Sympatric speciation, the divergence of one population into two or more species without geographical isolation, remains a controversial topic in evolutionary biology (Gavrilets 2004; Coyne 2007). For decades, the idea of universal allopatric speciation, resulting from genetic drift and selection after geographic isolation, has dominated speciation research (Mayr 1963; Mallet 2001). Nevertheless, theory predicts that under certain conditions speciation is possible without complete physical isolation of diverging populations (Dieckmann and Doebeli 1999; Higashi et al. 1999; Takimoto et al. 2000; Doebeli and Dieckmann 2003; Gavrilets 2003, 2004; Gavrilets and Vose 2005; Kawata et al. 2007). Strong disruptive selection for alternative “fitness peaks” in association with evolution of mate discrimination ranks among the most common scenarios (Gavrilets 2004; Coyne 2007), besides resource-specific assortative mating or hybrid speciation (Arnold 1997; Feder 1998; Seehausen 2004).
Empirical case studies suggest that several species pairs and radiations of plants and animals most likely evolved in sympatry (Schliewen et al. 1994, 2001; Berlocher and Feder 2002; Schliewen and Klee 2004; Feder et al. 2005; Savolainen et al. 2006; Friesen et al. 2007; Rolán-Alvarez 2007), but the total number of unambiguous cases remains low (Coyne 2007). The discussion currently focuses on the frequency of sympatric speciation in nature and, ultimately, on the mechanisms promoting it (Mallet 2001; Turelli et al. 2001; Via 2001; Coyne 2007). Recently, the idea of the mosaic nature of animal genomes (Templeton 1981; Mallet 1995, 2005; Feder 1998) has gained new momentum, suggesting that gene flow among recently evolved sympatric species is common and even generates adaptive variation (Wu 2001; Seehausen 2004; Mallet 2007).
Coyne and Orr (2004) suggested four criteria to reject the null hypothesis of allopatric speciation: (1) sympatry, (2) substantial reproductive isolation, and (3) sister group relationship of the diverged species with (4) implausibility of allopatric scenarios. Sister species or species flocks endemic to habitat islands, such as oceanic islands or isolated freshwater lakes, appear to be promising systems to test for these criteria because such isolated habitats allow ruling out phases of physical isolation (Via 2001; Coyne and Orr 2004). “Roundfin” sailfin silversides, endemic to isolated Lake Matano in Central Sulawesi (Indonesia), might represent an additional example of sympatric speciation, and are also a promising model to test for mechanisms promoting divergence. These small, atheriniform (Teleostei: Atheriniformes) freshwater fish are characterized by having rounded second dorsal and anal fins, distinguishing them from sympatric “sharpfin” sailfin silversides (Kottelat 1991). Three morphospecies are characterized according to the shape and size of adult, spawning individuals: high-bodied, large Telmatherina antoniae“large,” slender and small T. antoniae“small,” and slender, large T. prognatha (Kottelat 1991; Herder et al. 2006a). In contrast to the dusky-gray females, males of all three morphospecies occur in bright yellow, blue, or blue-yellow color morphs (Herder et al. 2006a) (Fig. 1). These fish are mobile and nonterritorial promiscuous substrate spawners (Gray and McKinnon 2006). Lake Matano is a comparably small (approx. 32 by 6 km; ≈164 km2) but extremely deep (> 590 m) graben-lake, with steep walls and without major intralake barriers down to more than 400 m depth (Haffner et al. 2001, Fig. 1). It is the uppermost of “Wallace's dreamponds” (Herder et al. 2006b), that is the Malili Lakes, a hotspot of freshwater diversity (von Rintelen et al. 2007). The lakes harbor endemic radiations of snails, crustaceans, and fish (Kottelat 1990a,b, 1991; von Rintelen et al. 2007). Age estimates of 1–2 Myr are provided in the literature, but have never been tested critically (von Rintelen et al. 2004).
The radiation of sailfin silversides has recently attracted attention as a model system for speciation processes. Roy et al. (2004, 2007a,b) identified three mitochondrial clades in Lake Matano's Telmatherina and based analyses of speciation processes on those three mtDNA haplotype groups. However, nuclear data only support two monophyletic groups (Herder et al. 2006b), corresponding to morphologically well-defined roundfins and sharpfins (Kottelat 1991). The additional mitochondrial clade results from introgression of haplotypes common in stream populations, into sharpfins (Herder et al. 2006b). Hence, sharpfins carry both “native” and introgressed “stream” mtDNA haplotypes, whereas roundfins are clearly monophyletic according to both marker systems.
The present study applies Coyne and Orr's (2004) criteria for sympatric speciation to Lake Matano's roundfins. Based on data derived from nuclear population-level genetic markers, ecological field observations, and analysis of body shape and stomach contents, we test for morphological, ecological, and genetic divergence within the well defined, compact area of an ancient lake. This approach allows incorporation of hypotheses on mechanisms discussed to drive speciation processes, namely ecological selection with respect to body shape, trophic ecology, and habitat use and sexual selection with respect to male coloration.