The tropics are the source of most biodiversity yet inadequate sampling obscures answers to fundamental questions about how this diversity evolves. We leveraged samples assembled over decades of fieldwork to study diversification of the largest tropical bird radiation, the suboscine passerines. Our phylogeny, estimated using data from 2389 genomic regions in 1940 individuals of 1287 species, reveals that peak suboscine species diversity in the Neotropics is not associated with high recent speciation rates but rather with the gradual accumulation of species over time. Paradoxically, the highest speciation rates are in lineages from regions with low species diversity, which are generally cold, dry, unstable environments. Our results reveal a model in which species are forming faster in environmental extremes but have accumulated in moderate environments to form tropical biodiversity hotspots.

An implicit assumption of speciation biology is that population differentiation is an important stage of evolutionary diversification, but its significance as a rate-limiting control on phylogenetic speciation dynamics remains largely untested. If population differentiation within a species is related to its speciation rate over evolutionary time, the causes of differentiation could also be driving dynamics of organismal diversity across time and space. Alternatively, geographic variants might be short-lived entities with rates of formation that are unlinked to speciation rates, in which case the causes of differentiation would have only ephemeral impacts. By pairing population genetics datasets from 173 New World bird species (>17,000 individuals) with phylogenetic estimates of speciation rate, we show that the population differentiation rates within species are positively correlated with their speciation rates over long timescales. Although population differentiation rate explains relatively little of the variation in speciation rate among lineages, the positive relationship between differentiation rate and speciation rate is robust to species-delimitation schemes and to alternative measures of both rates. Population differentiation occurs at least three times faster than speciation, which suggests that most populations are ephemeral. Speciation and population differentiation rates are more tightly linked in tropical species than in temperate species, consistent with a history of more stable diversification dynamics through time in the Tropics. Overall, our results suggest that the processes responsible for population differentiation are tied to those that underlie broad-scale patterns of diversity.