Species-Specific Population Structure in Rock-Specialized
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J Mol Evol (2007) 64:33–49 DOI: 10.1007/s00239-006-0011-4 Species-Specific Population Structure in Rock-Specialized Sympatric Cichlid Species in Lake Tanganyika, East Africa Kristina M. Sefc,1 Sanja Baric,2 Walter Salzburger,3* Christian Sturmbauer1 1 Department of Zoology, Karl Franzens University of Graz, Universita¨ tsplatz 2, A-8010 Graz, Austria 2 Research Centre for Agriculture and Forestry Laimburg, Laimburg 6, I-39040 Auer/Ora (BZ), Italy 3 Lehrstuhl fu¨ r Zoologie und Evolutionsbiologie, Department of Biology, and Center for Junior Research Fellows, University of Konstanz, Universita¨ tsstrasse 10, 78457 Konstanz, Germany Received: 18 January 2006 / Accepted: 16 October 2006 [Reviewing Editor: Dr. Rafael Zardoya] Abstract. Species richness and geographical pheno- stenotopic Lake Tanganyika species. The amount of typic variation in East African lacustrine cichlids are genetic differentiation among populations was not re- often correlated with ecological specializations and lated to the degree of geographical variation of body limited dispersal. This study compares mitochondrial color, especially since more phenotypic variation is and microsatellite genetic diversity and structure observed in O. ventralis than in the genetically highly among three sympatric rock-dwelling cichlids of Lake structured E. cyanostictus. Tanganyika, Eretmodus cyanostictus, Tropheus moorii, and Ophthalmotilapia ventralis. The species represent Key words: Genetic differentiation — Population three endemic, phylogenetically distinct tribes (Eret- expansion — Isolation by distance — Philopatry — modini, Tropheini, and Ectodini), and display diver- Habitat heterogeneity — Geographic color variation gent ecomorphological and behavioral specialization. Sample locations span both continuous, rocky shore- line and a potential dispersal barrier in the form of a muddy bay. High genetic diversity and population differentiation were detected in T. moorii and E. cya- Introduction nostictus, whereas much lower variation and structure were found in O. ventralis. In particular, while a 7-km- The origin of biological diversity is of profound wide muddy bay curtails dispersal in all three species to interest to evolutionary biologists, not least because a similar extent, gene flow along mostly continuous the amount of variation is distributed unevenly across habitat appeared to be controlled by distance in E. groups of organisms. Cichlid fish of the East African cyanostictus, further restricted by site philopatry and/ Great Lakes, for example, range among the most or minor habitat discontinuities in T. moorii, and diverse species flocks in vertebrates (Fryer 1959; unrestrained in O. ventralis. In contrast to the general Fryer and Iles 1972; Dominey 1984; Sturmbauer pattern of high gene flow along continuous shorelines 1998; Kocher 2004; Salzburger and Meyer 2004). The in rock-dwelling cichlids of Lake Malawi, our study lacustrine radiations of cichlids in Lakes Malawi, identifies differences in population structure among Victoria, Tanganyika, and several smaller lakes pro- duced enormous numbers of endemic, ecologically, *Present address: Department of Ecology and Evolution, Uni- and morphologically highly differentiated, species versity of Lausanne, Le Biophore, 1015 Lausanne, Switzerland within short evolutionary time spans (Salzburger Correspondence to: C. Sturmbauer; email: christian.sturmbauer@ et al. 2002, 2005; Verheyen et al. 2003; Joyce et al. uni-graz.at 2005). Estimates of the ages and numbers of cichlid 34 species for the East African Great Lakes range from 9 structure across larger geographic distances (Shaw et to 12 million years (my), with 250 species, for Lake al. 2000; Taylor and Verheyen 2001; Pereyra et al. Tanganyika; 4 to 9 my, with 700–800 species, for 2004). Lake Malawi; and 0.2 to 0.5 my, with 500–700 Although even short habitat discontinuities act as species, for Lake Victoria (Kornfield and Smith 2000; strong migration barriers to some rock-dwellers of Snoeks 2001; Turner et al. 2001). The fast speciation Lake Malawi, they seem to disperse freely along rates in lacustrine cichlids have been associated with a continuous rocky shorelines (van Oppen et al. 1997a; variety of mechanisms and conditions, including Arnegard et al. 1999; Rico and Turner 2002). We do natural and sexual selection, hybridization, and not know of studies on the population structure of habitat complexity and instability (Fryer and Iles Lake Victoria cichlids, but a representative of the 1972; Kornfield and Smith 2000; Kocher 2004; Salz- ‘‘Lake Victoria superflock’’ from an unstructured burger and Meyer 2004; Schliewen and Klee 2004; satellite lake displayed little if any genetic structure Seehausen 2004). There