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Morphometric Differentiation Among Haplochromine Cichlid Fish Species

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Morphometric Differentiation Among Haplochromine Cichlid Fish Species Accepted on 30 July 2010 Ó 2011 Blackwell Verlag GmbH J Zool Syst Evol Res doi: 10.1111/j.1439-0469.2011.00624.x 1Department of Zoology, University of Graz, Universita¨tsplatz 2, Graz, Austria; 2National Museums of Kenya, Ichthyology Section, Nairobi, Kenya Morphometric differentiation among haplochromine cichlid fish species of a satellite lake of Lake Victoria Elizabeth A. Odhiambo1,2,Michaela Kerschbaumer1,Lisbeth Postl1 and Christian Sturmbauer1 Abstract Lake Victoria holds a young but species-rich assemblage of cichlid fishes, which form a monophyletic assemblage with additional species from surrounding water bodies, termed the Lake Victoria superflock. Lake Victoria is surrounded by smaller lakes that are somewhat disconnected from the main lake. Lake Kanyaboli is such a small lake, having markedly reduced species diversity, in part comprised of Lake Victoria species and endemics. Here, we studied the modern haplochromine component of the cichlid fauna, represented by Lipochromis maxillaris, Astatotilapia nubila, Xystichromis phytophagus and Astatotilapia sp. ÔBigeyeÕ, as well as a number of unidentified modern haplochromine specimens. We used landmark-based geometric morphometrics to study the degree of morphological divergence among those young entities. Twenty landmarks and 14 interlandmark distances were used for shape analysis. Multivariate analysis revealed significant differences between all four species, but principal component analysis and canonical variate analysis did not clearly discriminate between A. nubila and X. phytophagus, demonstrating great overall morphological similarity despite clear dietary differences. Besides coloration there was sexual dimorphism in body proportions, so that only male individuals were analysed further. In all four species, the observed similarities and differences in body shape conform to the type of ecological specialization of the fish. Most unidentified specimens overlapped the range of A. nubila and X. phytophagus, while the assignment test based on the canonical variate analysis suggested 70% of the three overlapping entities as separate units. To test their reproductive distinctness and to demonstrate potential hybridization, nuclear genetic data are needed. Key words: Lake Victoria – Lake Kanyaboli – landmark analysis – interlandmark distances – Eastern Africa Introduction Lake Victoria must have been truly explosive (Seehausen With an estimated geological age of 250 000–750 000 years 2000). (Temple 1969; Johnson et al. 2000), Lake Victoria is not only Whereas the cichlids of older lakes like Lake Tanganyika are the largest and shallowest, but is also the youngest of the great morphologically, genetically and ecologically more distinct, lakes of Eastern Africa. The cichlids of this lake are renowned the haplochromine cichlids of Lake Victoria are highly similar for their adaptive radiation and explosive speciation (Fryer morphologically (Greenwood 1979, 1980; Meyer et al. 1990; and Iles 1972; Kaufman et al. 1997; Kocher 2004). Various Verheyen et al. 2003) and offer the most complex taxonomic causes have been discussed to be the driving forces behind this puzzle (Van Oijen 1982, 1991; Seehausen 1996; Van Oijen and rapid speciation, e.g. sensory drive in cichlid fish (Seehausen Witte 1996; Seehausen et al. 2003a,b), both at the generic and et al. 2008), sympatric speciation by disruptive sexual selection at the species level (Barel et al. 1991; Booton et al. 1999). (Seehausen and van Alphen 1999), heritability and hetero- Greenwood already highlighted the narrow clustering around chrony of polychromatism (Maan et al. 2005), selection on the modal form, the presence of all intergrades within coloration and male–male competition (Carleton et al. 2005; morphoclines of ÔspeciesÕ (Greenwood 1974, 1981), which Dijkstra et al. 2006, 2008; Maan et al. 2006 and Maan et al. was later confirmed by biochemical and molecular phyloge- 2008, Seehausen and Schluter 2004) or sex reversal (Lande netic studies (Meyer et al. 1990; Nagl et al. 2000), altogether et al. 2001). Concerning the time scale of this adaptive supporting that the Lake Victoria haplochromines are at an radiation, the remarkably diverse species flock was suggested early stage of radiation. Additional human-induced problems to have evolved in situ in less than 200 000 years (Meyer et al. need to be considered: the dramatic decline of the haplochro- 1990; Verheyen et al. 2003; Genner et al. 2007). Considering mine cichlids in the lake in the 1980s as a result of the the findings of Johnson et al. (1996) who revealed that the lake introduction of the Nile perch and frequent blooms of blue- dried out (almost) completely during the late pleistocene about green algae because of deforestation and overfertilization 12,400 14C-years ago, the cichlid fauna in Lake Victoria might (Witte et al. 1992, 2005; Seehausen et al. 2003a,b). Natural have even evolved and radiated within this remarkably short hybridization because of turbid water conditions (Seehausen period of time (Seehausen 2002). While the actual age of the et al. 2003a,b) complicate taxonomic classification (Witte et al. flock is currently disputed (Fryer 1997, 2001, 2004; Nagl et al. 2007). 