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.

Keywords: hybrid incompatibility; mechanism of speciation; speciation gene; species concept.

Fig. 1.

Pairwise postzygotic reproductive isolation in flies and birds. (A) Genetic distance and intrinsic postzygotic RI in 173 pairwise Drosophila crosses. Red squares denote species crosses within a representative subclade with “fast” species-specific velocities of RI evolution (D. willistoni species group); blue triangles denote species with a “slow” velocity of RI evolution (D. virilis species group). Red (solid) and blue (dashed) lines indicate corresponding clade-specific trajectories from fitted linear model; thick and thin lines denote fits for sympatric and allopatric species pairs, respectively. Postzygotic RI ranges from 0 (hybrid offspring both fertile and viable) to 1 (all hybrids are sterile or inviable). (B) Genetic distance and postzygotic RI from 287 pairwise bird crosses. Red denotes pheasants and allies (Phasianidae), a representative clade with fast species-specific velocities of RI evolution; blue denotes parrots (Psittacidae), a family with slow velocities of RI evolution. Red (solid) and blue (dashed) lines denote model-predicted relationships for these clades under the asymptotic model for the accumulation of RI through time. Points in both A and B were jittered slightly in the x-plane to reduce overplotting.

Fig. 2.

Estimates of clade-specific velocities of RI evolution (ψ). (A) Premating ψ for nine Drosophila subclades where sampling was adequate to estimate clade-specific speciation rates. (B) Postzygotic ψ for Drosophila. (C) Postzygotic ψ across 30 families of birds. Confidence intervals denote 90% Bayesian credible interval about the mean. Point size reflects the number of species from each clade for which RI data were available.

Fig. 3.

Rates of speciation are uncorrelated with clade-specific variation in the rate at which species accumulate RI (Table 1; Table S3). (A) Premating ψ and relative speciation rate across nine Drosophila clades assuming low relative extinction rates (ψ model: asymptotic). (B) Postzygotic ψ for Drosophila (linear model) and relative speciation rates. (C) Postzygotic ψ estimates and mean speciation rate across 30 avian families (ψ model: asymptotic). (D) Postzygotic ψ estimates and the maximum speciation rate for bird clades.

Fig. 4.

Relationship between rates of speciation and species-specific velocities of postzygotic RI evolution across 244 species of birds. Instantaneous rates of speciation were estimated for each lineage under a statistical model that allowed each species to have a potentially unique rate of speciation (Fig. S5). Identically colored points denote species from the same order. Species that quickly evolve intrinsic reproductive isolation from other species do not speciate at faster rates than other species.