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

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 influence the temporal persistence of reproductively isolated populations (15, 19) than by the rate at which RI itself evolves. Finally, macroevolutionary diversity dynamics might be regulated primarily by factors that influence extinction rates (4). These factors need not be independent of reproductive isolation. For example, reproductive barriers can reduce the probability of population fusion following secondary contact between nascent species, thus exerting a direct effect on population persistence (2). Likewise, RI can influence the dynamics of geographic range evolution, which may in turn have secondary consequences for rates of demographic extinction and allospecies formation (17, 18).Here, we provide a direct test of the relationship between reproductive isolation and macroevolutionary diversification. If the widespread variation observed in macroevolutionary diversification rates (20, 21) is attributable to factors that cause RI (2, 22, 23), then it must also be true that lineage-specific differences in the rate at which RI evolves will influence large-scale patterns of species diversification. In this context, a species with a “fast” rate of RI evolution will, all else being equal, form more reproductively isolated lineages than a species with a “slow” rate of RI evolution.We use data from the two groups of animals for which the most extensive multispecies RI data have been compiled and for which we could derive phylogeny-based estimates of species diversification rates. The first dataset is an update of Coyne and Orr’s (2) seminal work on the relationship between genetic distance, geographic status, and reproductive isolation in Drosophila (24) and contains estimates of both premating and intrinsic postzygotic RI. The second dataset includes measurements of intrinsic postyzygotic isolation from interspecies hybridizations in birds (25, 26). We developed a modeling framework for estimating species- and clade-specific differences in the rate of evolution of RI and applied it to both birds and flies to test whether lineages that quickly evolve RI are characterized by fast rates of macroevolutionary diversification. This framework can be used to assess whether any components of reproductive isolation are associated with speciation rates as measured at macroevolutionary scales. We find significant heterogeneity within both flies and birds in the rate at which lineages evolve intrinsic postzygotic isolation. However, this variation is uncorrelated with macroevolutionary rates of species diversification. These results suggest that patterns of biological diversity may have less to do with reproductive isolation than generally assumed.