Evaluating the role of coevolution in a horizontally transmitted mutualism

Mutualism depends on the alignment of host and symbiont fitness. Horizontal transmission can readily decouple fitness interests, yet horizontally transmitted mutualisms are common in nature. We hypothesized that pairwise coevolution and specialization in host-symbiont interactions underlies the maintenance of cooperation in a horizontally transmitted mutualism. Alternatively, we predicted selection by multiple host species may select for cooperative traits in a generalist symbiont through diffuse coevolution. We tested for signatures of pairwise coevolutionary change between the squash bug Anasa tristis and its horizontally acquired bacterial symbiont Caballeronia spp. by measuring local adaptation. We found no evidence for local adaptation between sympatric combinations of A. tristis squash bugs and Caballeronia spp. across their native geographic range. To test for diffuse coevolution, we performed reciprocal inoculations to test for specialization between three Anasa host species and Caballeronia spp. symbionts isolated from conspecific hosts. We observed no evidence of specialization across host species. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia spp. symbionts. Specifically, diffuse coevolution between multiple host species with a shared generalist symbiont may maintain cooperative traits despite horizontal transmission.

Could diffuse coevolution explain the generic eggshell color of the brown-headed cowbird?

The brown-headed cowbird (hereafter cowbird) is an avian brood parasite that produces an egg dissimilar to those produced by the majority of its diverse host community. The cowbird’s generic egg may result from a Jack-of-all-trades strategy; however, the evolutionary mechanisms that select for their generic eggs are unclear. Here we propose that the cowbird’s eggshell phenotypes have evolved via diffuse coevolution, which results from community-level selective pressures, rather than via pairwise coevolution that occurs between a particular host species and its brood parasite. Under diffuse coevolution the cowbird’s host community, with varying eggshell phenotypes and recognition abilities, would select for a cowbird eggshell phenotype intermediate to those of its host community. This selection is exerted by hosts that reject cowbird eggs, rather than those that accept them; therefore, we expect cowbird eggshell colors can be approximated by both the phenotypes and rejection abilities of their host community. Here we use eggshell reflectance data from 43 host species to demonstrate that the cowbird eggshell phenotypes are reasonably predicted (within 2 just noticeable differences) by the eggshell phenotypes and rejection rates of their hosts. These findings suggest that cowbird eggshell phenotypes, and potentially those of other some generalist parasites, may evolve via diffuse coevolution. Importantly, this research provides insight into the underlying evolutionary processes that explain observed phenotypic variation and provides a framework for studying selection on both specialist and generalist parasites' traits.

Epilogue

This epilogue summarizes key themes and presents some final thoughts. This book examined one of the most intriguing and central components of biodiversity: ecological interactions. The analysis has revealed some patterns in the structure of mutualistic networks that pervade their organization despite the variable environmental settings where they occur. Network theory describes an intermediate scenario to the extremes of highly specific one-on-one coevolution and largely intractable diffuse coevolution. Network theory also provides useful tools aimed at the identification of the key elements supporting these complex networks. Understanding the modular structure of the interaction networks is central to identifying the basic coevolutionary units.