2000; Verheyen et al. 2003; Elmer et al. 2009), it is clear that Haplochromine cichlids exhibit sexual dimorphism, with irrespective whether some endemic cichlid species survived the females usually exhibiting a totally different colour from that drought inside or outside the lake basin, cichlid speciation in of males, because they are usually camouflaged as a conse- quence of their breeding mode as mouthbrooders. So while live body coloration, especially that of adult males, is an important Corresponding author: Christian Sturmbauer (christian.sturmbauer@ diagnostic character (at least for preliminary field identifica- uni-graz.at) Contributing authors: Elizabeth A. Odhiambo ([email protected]), tion), it can mostly be applied only on live male specimens, Michaela Kerschbaumer ([email protected]), which may also lose their colour in response to stress, bright Lisbeth Postl ([email protected]) light, emotional state of the fish (Conte 2004) and after J Zool Syst Evol Res (2011) 49(3), 216–223 Morphometric differentiation among haplochromine cichlid fish species 217 preservation. DNA sequences as tools for bar coding proved alluaudi Pellegrin, 1904; Pseudocrenilabrus multicolor victoriae inefficient because of the stage of incomplete lineage sorting, Seegers, 1990; Astatotilapia nubila Boulenger, 1906; Xystichr- because several species share haplotypes or alleles (Nagl et al. omis phytophagus Greenwood, 1966; Lipochromis maxillaris 1998, 2000). All these factors led to the quest for an objective, Trewavas, 1928, a rare and undescribed species – Astatotilapia reliable and repeatable procedure for quantifying morpholog- sp. ÔBigeyeÕ and possibly more undescribed entities. Of these, ical differences and discriminating between different species. Astatoreochromis alluaudi and Pseudocrenilabrus multicolor The classic works solely applied traditional morphometrics victoriae represent ancient splits within the haplochromines. (TM) in their morphological analyses, mainly involving linear The remaining species are part of the ÔmodernÕ haplochromine measurements (trusses) or angles from different points on the species superflock (Salzburger et al. 2005), which are part of body (Barel et al. 1977; Snoeks 1994), and proved to be only the c-lineage sensu Clabaut et al. (2005). partially able to characterize and distinguish species. To Using landmark analysis in combination with interlandmark overcome these problems, geometric morphometrics (GM) distances (ILD) generated from the landmarks, the study was applied in more recent works (Kassam et al. 2002, 2003; attempts to test the degree of morphological distinction among Costa et al. 2006) and turned out to be a powerful tool for the four recognized species of modern haplochromines in Lake addressing shape differences, even in preserved specimens. Kanyaboli and to analyse the assignment of about 90 Further, GM remains compatible with and complementary to unidentified specimens which could not be assigned to either modern statistical analyses (Adams et al. 2004) and provides a of the recognized entities. The fit to nuclear genetic markers is unique opportunity to visualize the distinctive body regions a long-term goal of this approach and will be addressed in a using thin plate splines and deformation grids – a fact which forthcoming work. greatly enhances interpretation of results with respect to the ecological significance of the observed differences (Bookstein 1991). Material and Methods While many of the Lake Victoria haplochromine species Sample collection and data acquisition have been classified based mainly on coloration of mature Between May 2007 and April 2008, samples were collected from 33 males, little effort has been put on establishing the shape localities covering the entire lake (approximately 11 km2) using gill differences between the species, so that quantifiable differences nets, traps and baited hooks. In total, 145 (139 males, six females) in shape are not known to date. This study is one of the first to individuals were sampled of Astatotilapia nubila, 174 (136 males, 38 apply GM on Lake Victoria cichlids (but see, Fermon and females) of Lipochromis maxillaris, 191 (131 males, 60 females) of Xystichromis phytophagus and three (one male, two females) individ- Cibert 1998). We selected the relatively simple species com- uals of the rare
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