Thermal sensitivity of theSpiroplasma-Drosophila hydeiprotective symbiosis: The best of climes, the worst of climes

Abstract

The outcome of natural enemy attack in insects has commonly been found to be influenced by the presence of protective symbionts in the host. The degree to which protection functions in natural populations, however, will depend on the robustness of the phenotype to variation in the abiotic environment. We studied the impact of a key environmental parameter – temperature – on the efficacy of the protective effect of the symbiont Spiroplasma on its host Drosophila hydei, against attack by the parasitoid wasp Leptopilina heterotoma. In addition, we investigated the thermal sensitivity of the symbiont’s vertical transmission, which may be a key determinant of the ability of the symbiont to persist. We found that vertical transmission was more robust than previously considered, with Spiroplasma being maintained at 25 °C, 18 °C and with 18/15 °C diurnal cycles, with rates of segregational loss only increasing at 15 °C. Protection against wasp attack was ablated before symbiont transmission was lost, with the symbiont failing to rescue the fly host at 18 °C. We conclude that the presence of a protective symbiosis in natural populations cannot be simply inferred from presence of a symbiont whose protective capacity has been tested under narrow controlled conditions. More broadly, we argue that the thermal environment is likely to represent an important determinant of the evolutionary ecology of defensive symbioses in natural environments, potentially driving seasonal, latitudinal and altitudinal variation in symbiont frequency, and modulating the strength of selection for symbiotic protective systems compared to defensive systems encoded in the nuclear genomes.

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

“…In the pea aphid, H. defensa-mediated protection against A. ervi has been repeatedly shown to be negatively impacted, or fail, at warmer temperatures relative to cooler controls, with even a modest temperature rise of 2.5°C enough to reduce the strength of H. defensa-mediated protection (Bensadia et al, 2006;Doremus et al, 2018;Higashi et al, 2020). In contrast to the studies above, Spiroplasma-mediated protection against Leptopilina heterotoma in Drosophila hydei completely failed at a cooler temperature of 18°C compared to 25°C (Corbin et al, 2021).…”

“…The outcome of natural enemy attack in insects can be modulated by the presence of defensive heritable symbionts residing within the host. Beyond symbiont presence, studies have shown that genetic and environmental factors can also mediate the outcome of symbiont-mediated defence (Doremus et al, 2018;Vorburger and Perlman, 2018;Corbin et al, 2021;Chrostek et al, 2021).…”

Impact of heat stress on the fitness outcomes of symbiotic infection in aphids: a meta-analysis

“…Hamiltonella defensa in aphids and Spiroplasma sp. in drosophilids [27,28,30]) or viruses (e.g. Wolbachia sp.…”

The Microbiome and Mosquito Vectorial Capacity: Rich Potential for Discovery and Translation

“…In mosquitoes, 40 the microbiome, which consists of bacteria, viruses and fungi, profoundly alters host phenotypes. Acquisition and the composition of the microbiome is influenced by several abiotic and biotic factors, including host and microbial genetics [1][2][3][4] and the environment [5][6][7]. Therefore microbiomes of mosquitoes can vary substantially between individuals, life stages, species, and over geographical space [8,9], and this variation likely contributes to differences in host phenotypes.…”