Phylogenomics reveals the deep ocean as an accelerator for evolutionary diversification in anglerfishes

Abstract

ABSTRACTColonization of a novel habitat is often followed by radiation in the wake of ecological opportunity. Alternatively, some habitats should be inherently more constraining than others if the challenges of that environment have few evolutionary solutions. We examined the push-and-pull of these factors on evolution following habitat transitions, using anglerfishes (Lophiiformes) as a model. Deep-sea fishes are notoriously difficult to study, and poor sampling has limited progress thus far. Here we present a new phylogeny of anglerfishes with unprecedented taxonomic sampling (1,092 loci and 40% of species), combined with three-dimensional phenotypic data from museum specimens obtained with micro-CT scanning. We use these datasets to examine the tempo and mode of phenotypic and lineage diversification using phylogenetic comparative methods, comparing lineages in shallow and deep benthic versus bathypelagic habitats. Our results show that anglerfishes represent a surprising case where the bathypelagic lineage has greater taxonomic and phenotypic diversity than coastal benthic relatives. This defies expectations based on ecological principles since the bathypelagic zone is the most homogeneous habitat on Earth. Deep-sea anglerfishes experienced rapid lineage diversification concomitant with colonization of the bathypelagic zone from a continental slope ancestor. They display the highest body, skull and jaw shape disparity across lophiiforms. In contrast, reef-associated taxa show strong constraints on shape and low evolutionary rates, contradicting patterns suggested by other shallow marine fishes. We found that Lophiiformes as a whole evolved under an early burst model with subclades occupying distinct body shapes. We further discuss to what extent the bathypelagic clade is a secondary adaptive radiation, or if its diversity can be explained by non-adaptive processes.