Habitat-specific temporal variation in the pace of fish diversification

Abstract

Speciation and extinction events are concentrated unevenly through space and time, shaping the global distribution of extant biodiversity. Habitats modulate these dynamics over short timescales by determining the ecological landscape and providing substrate for diversification. This raises questions about whether biotic and abiotic heterogeneity across habitats also influenced diversification rate over geological timescales. Here, we show the rate of species diversification varies through time according to major differences between aquatic habitats for ray-finned fishes, which comprise over half of vertebrate diversity. Phylogeny-wide net diversification rates have accelerated 1.5-1.7x in reef-associated, freshwater benthopelagic and freshwater demersal lineages, which inhabit complex benthic habitats, while remaining constant through time in other less complex habitats such as the pelagic zone. Combined evidence across multiple diversification models implicates the rise of benthic-feeding fishes, which capitalized on functional feeding innovations and the reorganization of benthic resources following the Paleocene-Eocene Thermal Maximum. Our results show that the global biodiversity of ray-finned fishes is shaped by a combination of clade-specific pulses and tree-wide rate shifts, an outcome of the dynamic interplay between the traits of species and the features of the habitats they occupy. Significance statementAquatic habitats vary considerably in their biotic and abiotic properties. In this study, we demonstrate that these differences have modulated the pace of species diversification through time for ray-finned fishes, a group that represents over half of extant vertebrate species. By estimating habitat-specific speciation and extinction rates at a high temporal resolution, we find accelerated diversification beginning [~]50 Mya for species living in complex benthic habitats. We show that this pattern is in part driven by the rise of species that took advantage of functional innovations to feed on a diverse array of benthic associated resources, like coral and algae. These results highlight the interplay between the traits of species and the properties of the habitats they occupy in generating the biodiversity patterns observed today.