Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika

Abstract

The current phylogenetic hypothesis for the endemic Lake Tanganyika cichlid fishes of the tribe Eretmodini is based solely on morphology and suggests that more complex trophic morphologies derived only once from a less specialized ancestral condition. A molecular phylogeny of eretmodine cichlids based on partial mitochondrial DNA cytochrome b and control-region sequences was used to reconstruct the evolutionary sequence of trophic adaptations and to test alternative models of morphological divergence. The six mitochondrial lineages found disagree with the current taxonomy and the morphology-based phylogeny. Mitochondrial lineages with similar trophic morphologies are not grouped monophyletically but are typically more closely related to lineages with different trophic phenotypes currently assigned to other genera. Our results indicate multiple independent origins of similar trophic specializations in these cichlids. A pattern of repeated divergent morphological evolution becomes apparent when the phylogeography of the mitochondrial haplotypes is analyzed in the context of the geological and paleoclimatological history of Lake Tanganyika. In more than one instance within Lake Tanganyika, similar morphological divergence of dentitional traits occurred in sympatric species pairs. Possibly, resource-based divergent selective regimes led to resource partitioning and brought about similar trophic morphologies independently and repeatedly.Phylogenetic information about species that form adaptive radiations will increase knowledge about the patterns and processes that drive morphological diversification and speciation. The reconstruction of morphological diversification based on a molecular phylogeny may offer new insights into the causes of phenotypic differentiation and speciation and the role of determinism and internal constraints in the evolution of adaptive radiations (1-6). The endemic cichlid species flocks of the East African Great Lakes-Victoria, Malawi, and Tanganyika-provide outstanding examples for adaptive radiations and rapid speciation resulting in unparalleled species diversities of hundreds of endemic species in each of these three lakes (1, 7). Lake Tanganyika is the longest (650 km long), deepest (about 1.4 km deep), and oldest [9-12 million years (8)] and houses the genetically most diverse flock of cichlids (reviewed in ref. 1).Cichlids of the tribe Eretmodini (9) are endemic to Lake Tanganyika. They encompass a high degree of diversity in oral tooth shapes and might therefore serve as a model system to investigate morphological differentiation among closely related species. This tribe comprises four nominal species currently assigned to three genera: Eretmodus cyanostictus, Spathodus erythrodon, Spathodus marlieri, and Tanganicodus irsacae. The shape of the oral jaw teeth is the main taxonomic character defining these species. The teeth of Eretmodus are spatula-shaped with a slender neck region, those of Spathodus are cylindrical with a flattened and truncated crown, and those of Tanganico...

Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus

“…Thick lines denote median estimates, thin lines indicate 95% HPD intervals. The y-axis represents the population size parameter (female effective population size, fN e , times the mutation rate, l) 1996; Rüber et al, 1999Rüber et al, , 2001Duftner et al, 2007;Egger et al, 2007). Extrapolating from other stenotopic rock-dwellers, we predicted that the phylogeographic structure of Altolamprologus spp.…”

Genetic and developmental basis of cichlid trophic diversity

“…Suction feeders, on the other hand, are characterized by an outer row of large, intermittently spaced teeth with fewer cusps. Like jaw morphology, cichlid dental patterning has evolved rapidly and replicatively, and is associated with both ancient and contemporary trophic evolution (Ruber et al, 1999;Huysseune et al, 2002;Streelman et al, 2003).…”

Microsatellites reveal high levels of population substructuring in the species–poor Eretmodine cichlid lineage from Lake Tanganyika

“…These include polygamous maternal mouth-brooders, monogamous substrate spawners, harem-based shell spawners and biparental mouthbrooders. Previous, lake-wide studies of rock-dwelling cichlid species from Lake Tanganyika indicate mitochondrial DNA (mtDNA) haplotypes with geographically restricted distributions in some species (Sturmbauer & Meyer 1992;Sturmbauer et al 1997;RÏber et al 1999). Other species show almost no geographical subdivision, suggesting that geological events and physical barriers may di¡erentially a¡ect gene £ow in closely related species, even those employing similar breeding systems Sturmbauer et al 1997).…”

“…E. cyanostictus is an apparently monogamous, sexually monochromatic, biparental mouth-brooder that exhibits a female-to-male pattern of mouth-brooding (Yamaoka et al 1986;Kuwamura et al 1989) and is widely distributed over the southern half of the lake. Previous research has revealed considerable di¡erences in mtDNA haplotype and microsatellite frequencies between populations (RÏber et al 1999(RÏber et al , 2001). E. cyanostictus retains only a vestigial swim bladder (Konings 1998), which is likely to allow it to remain close to the substrate in turbulent conditions.…”