Breakdown of a defensive symbiosis, but not endogenous defences, at elevated temperatures

Abstract

Environmental factors, including temperature, can have large effects on species interactions, including mutualisms and antagonisms. Most insect species are infected with heritable bacterial symbionts with many protecting their hosts from natural enemies. However, many symbionts or their products are thermally sensitive; hence, their effectiveness may vary across a range of temperatures. In the pea aphid, Acyrthosiphon pisum, the bacterial symbiont Hamiltonella defensa and its associated APSE bacteriophages confer resistance to this aphid's dominant parasitoid, Aphidius ervi. Here, we investigate the effects of temperature on both endogenous and symbiont-based protection against this parasitoid. We also explored the defensive properties of the X-type symbiont, a bacterium hypothesized to shape aphid defence when co-occurring with H. defensa. We show that H. defensa protection fails at higher temperatures, although some aphid genotype and H. defensa strain combinations are more robust than others at moderately warmer temperatures. We also found that a single X-type strain neither defended against parasitism by A. ervi nor rescued lost H. defensa protection at higher temperatures. In contrast, endogenous aphid resistance was effective across temperatures, revealing that these distinct defensive modes are not equally robust to changing environments. Through a survey of field-collected pea aphids, we found a negative correlation between H. defensa frequencies and average daily temperatures across North American locales, fitting expectations for reduced symbiont benefits under warm climates. Based on these findings, we propose that rising global temperatures could promote the widespread breakdown of defensive mutualisms, a prospect with implications for both human and ecosystem health.

The protector within: Comparative genomics of APSE phages across aphids reveals rampant recombination and diverse toxin arsenals

“…Facultative symbionts in insects can confer conditional fitness benefits to their hosts (Cass et al, 2016;Doremus et al, 2018;Polin et al, 2015), and H. defensa and its APSE-conferred defence against parasitoid wasps is one of the best studied cases (Oliver and Higashi, 2019). The results presented in this study support previous studies reporting a variable toxin cassette across APSE as well as intra-genic recombination.…”

Context‐dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum

“…It should be briefly noted that frequent associations between Hamiltonella and X‐type have unclear implications. While European X‐type strains modulate a variety of phenotypes under co‐infection with Spiroplasma (Heyworth & Ferrari, ), examinations of one strain from North America ruled out antiparasitoid defence, rescue of impaired Hamiltonella protection, antifungal defence and thermotolerance (Doremus & Oliver, ; Doremus et al., ), suggesting a need for further study. Also important here—beyond the fact that related strains from a given HFS species may vary in their protective capacities (Łukasik, Guo, et al., )—is that effective protection may require specific combinations of symbiont and enemy genotypes (Cayetano, Rothacher, Simon, & Vorburger, ), and that defence against enemies may be environmentally sensitive (Doremus et al., ).…”

Introduction: The host‐associated microbiome: Pattern, process and function

“…Results showed that both aphid and symbiont genotype can govern the efficacy of defence across temperatures. Most consistent, however, was the failure of symbiont defence at moderately warm temperatures frequently encountered in the field (Doremus et al., ). Consistent with these experimental findings, the protective symbionts ( Hamiltonella defensa ) were less common in warm locales across North America.…”