Ancient Hybridization and Phenotypic Novelty within Lake Malawi's Cichlid Fish Radiation

Abstract

Does hybridization play a broad innovative role in evolution? Many studies have shown hybrid origins of individual species, particularly in major adaptive radiations, but this may be a consequence, rather than a cause, of the existence of many closely related species. Cases of hybridization in the early stages of major adaptive radiations are comparatively rare. Here, we report phylogenetic evidence for ancient introgression between distinct lineages of the species-rich Lake Malawi haplochromine cichlid fishes. Mitochondrial DNA (mtDNA) sequences indicated surprisingly close relationships between the shallow-water rocky habitat "Mbuna" species and a group of dark-adapted "Deep-Benthic" species specialized for feeding in low-light conditions (dawn/dusk, under overhangs, and deep water). By contrast, analyses of nuclear amplified fragment length polymorphism data demonstrated that these Deep-Benthic cichlids were more closely related to shallow water "Shallow-Benthic" soft-sediment feeders, a group that shares similar head and body morphology. A coalescent-based computer simulation indicated that the mtDNA similarity of rocky habitat Mbuna species and dark-adapted Deep-Benthic species was due to hybridization rather than incomplete lineage sorting. Comparisons of morphology indicated that some Deep-Benthic species possessed novel morphology not present in other Lake Malawi species groups. Thus, these analyses support the hypothesis that ancient hybridization occurred within the Lake Malawi cichlid radiation, that the event occurred before the radiation of a species group adapted to low-light benthic habitats, and that this group went on to dominate the deep-water regions of Lake Malawi. The results of this study contribute to a growing literature consistent with a creative role of hybridization in the evolution of species diversity and adaptive radiations.