History matters: thermal environment before, but not during wasp attack determines the efficiency of symbiont-mediated protection

Abstract

The outcome of natural enemy attack in insects is commonly impacted by the presence of defensive microbial symbionts residing within the host. Beyond their presence, the outcome of the interaction can also depend on genetic and environmental factors. The thermal environment is a key factor known to affect symbiont-mediated traits in insects, including their ability to defend against natural enemy attack. Cooler temperatures, for instance, have been previously shown to reduce Spiroplasma-mediated protection in Drosophila. Here, we dissect the effect of the thermal environment on Spiroplasma-mediated protection against Leptopilina boulardi in Drosophila melanogaster by examining the effect of temperature before, during and after wasp attack on fly survival and wasp success. We observed that the developmental temperature of the mothers' of attacked larvae, and not the temperature of the attacked larvae themselves during or after wasp attack, strongly determines the protective influence of Spiroplasma. Spiroplasma-mediated fly survival was found to be weaker when parental flies were reared at 21 C before their larvae were exposed to wasps compared to larvae derived from parental flies reared at 23 C or 25 C. Contrastingly, there was no effect of thermal environment on protection when mothers were reared at 25 C, and their progeny exposed to lower temperatures during and after wasp attack. The effect of developmental temperature on Spiroplasma-mediated protection is likely mediated by reduced Spiroplasma titre combined, at cooler temperatures, with segregation of infection. These results indicate the historical thermal environment is a stronger determinant of protection than current environment, and that protective capacity is partly an epigenetic trait.

Ecological histories determine the success of social exploitation

“…Both in pairs of a cooperation-proficient lab reference strain of M. xanthus and multiple cheater strains, and in pairs of natural isolates with only short histories of lab cultivation, the pre-development resource-level history of codeveloping strains is found to strongly affect social fitness during sporulation. An abiotic ecological gradient changes the character of exploitative social interactions in microbes, just as abiotic gradients can alter interspecific interactions (Friede et al 2016;Johnson et al 1997;Jones & Hurst 2023). For three of five strain pairs examined, low-resource growth by one or both strains in the pair eliminated a clear exploitative interaction observed when both strains were grown with high resources.…”

“…Species' ecological histories can impact the outcomes of their interaction (Grigaltchik et al 2012), in magnitude or even sign. For example, thermal histories can modify host-parasite-interaction phenotypes, such as when the degree to which Spiroplasma bacterial symbionts protect Drosophila melanogaster larvae from wasp attack is determined by the temperature at which the mother flies had previously developed, and not by the temperature at the time of wasp-larvae interaction (Jones & Hurst 2023). In predator-prey interactions between distinct species of bacteria, the very direction of predation can reverse as a function of the temperature at which one of the parties grew before the interaction (Vasse et al 2023).…”

“…However, the fitness of cooperators relative to defectors may also be impacted by prior ecological conditions. Ecological histories are known to influence a variety of inter-specific interactions (Grigaltchik et al 2012;Jones & Hurst 2023;Mcghee et al 2012) and may also influence the social fitness of microbes. The plausibility of this hypothesis is illustrated by experiments with the social amoeba Dictyostelium discoideum, which develops into spore-bearing fruiting bodies in response to starvation.…”

“…Ecological histories are known to influence a variety of inter-specific interactions (Grigaltchik et al . 2012; Jones & Hurst 2023; Mcghee et al . 2012) and may also influence the social fitness of microbes.…”

Warm temperature inhibits cytoplasmic incompatibility induced by endosymbiotic Rickettsiella in a spider host

“…Consequently, caution should be used when extrapolating inferences from Wolbachia CI studies to other bacterial symbionts. There is growing evidence that symbiont-induced host phenotypes, such as CI, can be thermally sensitive but potentially idiosyncratic (Corbin et al 2017, Doremus et al 2019, Shropshire et al 2020, Corbin et al 2021, Hague et al 2022, Jones et al 2023, Martins et al 2023. The effect of temperature on Rickettsiella-induced CI has not previously been investigated, but in a non-CI-inducing Rickettsiella strain in aphids, temperature affects Rickettsiella titer, host phenotype, and spread in the host population (Gu et al PNAS 2023).…”