Ecological and genomic signatures of the convergent evolution of planktivory in fossil and living reef fishes over deep time

Abstract

Abstract Transitions from benthic to pelagic habitats often coincide with shifts in diet, yet the genomic basis and macroevolutionary dynamics of these changes remain poorly understood. Surgeonfishes and allies (Acanthuriformes), with their rich fossil record, dietary diversity, and compact genomes, provide a powerful model to investigate these transitions across deep time. We integrate genomic data from 80 extant species with morphological data from 32 fossils to construct total-evidence, tip-dated phylogenomic trees and reconstruct ancestral diets and geographic ranges. We identify at least seven independent origins of planktivory and four reversals, with transitions concentrated in the Tethys and Indo-Pacific oceans. Contrary to the view that planktivory represents an evolutionary dead end, we find higher reversal rates and lower extinction in planktivores. Time-dependent models support both climate and phylogenetic effects on planktivorous lineage diversification. Using a newly assembled chromosome-level genome and 44 additional assemblies, we apply phenotype-aware selection models to identify 39 genes under convergent positive selection in planktivorous lineages. Six of these genes show accelerated evolution tied to metabolism and dietary specialization, and also exhibit codon-level parallelism or convergence. Our findings illuminate the ecological, biogeographic, and genomic basis of repeated dietary shifts and challenge assumptions about evolutionary constraints in pelagic environments.