Aphid Thermal Tolerance Is Governed by a Point Mutation in Bacterial Symbionts

Abstract

Symbiosis is a ubiquitous phenomenon generating biological complexity, affecting adaptation, and expanding ecological capabilities. However, symbionts, which can be subject to genetic limitations such as clonality and genomic degradation, also impose constraints on hosts. A model of obligate symbiosis is that between aphids and the bacterium Buchnera aphidicola, which supplies essential nutrients. We report a mutation in Buchnera of the aphid Acyrthosiphon pisum that recurs in laboratory lines and occurs in field populations. This single nucleotide deletion affects a homopolymeric run within the heat-shock transcriptional promoter for ibpA, encoding a small heat-shock protein. This Buchnera mutation virtually eliminates the transcriptional response of ibpA to heat stress and lowers its expression even at cool or moderate temperatures. Furthermore, this symbiont mutation dramatically affects host fitness in a manner dependent on thermal environment. Following a short heat exposure as juveniles, aphids bearing short-allele symbionts produced few or no progeny and contained almost no Buchnera, in contrast to aphids bearing symbionts without the deletion. Conversely, under constant cool conditions, aphids containing symbionts with the short allele reproduced earlier and maintained higher reproductive rates. The short allele has appreciable frequencies in field populations (up to 20%), further supporting the view that lowering of ibpA expression improves host fitness under some conditions. This recurring Buchnera mutation governs thermal tolerance of aphid hosts. Other cases in which symbiont microevolution has a major effect on host ecological tolerance are likely to be widespread because of the high mutation rates of symbiotic bacteria and their crucial roles in host metabolism and development. Aphids are sap-feeding insects that depend on obligate bacterial symbionts of the genus Buchnera for biosynthesis of needed nutrients. Studying Buchnera gene expression in pea aphids, we identified a recurring mutation (a single-base deletion) in the transcriptional promoter of the small heat-shock protein, ibpA. This mutation arose and was fixed twice in sublines derived from a single female aphid in the lab and kept at constant 20 °C. Experiments using aphid lines that differed only in the presence of this Buchnera mutation revealed that it eliminates the ibpA transcriptional response to heat shock and affects ibpA expression at low temperatures. In aphids containing Buchnera with the mutation, a short heat treatment as juveniles leads to elimination of most or all symbionts and to reproductive failure; the same treatment has little effect on aphids containing Buchnera without the mutation. Conversely, at constant lower temperatures, aphids with Buchnera bearing this mutation enjoy a reproductive advantage. Pea aphid populations are polymorphic for the Buchnera mutation, suggesting that it is maintained at substantial frequencies by selection. This study indicates that mutations in obligate symbionts can have major consequences for host fitness and geographic distributions.