On the Coyne and Orr-igin of species: effects of intrinsic postzygotic isolation, ecological differentiation, x chromosome size, and sympatry on Drosophila speciation

Abstract

Coyne and Orr found that mating discrimination (premating isolation) evolves much faster between sympatric than allopatric Drosophila species pairs. Their meta-analyses established that this pattern, expected under reinforcement, is common and that Haldane's rule is ubiquitous in Drosophila species divergence. We examine three possible contributors to the reinforcement pattern: intrinsic postzygotic isolation, dichotomized as to whether hybrid males show complete inviability/sterility; host-plant divergence, as a surrogate for extrinsic postzygotic isolation; and X chromosome size, whether roughly 20% or 40% of the genome is X-linked. We focus on "young" species pairs with overlapping ranges, contrasted with allopatric pairs. Using alternative criteria for "sympatry" and tests that compare either level of prezygotic isolation in sympatry or frequency of sympatry, we find no statistically significant effects associated with X chromosome size or our coarse quantifications of intrinsic postzygotic isolation or ecological differentiation. Although sympatric speciation seems very rare in animals, the pervasiveness of the reinforcement pattern and the commonness of range overlap for close relatives indicate that speciation in Drosophila is often not purely allopatric. It remains to determine whether increased premating isolation with sympatry results from secondary contact versus parapatric speciation and what drives this pattern.

Keywords: Allopatry; Dobzhansky-Muller incompatibilities (DMIs); extrinsic postzygotic isolation; parapatric speciation; reinforcement.

Figure 1

Patterns of prezygotic isolation as functions of genetic divergence (time) for pairs of Drosophila species with D_Nei ≤ 0.5. These phylogenetically corrected data are summarized and analyzed in Table 1. Black circles represent sympatric species pairs, grey squares represent allopatric pairs. Panel A. Open and filled symbols represent species contrasts with I_post = 0 and I_post > 0, respectively, where I_post denotes the Coyne and Orr (1989a) index of intrinsic postzygotic isolation. Panel B. Open and filled symbols represent species contrasts with I_ext = 0 and I_ext > 0, respectively, where I_ext denotes whether the pairs show ecological divergence according to Funk et al. (2006). Panel C. Open and filled symbols represent species contrasts with “small” and “large” X chromosomes, respectively.