Molecular phylogenetics supports multiple evolutionary transitions from marine to freshwater habitats in ariid catfishes

Abstract

Transitions between the marine and freshwater environments represent an extraordinary ecological shift that has promoted diversification in many groups of aquatic organisms. Here, molecular phylogenetics is utilized to investigate habitat transitions in a group of catfishes (Ariidae) that includes species inhabiting marine and brackish waters (>110 species) as well as freshwater environments (approximately 40 species). The Ariidae is nested within the Otophysi, the largest clade of primary freshwater fishes with four orders and 67 families. Optimizations of habitat transitions (freshwater vs. marine) onto a previously inferred phylogeny suggest a single invasion of marine waters at the root of the ariid tree followed by 10-15 events of freshwater colonization, implying reversion to the primitive otophysan condition. Thus, ariids provide an extraordinary example of bidirectional habitat transitions in fishes. Freshwater recolonization has occurred in all major provinces where ariids are present, such as the New World (Mesoamerica and South America), Madagascar, Africa, Southeast Asia, and the Sahul continent (Australia and New Guinea). The remarkable diversity of freshwater ariids in Australia-New Guinea and Mesoamerica is presumed to have been facilitated by the originally depauperate freshwater ichthyofaunas in both regions, particularly the low diversity of primary otophysan families in Mesoamerica and their absence in Australia and New Guinea. The lack of phylogenetic resolution among basal Sahul lineages coupled with their extraordinary level of morphological divergence and trophic diversity suggests an ancient rapid radiation promoted by freshwater colonization. For this reason, Sahul ariids represent an excellent system for studying diversification associated with habitat transitions.