How locally adapted ecotypes are established and maintained within a species is a long-standing question in evolutionary biology. Using forest and prairie ecotypes of deer mice ( Peromyscus maniculatus ), we characterized the genetic basis of variation in two defining traits—tail length and coat color—and discovered a 41-megabase chromosomal inversion linked to both. The inversion frequency is 90% in the dark, long-tailed forest ecotype; decreases across a habitat transition; and is absent from the light, short-tailed prairie ecotype. We implicate divergent selection in maintaining the inversion at frequencies observed in the wild, despite high levels of gene flow, and explore fitness benefits that arise from suppressed recombination within the inversion. We uncover a key role for a large, previously uncharacterized inversion in the evolution and maintenance of classic mammalian ecotypes.

A long-standing question in evolutionary biology is how differences in multiple traits can evolve quickly and be maintained together during local adaptation. Using forest and prairie ecotypes in deer mice, which differ in both tail length and coat color, we discovered a 41 Mb chromosomal inversion that is strongly linked to variation in both traits. The inversion maintains highly divergent loci in strong linkage disequilibrium and likely originated ~170 kya, long before the forest-prairie divergence ~10 kya. Consistent with a role in local adaptation, inversion frequency is associated with phenotype and habitat across both a local transect and the species range. Still, although eastern and western forest subspecies share similar phenotypes, the inversion is absent in eastern North America. This work highlights the significance of inversion polymorphisms for the establishment and maintenance of multiple locally adaptive traits in mammals, and demonstrates that, even within a species, parallel phenotypes may evolve through nonparallel genetic mechanisms.

Abstract. Greater resource use by diverse communities might result from species occupying complementary niches. Demonstrating niche complementarity among species is challenging, however, due to the difficulty in relating differences between species in particular traits to their use of complementary resources. Here, we overcame this obstacle by exploiting plastic foraging behavior in a community of predatory insects common on Brassica oleracea plants in Washington, USA. These predators complemented one another by partitioning foraging space, with some species foraging primarily along leaf edges and others at leaf centers. We hypothesized that emergent biodiversity effects would occur when predators partitioned foraging space on leaves, but not when spatial complementarity was dampened. Indeed, on intact leaves, edge-and center-foraging predators combined to kill more prey than any single predator species could by itself. These emergent diversity effects, however, disappeared on plants damaged by the caterpillar Plutella xylostella. Caterpillar chew-holes brought edge habitats to the center of leaves, so that all predator species could attack aphids anywhere on plants. With spatial niche differences diminished, there were no benefits of predator diversity; the most voracious single predator species killed the most aphids. Thus, caterpillar herbivory determined whether multi-predator-species effects reflected complementarity or species' individual impacts. Our study provides direct evidence for a causative relationship between niche differentiation and increased resource consumption by diverse communities, as revealed by ecological engineers that homogenize the foraging environment.

LINE-1 (long interspersed element-1) retroelements are the only active autonomous endogenous retroelements in human genomes. Their retrotransposition activity has created close to 50% of the current human genome. Due to the apparent costs of this proliferation, host genomes have evolved multiple mechanisms to curb LINE-1 retrotransposition. Here, we investigate the evolution and function of the LINE-1 restriction factor APOBEC3A, a member of the APOBEC3 cytidine deaminase gene family. We find that APOBEC3A genes have evolved rapidly under diversifying selection in primates, suggesting changes in APOBEC3A have been recurrently selected in a host-pathogen "arms race." Nonetheless, in contrast to previous reports, we find that the LINE-1 restriction activity of APOBEC3A proteins has been strictly conserved throughout simian primate evolution in spite of its pervasive diversifying selection. Based on these results, we conclude that LINE-1s have not driven the rapid evolution of APOBEC3A in primates. In contrast to this conserved LINE-1 restriction, we find that a subset of primate APOBEC3A genes have enhanced antiviral restriction. We trace this gain of antiviral restriction in APOBEC3A to the common ancestor of a subset of Old World monkeys. Thus, APOBEC3A has not only maintained its LINE-1 restriction ability, but also evolved a gain of antiviral specificity against other pathogens. Our findings suggest that while APOBEC3A has evolved to restrict additional pathogens, only those adaptive amino acid changes that leave LINE-1 restriction unperturbed have been tolerated.

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.