances are given in bold text on the diagonal. Source localities of specimens are given in Appendix I

table

Table 2.—Approximate unbiased (AU) P values for the best maximum-likelihood tree and alternative a priori and a posteriori phylogenetic hypotheses. Asterisk(*) indicates significance at P < 0.05

table

Table 3.—Comparison between Miniopterus natalensis and M. fraterculus for morphological, echolocation, and dietary variables for bats captured in Knysna Forest, South Africa (Fig. 1, site 5)

table

Table 4.—The results of discriminant function analysis on morphological parameters for Miniopterus natalensis and M. fraterculus captured in Knysna Forest, South Africa (Fig. 1, site 5)

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