Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation

Abstract

Hybridization is often maladaptive and in some instances has led to the loss of biodiversity. However, hybridization can also promote speciation, such as during homoploid hybrid speciation, thereby generating biodiversity. Despite examples of homoploid hybrid species, the importance of hybridization as a speciation mechanism is still widely debated, and we lack a general understanding of the conditions most likely to generate homoploid hybrid species. Here we show that the level of genetic divergence between hybridizing species has a large effect on the probability that their hybrids evolve reproductive isolation. We find that populations of hybrids formed by parental species with intermediate levels of divergence were more likely to mate assortatively, and discriminate against their parental species, than those generated from weakly or strongly diverged parental species. Reproductive isolation was also found between hybrid populations, suggesting differential sorting of parental traits across populations. Finally, hybrid populations derived from three species were more likely to evolve reproductive isolation than those derived from two species, supporting arguments that hybridization-supplied genetic diversity can lead to the evolution of novel "adaptive systems" and promote speciation. Our results illustrate when we expect hybridization and admixture to promote hybrid speciation. Whether homoploid hybrid speciation is a common speciation mechanism in general remains an outstanding empirical question.

Keywords: Drosophila; homoploid; hybridization; mating behavior; speciation.

Fig. 1.

Behavioral isolation between hybrid populations and their parents. (A) The proportion of hybrid populations that exhibited behavioral isolation from both their parental species was highest at intermediate levels of parental divergence (Nei’s D). (B) The strength of reproductive isolation in hybrid populations that displayed assortative mating in female-choice mating trials increased with increasing levels of parental divergence. (C) When considering hybrid populations that did not show any evidence of assortative mating, the strength of discrimination against one parental species (i.e., preference for the other parental species) increased with increasing parental divergence. In all panels, gray points are observed values, vertical bars are 95% binomial confidence intervals, and colored points are model-predicted values (SI Appendix). Note the break in the y axis of A between 0.2 and 0.45.

Fig. 2.

Hybrid populations that displayed RI from their parental species also showed RI from other hybrid populations. Hybrid populations derived from D. paulistorum ‘Orinoco’ × D. paulistorum ‘Amazon’ and D. yakuba × D. santomea showed evidence of RI between other hybrid populations of the same parental type in 36 of 40 pairwise comparisons. Nonsignificant (ns) Tukey’s pairwise contrasts, corrected for multiple comparisons, are indicated with brackets. All comparisons were conducted between the proportion of focal males that mated in control trials (dark-gray boxes) and trials where females were given a choice between males from their same population, a different hybrid population, or males of their parental species (light-gray boxes).

Fig. 3.

Hybrid populations derived from three parental species are more likely to evolve behavioral isolation from their parental species. (A) A larger fraction of hybrid populations evolved behavioral isolation from their parental species when they were the result of crossing three parental species compared with two. However, the strength of assortative mating (i.e., reproductive isolation) within populations that did show evidence of evolving behavioral isolation did not differ between biparental or triparental hybrid populations (B). Biparental crosses 1–3 represent the different pairwise combinations of the parental species used to generate hybrid populations that were the result of crossing two species, and triparental hybrid populations were generated by crossing all three of the parental species (SI Appendix). The “NA” in A indicates that one of the three possible biparental crosses for the paulistorum flies was not conducted.