Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts
Significance Symbiosis between animals and bacteria enables the exploitation of new ecological niches and promotes diversification. Many insects have obligate heritable bacteria that provision nutrients enabling new lifestyles, such as sap feeding. A model system for obligate symbiosis is the pea aphid and its heritable bacterial symbiont Buchnera aphidicola. Using this system, we address the extent of variation in host regulation of symbiont populations and find that pea aphids have extensive genetic variation in the ability to regulate Buchnera numbers. In addition, higher abundance of Buchnera is associated with lower reproductive rates in aphid hosts. Thus, we provide experimental evidence demonstrating that genetic variation in hosts affects regulation of symbiosis, suggesting fitness costs and potential negative consequences of obligate symbiosis. Symbiotic relationships promote biological diversification by unlocking new ecological niches. Over evolutionary time, hosts and symbionts often enter intimate and permanent relationships, which must be maintained and regulated for both lineages to persist. Many insect species harbor obligate, heritable symbiotic bacteria that provision essential nutrients and enable hosts to exploit niches that would otherwise be unavailable. Hosts must regulate symbiont population sizes, but optimal regulation may be affected by the need to respond to the ongoing evolution of symbionts, which experience high levels of genetic drift and potential selection for selfish traits. We address the extent of intraspecific variation in the regulation of a mutually obligate symbiosis, between the pea aphid (Acyrthosiphon pisum) and its maternally transmitted symbiont, Buchnera aphidicola. Using experimental crosses to identify effects of host genotypes, we measured symbiont titer, as the ratio of genomic copy numbers of symbiont and host, as well as developmental time and fecundity of hosts. We find a large >10 fold) range in symbiont titer among genetically distinct aphid lines harboring the same Buchnera haplotype. Aphid clones also vary in fitness, measured as developmental time and fecundity, and genetically based variation in titer is correlated with host fitness, with higher titers corresponding to lower reproductive rates of hosts. Our work shows that obligate symbiosis is not static but instead is subject to short term evolutionary dynamics, potentially reflecting coevolutionary interactions between host and symbiont.
Proceedings of the National Academy of Sciences