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Allopatric Differentiation in the Marcusenius Macrolepidotus Species Complex in Southern and Eastern Africa: the Resurrection of M

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Allopatric Differentiation in the Marcusenius Macrolepidotus Species Complex in Southern and Eastern Africa: the Resurrection of M Journal of Natural History, 2007; 41(9–12): 647–708 Allopatric differentiation in the Marcusenius macrolepidotus species complex in southern and eastern Africa: the resurrection of M. pongolensis and M. angolensis, and the description of two new species (Mormyridae, Teleostei) BERND KRAMER1, PAUL SKELTON2, HERMAN VAN DER BANK3 & MICHAEL WINK4 1University of Regensburg, Zoological Institute, Universita¨tsstrabe 31, D-93040 Regensburg, Germany, 2South African Institute for Aquatic Biodiversity, Private Bag 1015, Grahamstown 6140, South Africa, 3University of Johannesburg, Department of Zoology, Kingsway Campus, PO Box 524, Auckland Park, 2006, South Africa, and 4Heidelberg University, Institute of Pharmacy and Molecular Biotechnology, Im Neuenheimer Feld 364, D-69120 Heidelberg, Germany (Accepted 18 January 2007) Abstract We critically compared local populations of the bulldog fish, Marcusenius macrolepidotus (Peters 1852), from different watersheds, from the furthest south (28u South, South Africa) to the Equator in Kenya. We ascertained allopatric differentiation from topotypical M. macrolepidotus from the Lower Zambezi River (Mozambique) in morphology, electric organ discharges, and molecular genetics for: (1) samples from the Okavango and Upper Zambezi Systems (Botswana and Namibia), (2) samples from South Africa’s rivers draining into the Indian Ocean, and (3) samples from the East African Tana River (Kenya). Significant genetic distances in the mitochondrial cytochrome b gene and differing ISSR-PCR profiles corroborate differentiation between the four taxa. We resurrect M. pongolensis (Fowler, 1934) for South Africa (sample 2), and M. angolensis (Boulenger, 1905) for the Quanza River/Angola. We recognize M. altisambesi sp. n. for the Upper Zambezi/Okavango specimens (sample 1), and M. devosi sp. n. for those from Kenya (sample 3). Keywords: Teleostei, Mormyridae, Marcusenius, systematics, morphometrics, electric organ discharges, molecular genetics, southern Africa Introduction Marcusenius Gill, 1862 is the largest genus of the Mormyridae, comprising 33 species in the catalogue of fishes (Eschmeyer 2006), distributed throughout tropical central, western, eastern, and north-eastern Africa (Nile System). In southern Africa only a single species, M. macrolepidotus (Peters, 1852), has been recognized, known commonly as the bulldog Correspondence: Bernd Kramer, Zoological Institute, University of Regensburg, Universita¨tsstrabe 31, D-93040 Regensburg, Germany. Fax: +49 (0) 941-943 2905. Email: [email protected] ISSN 0022-2933 print/ISSN 1464-5262 online # 2007 Taylor & Francis DOI: 10.1080/00222930701250987 648 B. Kramer et al. fish, a name which refers to this fish’s well-developed mental lobe on the lower jaw that is also present in other Marcusenius species (Figure 1). Marcusenius macrolepidotus ranges widely in southern and East Africa, occurring in most rivers of East Africa from the equatorial Tana River in Kenya southwards (Seegers 1996, p. 76) to the Mhlatuze River in South Africa’s KwaZulu-Natal province (almost 29u S; Skelton 1993, 2001). It also occurs in the Upper Zaire (Congo River), and is widespread and common in the western Cunene, Okavango and Upper Zambezi Systems. Figure 1. All species and forms of the Marcusenius macrolepidotus species complex, as studied in the present paper. (A) M. macrolepidotus (Peters, 1852), ZMB 3678 (lectotype L. Seegers; photo: L. Seegers). (B) Gnathonemus angolensis Boulenger 1905, BMNH 1905.5.29.64 (holotype). (C) Gnathonemus moeruensis Boulenger 1915, MRAC 14137 (holotype). (D) Gnathonemus pongolensis Fowler 1934, ANSP 54950 (holotype). (E) M. macrolepidotus (Peters 1852), SAIAB 060847, coll. R. Bills 1 Aug.1999, Lower Zambezi. (F) M. macrolepidotus (Peters 1852), SAIAB 060947, coll. R. Bills 15 Aug.1999, lower Pungwe River System. (G) M. devosi sp. n., coll. L. de Vos and B. Kramer 3/6 Sept. 2001, Lower Tana River/Kenya. (H) M. macrolepidotus (Peters, 1852), SAIAB 73790 (largest specimen), coll. R. Bills 14 Aug. 2003, Rovuma System. (I) M. macrolepidotus (Peters 1852), SAIAB 055874, coll. R. Bills 20 July 1997, Mulela River/Mozambique. (J) M. altisambesi sp. n., coll. F.H. van der Bank and B. Kramer, 11/12 August 2004, Okavango River, live fish of SL 13 cm photographed 20 April 2006. (K) M. altisambesi sp. nov, coll. F. H. van der Bank and B. Kramer, 21 August 1999, Upper Zambezi, Kalimbeza, live specimen of 16.5 cm SL photographed 3 July 2003. (L) M. macrolepidotus (Peters 1852), sampled together with SAIAB 67369, coll. R. Bills 29 Sept. 2002, Buzi River System, specimen of 13 cm SL photographed alive 