Abstract
Understanding the general features of speciation is an important goal in evolutionary biology, and despite significant progress, several unresolved questions remain. We analyzed an extensive comparative dataset consisting of more than 1900 crosses between 92 species of toads to infer patterns of reproductive isolation. This unique dataset provides an opportunity to examine the strength of reproductive isolation, the development and sex ratios of hybrid offspring, patterns of fertility and infertility, and polyploidization in hybrids all in the context of genetic divergence between parental species. We found that the strength of intrinsic postzygotic isolation increases with genetic divergence, but relatively high levels of divergence are necessary before reproductive isolation is complete in toads. Fertilization rates were not correlated to genetic divergence, but hatching success, the number of larvae produced, and the percentage of tadpoles reaching metamorphosis were all inversely related with genetic divergence. Hybrids between species with lower levels of divergence developed to metamorphosis, while hybrids with higher levels of divergence stopped developing in gastrula and larval stages. Sex ratios of hybrid offspring were biased towards males in 70% of crosses and biased towards females in 30% of crosses. Hybrid females from crosses between closely related species were completely fertile, while approximately half (53%) of hybrid males were sterile, with sterility predicted by genetic divergence. The degree of abnormal ploidy in hybrids was positively related to genetic divergence between parental species, but surprisingly, polyploidization had no effect on patterns of asymmetrical inviability. We discuss explanations for these patterns, including the role of Haldane's rule in toads and anurans in general, and suggest mechanisms generating patterns of reproductive isolation in anurans.
Highlights
Reproductive isolation is a defining characteristic of a biological species, and it is integral to creating and maintaining species boundaries [1]
Patterns of Reproductive Isolation We compiled the data found in Blair (1972) [40] which consisted of 1,934 crosses between 92 species of Bufo; one of the largest datasets for any vertebrate organism
We developed an index of reproductive isolation to explore the relationship between reproductive isolation and genetic distance (Table 1 and see Methods)
Summary
Reproductive isolation is a defining characteristic of a biological species, and it is integral to creating and maintaining species boundaries [1]. The broad patterns produced from these studies can be summarized as follows: 1) hybrid sterility evolves faster than hybrid inviability, but both measures of reproductive isolation evolve gradually; 2) the time frame in which pre- or postzygotic isolation evolves between species is organism-specific; and 3) Haldane’s rule is obeyed regardless of sex determination system (ZW or XY), and is an important first step toward the reproductive isolation of biological species [1,25–27, but see 28] These comparative analyses have been used to demonstrate that ecological divergence and reproductive isolation are strongly associated, suggesting that ecological adaptation plays an important role in reproductive isolation [29]
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