is compelling evidence of (Abila et al. 2004). In contrast, studies of rock spe- sympatric divergence in small West African (Schlie- cialists from Lake Tanganyika demonstrated high wen et al. 1994; Schliewen and Klee 2004) and Nic- population differentiation along continuous stretches araguan crater lake cichlids (Barluenga et al. 2006), of shoreline as well as across habitat barriers (Ru¨ ber and to some extent also in Lake Victoria (Seehausen et al. 2001; Taylor et al. 2001; Duftner et al. 2006). and van Alphen 1999), but in more mature species The present study compares genetic differentiation flocks such as Lakes Malawi and, especially, Tang- and diversity in nuclear and mitochondrial markers anyika, diversification has been attributed largely to in representatives of three endemic tribes of Lake allopatric processes (Sturmbauer 1998). Tanganyika, Eretmodus cyanostictus (Eretmodini), Among the most severe events repeatedly reshap- Ophthalmotilapia ventralis (Ectodini), and Tropheus ing the East African Great LakesÕ lacustrine envi- moorii (Tropheini; Poll 1986). The tribes span a large ronments, fluctuations in the water level associated part of the phylogenetic diversity of cichlids in Lake with paleoclimatic changes and geologic activity were Tanganyika (Fig. 1) (Salzburger et al. 2002). The shown to have affected the population structure and monogamous, biparental mouthbrooding Eretmodini speciation patterns in all three Great Lakes simulta- are one of the eight seeding lineages of the Lake neously (Sturmbauer et al. 2001; Verheyen et al. Tanganyika radiation (Salzburger et al. 2002). Re- 2003). Rossiter (1995) coined the term ‘‘species duced swim bladders are believed to constrain dis- pump’’ for the diversifying action of fluctuating lake persal of E. cyanostictus; the species has been shown levels and the associated recurrent cycles of popula- to be genetically structured in other localities (Taylor tion fusion and fragmentation. Radiations of several et al. 2001; Ru¨ ber et al. 2001) and provides a refer- cichlid lineages in Lake Tanganyika, for example, ence to evaluate the level of differentiation in the coincide with major water level changes (Sturmbauer other species. Ectodini and Tropheini derive from the et al. 2003; Brandsta¨ tter et al. 2005; Duftner et al. ancestor of the ‘‘redefined H-lineage’’ (Salzburger 2005; Koblmu¨ ller et al. 2005), and phylogeographic et al. 2002), a particularly species-rich lineage of patterns of several benthic species provide evidence of mouthbrooding cichlids exhibiting a wealth of mor- recurrent population shifts coupled with changes of phological, ecological, and behavioral diversity. Even shoreline structure and water depth (Verheyen et al. within tribes, diversity is high: the 35 Ectodini species 1996; Sturmbauer et al. 1997, 2001, 2005; Ru¨ ber et al. encompass maternal and biparental mouthbrooders, 1999; Baric et al. 2003). as well as specialized rock- and sand-dwellers with The potential for allopatric diversification in East different feeding modes (Koblmu¨ ller et al. 2004). The African cichlids is best illustrated by one of the most ectodine representative in this study, O. ventralis, is a species-rich clades, the mbuna haplochromines of rock-dwelling, polygamous, maternal mouthbrooder, Lake Malawi, which are comprised of stenotopic whose males defend territories around a nest site inhabitants of rocky coasts. With little to no gene (bowers) consisting of a layer of sand on a flat rock flow across habitat barriers such as sandy and deep- surface, and are visited by gravid females for water sections (van Oppen et al. 1997a; Arnegard spawning (Konings 1998). The 25 Tropheini species et al. 1999; Markert et al. 1999; Danley et al. 2000; endemic to Lake Tanganyika are member of the Rico and Turner 2002), numerous local variants are ‘‘modern haplochromines’’ and sister-group to the likely to have evolved allopatrically on a small spatial species flocks of Lakes Malawi and Victoria and scale (Fryer and Iles 1972; Ribbink et al. 1983). Ge- several other East African riverine and lacustrine netic differentiation among non-mbuna cichlid spe- cichlids (Salzburger et al. 2005). Within the Trophe- cialists of rocky and sandy habitat in Lake Malawi is ini, the genus Tropheus is renowned for pronounced equally dictated by habitat structure (Pereyra et al. geographical color variation: more than 100 different 2004), whereas neither benthic generalists nor pelagic color morphs have been described (Schupke 2003). and demersal species developed significant genetic Although classified into several nominal species, the 35 Fig. 1. Sampling sites and study species. A Lake Tanganyika, with the locations of the sample sites along the southwestern shoreline. Bathymetric lines are approximated according to Fig. 1 of Gasse et al. (1989). B Cladogram