Abstract

Heritable symbionts play an essential role in many aspects of host ecology in a temperature-dependent manner. However, how temperature impacts the host and their interaction with endosymbionts remains largely unknown. Here, we investigated the impact of moderate (20°C) and high (30 and 35°C) temperatures on symbioses between the spider mite Tetranychus truncatus and two maternally inherited endosymbionts (Wolbachia and Spiroplasma). We found that the thermal tolerance of mites (as measured by survival after heat exposure) was lower for mites that were singly infected with either Wolbachia or Spiroplasma than it was for co-infected or uninfected mites. Although a relatively high temperature (30°C) is thought to promote bacterial replication, rearing at high temperature (35°C) resulted in losses of Wolbachia and particularly Spiroplasma. Exposing the mites to 20°C reduced the density and transmission of Spiroplasma but not Wolbachia. The four spider mite strains tested differed in the numbers of heat shock genes (Hsps) induced under moderate or high temperature exposure. In thermal preference (Tp) assays, the two Wolbachia-infected spider mite strains preferred a lower temperature than strains without Wolbachia. Our results show that endosymbiont-mediated spider mite responses to temperature stress are complex, involving a combination of changing endosymbiont infection patterns, altered thermoregulatory behavior, and transcription responses.

Highlights

  • Temperature has a substantial impact on a wide range of ecologically important traits in many ectothermic organisms (Colinet et al, 2015; Sgro et al, 2016; Ma et al, 2021) and their symbiotic microbiota (Kiers et al, 2010)

  • When the four mite strains were reared at 30 and 35◦C, the female survival rate after 5 days was sharply lower in the singly infected strains than in the co-infected and uninfected strains (Figure 1). These results indicate that spider mites singly infected with Wolbachia or Spiroplasma are sensitive to high temperatures

  • The prevalence of Spiroplasma in singly infected strains decreased from 90.8% in the F1s to 55.8% in the F2s, while the prevalence of Spiroplasma in co-infested strains fluctuated across the four generations (Figures 4C,D). These results suggest that high temperature reduces vertical transmission efficiency of Wolbachia or Spiroplasma in all spider mite strains with varying degrees, and Spiroplasma is more sensitive to high temperatures than Wolbachia

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Summary

Introduction

Temperature has a substantial impact on a wide range of ecologically important traits in many ectothermic organisms (Colinet et al, 2015; Sgro et al, 2016; Ma et al, 2021) and their symbiotic microbiota (Kiers et al, 2010). Heritable bacterial symbionts, which are pervasive in many arthropods, affect the host’s response to abiotic stressors, including temperature (Lemoine et al, 2020). Bacterial endosymbionts can both mediate and constrain host adaptation to temperature. The obligate bacterial endosymbiont, Buchnera, limits the thermal tolerance of its aphid hosts and represents an “Achilles’ heel” of their thermal response (Dunbar et al, 2007; Zhang et al, 2019), while the facultative endosymbiont Serratia symbiotica increases aphid survival or reproduction under heat exposure likely through releasing metabolites (Montllor et al, 2002; Burke et al, 2010). Thermal effects mediated by symbionts may affect host distribution as well as responses to ongoing changing climate

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