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Ecological speciation is the promotion of reproductive isolation via the divergent adaptation of populations to alternative environments. A prediction peculiar to ecological speciation is that hybrids between such populations should be adapted poorly to parental environments, yielding reduced fitness and postmating isolation. However, F1 analyses alone cannot demonstrate that ecological ('extrinsic') factors contribute to such isolation. Rather, this requires documenting a 'switch' in the relative fitnesses of reciprocal backcrosses between environments. Specifically, each backcross should exhibit higher fitness in the environment of its pure parent, with which it shares the most genes, including environment-specific ones. In contrast, because genetic proportions are expected to be similar for all backcrosses ([approximately equal to] 3/4 from one parental type and [approximately equal to] 1/4 from the other), the more general genetic incompatibilities responsible for 'intrinsic' isolation predict no such environment-specific fitness switches. Thus, although intrinsic isolation may contribute to the fitness reduction and variation underlying such patterns, it offers an insufficient explanation for them. Here, we present a quantitative genetic 'backcross' analysis of sympatric Neochlamisus bebbianae leaf beetle populations adapted to maple versus willow host plants. Results statistically supported ecological speciation predictions, notably the switch in relative fitness for backcross types, the expected rank order of cross type fitnesses, and appreciable extrinsic isolation. We additionally documented genetic variation in host-associated fitness, ruled out nongenetic maternal effects, and discuss the maintenance of ecological differentiation in sympatry. In summary, our study provides a rare and strongly supported demonstration of genetically based, ecologically dependent postmating isolation during ecological speciation. divergent adaptation | ecological speciation | host races | hybrid fitness | reproductive isolation www.pnas.org/cgi/doi/10.1073/pnas.0909424106

To what degree is the divergent adaptation responsible for life's phenotypic variety also responsible for generating the millions of species that manifest this variation? Theory predicts that ecological divergence among populations should promote reproductive isolation, and recent empirical studies provide support for this hypothesis in a limited number of specific taxa. However, the essential question of whether ecology plays a truly general role in speciation has yet to be systematically evaluated. Here we address this integral issue using an approach that adds an ecological dimension to comparative studies investigating the relationship between reproductive isolation and divergence time. Specifically, we quantify ecological divergence for >500 species pairs from eight plant, invertebrate, and vertebrate taxa and statistically isolate its association with reproductive isolation. This approach demonstrates a highly consistent and significant positive association between ecological divergence and reproductive isolation across taxa. This relationship was also observed across different aspects of ecological divergence and components of reproductive isolation. These findings are highly consistent with the hypothesis that ecological adaptation plays a fundamental and taxonomically general role in promoting reproductive isolation and speciation. comparative methods | Coyne and Orr | divergent adaptation | ecological speciation | genetic distance