Phylogenomics establishes an Early Miocene reconstruction of reef vertebrate diversity

Oceans blanket more than two-thirds of Earth’s surface, yet marine
biodiversity is disproportionately concentrated in near-shore habitats,
especially coral reefs. Investigating the origins of the exceptional
species diversity found on coral reefs is crucial for predicting how these
ecosystems will respond to anthropogenic disturbances. Here, we use a
genome-scale dataset to reconstruct the evolutionary history of the
wrasses and parrotfishes (Labridae), which rank among the most
species-rich and ecologically diverse lineages of reef fishes. We show
that all major labrid clades experienced concurrent pulses of evolutionary
innovation and rapid lineage diversification over a period of fewer than
five million years during the Early Miocene. Analyses of historical
biogeography, character evolution, and phenotypic diversification rates
demonstrate that no single phenotypic innovation can explain this period
of accelerated diversification in wrasses. Instead, modern labrid
diversity is a mosaic of multiple concurrent adaptive and non-adaptive
radiations that diversified ~20-15 million years ago. These results draw
parallels to the evolutionary histories of many animal groups after the
Cretaceous-Paleogene mass extinction, suggesting a marked change in marine
biodiversity associated with the Miocene emergence of novel ecological
opportunities that wrasses exploited. Our results corroborate recently
reported fossil evidence for an Early Miocene extinction event in oceanic
vertebrates that we tie to changes in coral reef faunal composition and
ubiquity and support this period as a crucial time in the assembly of
present-day oceanic ecosystems.