Increased phenotypic diversity as a consequence of ecological opportunity in the island radiation of Sulawesi ricefishes (Teleostei: Adrianichthyidae).

Abstract

Ecological opportunity is considered a main driver of adaptive diversification. Colonization of new areas and habitats provides novel opportunities, which may lead to phenotypic change and rapid diversification. The geographically isolated island Sulawesi in Indonesia hosts numerous endemic radiations. The ricefish family Adrianichthyidae is the most speciose of the few exclusively freshwater-dwelling fish lineages that colonized the tropical island. While the family's distribution includes large parts of Asia, the monophyletic lineage endemic to Sulawesi comprises more than half of all species described, with conspicuous morphological diversity. Using shape and size as proxies for phenotypic and ecological diversity, we first test the hypothesis that Sulawesi ricefishes are more diverse than non-Sulawesi species. We then ask if adaptation to alternative macrohabitats, namely rivers and lakes, can explain phenotypic diversification. We find that Sulawesi ricefishes exhibit greater disparity in body and head shape than non-Sulawesi ricefishes. By including phylogenomic data, we demonstrate that shape diversity in Sulawesi evolved along multiple trajectories, with reduced phylogenetic influence. Changes in body depth and head elongation are prominent, indicating distinct ecological drivers. In particular, body depth evolves along the river-lake axis, and lake species are more diverse compared to riverine ricefishes. In some lacustrine species, pronounced changes in head shape, a trait commonly associated with feeding in fishes, suggest trophic adaptation. Rates of phenotype evolution are higher in the Sulawesi lineages, in particular in lacustrine species. Lastly, we identified opposing trends in size evolution, with generally larger bodies in Sulawesi and repeated miniaturization in non-Sulawesi species. Our results indicate that ecological opportunity greatly influenced the observed phenotype diversity. Low diversity of freshwater fish lineages created environments with reduced competition, whereas additional factors, such as the island's complex geological history, created diverse habitats. As reflected in very localized endemism, species diversity is possibly also driven by long-term spatial isolation, which alone however offers insufficient explanation for the increase in phenotypic disparity. Taken together, ecological opportunity was a dominant driver of the phenotypic diversification of Sulawesi ricefishes, potentially complemented by past introgressive hybridization events and small-scale spatial isolation.