Ecological differences often evolve early in speciation as divergent natural selection drives adaptation to distinct ecological niches, leading ultimately to reproductive isolation. Though this process is a major generator of biodiversity, its genetic basis remains poorly understood. Here we investigate the genetic architecture of niche differentiation in a sympatric species pair of threespine stickleback fish by mapping the environment-dependent effects of phenotypic traits on hybrid feeding and performance under semi-natural conditions. We show that multiple, unlinked loci act largely additively to determine position along the major niche axis separating these recently diverged species. We also find that functional mismatch between phenotypic traits reduces growth of some stickleback hybrids beyond that expected from an intermediate phenotype, suggesting a role for epistasis between the underlying genes. This functional mismatch might lead to hybrid incompatibilities that are analogous to those underlying intrinsic reproductive isolation but that depend on the ecological context.

The deer mouse (genus Peromyscus) is the most abundant mammal in North America, and it occupies almost every type of terrestrial habitat. It is not surprising therefore that the natural history of Peromyscus is among the best studied of any small mammal. For decades, the deer mouse has contributed to our understanding of population genetics, disease ecology, longevity, endocrinology and behavior. Over a century's worth of detailed descriptive studies of Peromyscus in the wild, coupled with emerging genetic and genomic techniques, have now positioned these mice as model organisms for the study of natural variation and adaptation. Recent work, combining field observations and laboratory experiments, has lead to exciting advances in a number of fields—from evolution and genetics, to physiology and neurobiology.DOI: http://dx.doi.org/10.7554/eLife.06813.001

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A central challenge in biology is to understand how innate behaviors evolve between closely related species. One way to elucidate how differences arise is to compare the development of behavior in species with distinct adult traits [1]. Here, we report that Peromyscus polionotus is strikingly precocious with regard to burrowing behavior, but not other behaviors, compared to its sister species P. maniculatus. In P. polionotus, burrows were excavated as early as 17 days of age, whereas P. maniculatus did not build burrows until 10 days later. Moreover, the well-known differences in burrow architecture between adults of these species-P. polionotus adults excavate long burrows with an escape tunnel, whereas P. maniculatus dig short, single-tunnel burrows [2-4]-were intact in juvenile burrowers. To test whether this juvenile behavior is influenced by early-life environment, we reciprocally cross-fostered pups of both species. Fostering did not alter the characteristic burrowing behavior of either species, suggesting that these differences are genetic. In backcross hybrids, we show that precocious burrowing and adult tunnel length are genetically correlated and that a P. polionotus allele linked to tunnel length variation in adults is also associated with precocious onset of burrowing in juveniles, suggesting that the same genetic region-either a single gene with pleiotropic effects or linked genes-influences distinct aspects of the same behavior at these two life stages. These results raise the possibility that genetic variants affect behavioral drive (i.e., motivation) to burrow and thereby affect both the developmental timing and adult expression of burrowing behavior.