22 February 2005. (M) M. pongolensis (Fowler, 1934), resurrected species, specimen of 11 cm SL reared in captivity from parents caught in Crocodile River, Incomati System, in February 1997, photographed alive 15 March 2005. Marcusenius species complex in southern Africa 649 As in many other fish of wide southern and even east African distribution, a critical comparison of allopatric populations has not been made, with the notable exceptions of the large-scaled Marcusenius species of west-central and central Africa by Boden et al. (1998), none of which occur in the area we were able to visit, and Malawi Marcusenius species (Tweddle and Willoughby 1982). While conducting an analysis of electric organ discharges (EODs) on mormyrids from southern Africa, usually regarded as Marcusenius macro- lepidotus, specimens from the Incomati System (South Africa) emitted distinctly different EODs compared to bulldogs from the Upper Zambezi in Namibia (for Upper Zambezi bulldogs, see Kramer 1997a, 1997b). Bulldogs from other southern African and East African origins revealed still more differentiation on which we report here. DNA markers, such as sequences of mitochondrial DNA (especially cytochrome b) have been widely employed to reconstruct the molecular phylogeny of some members of the Mormyridae in comparison to their corresponding morphology and electrophysiology (Alves-Gomes and Hopkins 1997; Sullivan et al. 2000, 2002; Lavoue´ et al. 2000; Lavoue´ and Sullivan 2004, Kramer et al. 2003, 2004). We have chosen the cyt b gene to reconstruct the phylogeny of the M. macrolepidotus complex. Since mtDNA is inherited maternally, hybridizations can distort the mtDNA phylogeny. In order to corroborate the findings from cyt b analysis we therefore used genomic fingerprinting with ISSR-PCR to analyse variation in the nuclear genome. The ISSR (Inter-simple-sequence-repeat) method has recently been added to the growing list of molecular tools. ISSR analysis is useful for testing genomic instability (Leroy et al. 2000), genetic diversity (Kantety et al. 1995), cultivar identification (Charters et al. 1996), molecular mapping (Ratnaparkhe et al. 1998), in forensic DNA profiling (Kumar et al. 2001) in plants, as well as for sexing in birds (Wink et al. 1998), or detecting hybrids in birds and reptiles (Wink et al. 2000). This PCR-based method uses primers annealing to microsatellite repeats to amplify the regions between adjacent, inversely orientated SSRs, provided they are close enough to allow exponential multiplication. The method targets inversions, insertions, deletions, and mutational events of microsatellites at multiple loci in the genome. Individuals of the same species usually show few to no differences between their ISSR patterns, whereas closely related taxa, such as subspecies and species, give a specific banding profile that can be used to study phylogenetic questions. EODs are a communication signal in mormyrid fishes that are also used for active location of objects (for reviews, see Kramer 1990, 1996; Bastian 1994; Moller 1995; Hopkins 1999). EODs play a key role in pair formation, mating, and social attraction in the bulldog fish (Werneyer and Kramer 2002, 2005; Hanika and Kramer 2005). EODs of sympatric mormyrids of the Upper Zambezi are species-specific (Kramer 1996) and have been used for phylogenetic analysis (Van der Bank and Kramer 1996; Kramer and Van der Bank 2000; Kramer et al. 2003, 2004). In addition to anatomical and genetic data, we utilize EOD as a taxonomic tool for analysing some of the populations forming a complex of allopatric species for M. macrolepidotus in southern and East Africa. Material and methods Electrical and morphological studies A total of 414 specimens was examined and at least 15 measurements (see Figure 2) and at least three meristic characters taken. The following abbreviations were used: PDL, predorsal length: distance tip of snout (excluding mental lobe or chin) to dorsal fin origin. PAL, distance 650 B. Kramer et al. Figure 2. Morphological measures used in the present study. For explanation of abbreviations, see Material and methods. tip of snout to anal fin origin. LD, dorsal fin length. LA, anal fin length. pD, distance dorsal fin origin to end of caudal peduncle. CPL, length of caudal peduncle (end of anal fin base to midbase caudal fin). CPD, depth of caudal peduncle: the least vertical distance across the Marcusenius species complex in southern Africa 651 caudal peduncle. LS, length of snout: distance tip of snout to posterior orbital rim of eye (LSo), centre of eye (LSc). HL, head length: distance tip of the snout to furthest bony edge of the operculum. Na, distance between the pair of nares of one side (from centre to centre). ED, eye diameter: defined by orbital rims. LPF, length of pectoral fins. SL, standard length: distance tip of snout to midbase caudal fin. BD, body depth: the greatest vertical distance across
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