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.

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Animals often adjust their behavior according to social context, but the capacity for such behavioral flexibility can vary among species. Here, we test for interspecific variation in behavioral flexibility by comparing burrowing behavior across three species of deer mice (genus Peromyscus) with divergent social systems, ranging from promiscuous (Peromyscus leucopus and Peromyscus maniculatus) to monogamous (Peromyscus polionotus). First, we compared the burrows built by individual mice to those built by pairs of mice in all three species. Although burrow length did not differ in P. leucopus or P. maniculatus, we found that P. polionotus pairs cooperatively constructed burrows that were nearly twice as long as those built by individuals and that opposite‐sex pairs dug longer burrows than same‐sex pairs. Second, to directly observe cooperative digging behavior in P. polionotus, we designed a burrowing assay in which we could video‐record active digging in narrow, transparent enclosures. Using this novel assay, we found, unexpectedly, that neither males nor females spent more time digging with an opposite‐sex partner. Rather, we demonstrate that opposite‐sex pairs are more socially cohesive and thus more efficient digging partners than same‐sex pairs. Together, our study demonstrates how social context can modulate innate behavior and offers insight into how differences in behavioral flexibility may evolve among closely related species.

Evolutionary biologists have long sought to understand the selective pressures driving phenotypic evolution. While most experimental data come from the study of morphological evolution, we know much less about the ultimate drivers of behavioral variation. Among the most striking examples of behavioral evolution are the long, complex burrows constructed by oldfield mice ( Peromyscus polionotus ssp.). Yet how these mice use burrows in the wild, and whether burrow length may affect fitness, remains unknown. A major barrier to studying behavior in the wild has been the lack of technologies to continuously monitor — in this case, nocturnal and underground — behavior. Here, we designed and implemented a novel radio frequency identification (RFID) system to track patterns of burrow use in a natural population of beach mice. We combine RFID monitoring with burrow measurements, genetic data, and social network analysis to uncover how these monogamous mice use burrows under fully natural ecological and social conditions. We first found that long burrows provide a more stable thermal environment and have higher juvenile activity than short burrows, underscoring the likely importance of long burrows for rearing young. We also find that adult mice consistently use multiple burrows throughout their home range and tend to use the same burrows at the same time as their genetic relatives, suggesting that inclusive fitness benefits may accrue for individuals that construct and maintain multiple burrows. Our study highlights how new automated tracking approaches can provide novel insights into animal behavior in the wild.