Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds

Abstract

The rate at which speciation occurs varies greatly among different kinds of organisms and is frequently assumed to result from species-or clade-specific factors that influence the rate at which populations acquire reproductive isolation. This premise leads to a fundamental prediction that has never been tested: Organisms that quickly evolve prezygotic or postzygotic reproductive isolation should have faster rates of speciation than organisms that slowly acquire reproductive isolation. We combined phylogenetic estimates of speciation rates from Drosophila and birds with a method for analyzing interspecific hybridization data to test whether the rate at which individual lineages evolve reproductive isolation predicts their macroevolutionary rate of species formation. We find that some lineages evolve reproductive isolation much more quickly than others, but this variation is decoupled from rates of speciation as measured on phylogenetic trees. For the clades examined here, reproductive isolation-especially intrinsic, postzygotic isolation-does not seem to be the rate-limiting control on macroevolutionary diversification dynamics. These results suggest that factors associated with intrinsic reproductive isolation may have less to do with the tremendous variation in species diversity across the evolutionary tree of life than is generally assumed. A central challenge at the interface between macroevolution and microevolution is to explain the population-level processes that contribute to biological variation in diversification rates and species richness (1). Phylogenetic evidence for biological variation in the rate of species diversification is widespread (2, 3), and numerous studies have now linked specific traits to the dynamics of speciation and extinction as realized over macroevolutionary timescales (2,4). At the population level, a microevolutionary research program on the biology of speciation has focused on the factors that lead to various forms of reproductive isolation (RI) between populations (5, 6). Explaining how and why RI evolves is generally considered to be the central and defining challenge in the study of speciation (2, 7-9), and recent studies have made great progress toward explaining the genetic and ecological basis for various forms of RI (7,8,10).Most microevolutionary research on speciation implicitly assumes that RI is the defining and rate-limiting step in the speciation process (7,8,11), but the evolution of RI need not bear any predictive relationship to rates of species diversification as realized over macroevolutionary timescales (12). This has long been recognized by the paleontological community, where "successful" speciation is believed to entail not only the evolution of reproductive isolation but also the persistence of incipient species (13-15). For example, speciation might be limited primarily by the rate at which lineages form allopatric isolates (6,16) or by the capacity for geographic range expansion (17, 18). Likewise, speciation might be limited more by factors that influe...

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