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Abstract Models of “plasticity‐first” evolution are attractive because they explain the rapid evolution of new complex adaptations. Nevertheless, it is unclear whether plasticity can facilitate rapid microevolutionary change between diverging populations. Here, we show how plasticity may have generated adaptive differences in fecundity between neighboring wild populations of burying beetles Nicrophorus vespilloides. These populations occupy distinct Cambridgeshire woodlands that are just 2.5 km apart and that probably originated from a common ancestral population about 1000‐4000 years ago. We find that populations are divergently adapted to breed on differently sized carrion. Adaptive differences in clutch size and egg size are associated with divergence at loci connected with oogenesis. The populations differ specifically in the elevation of the reaction norm linking clutch size to carrion size (i.e., genetic accommodation), and in the likelihood that surplus offspring will be lost after hatching. We suggest that these two processes may have facilitated rapid local adaptation on a fine‐grained spatial scale.

Abstract Mutually beneficial interactions between species play a key role in maintaining biodiversity and ecosystem function. Nevertheless, such mutualisms can erode into antagonistic interactions. One explanation is that the fitness costs and benefits of interacting with a partner species vary among individuals. However, it is unclear why such variation exists. Here, we demonstrate that social behavior within species plays an important, though hitherto overlooked, role in determining the relative fitness to be gained from interacting with a second species. By combining laboratory experiments with field observations, we report that conflict within burying beetles Nicrophorus vespilloides influences the fitness that can be gained from interacting with the mite Poecilochirus carabi. Beetles transport these mites to carrion, upon which both species breed. We show that mites help beetles win intraspecific contests for this scarce resource: mites raise beetle body temperature, which enhances beetle competitive prowess. However, mites confer this benefit only upon smaller beetles, which are otherwise condemned by their size to lose contests for carrion. Larger beetles need no assistance to win a carcass and then lose reproductive success when breeding alongside mites. Thus, the extent of mutualism is dependent on an individual's inability to compete successfully and singlehandedly with conspecifics. Mutualisms degrade into antagonism when interactions with a partner species start to yield a net fitness loss, rather than a net fitness gain. This study suggests that interactions with conspecifics determine where this tipping point lies.