Aphid Facultative Symbionts Aid Recovery of Their Obligate Symbiont and Their Host After Heat Stress

Abstract

Environmental conditions affect insect fitness, with many species constrained by specific temperature ranges. Aphids are limited to temperate climates and it is hypothesized that this is partly due to their heat-susceptible obligate nutritional symbiont Buchnera. Aphids often carry additional facultative symbionts which can increase the host's fitness after heat stress. Here we used the pea aphid (Acyrthosiphon pisum) and three of its facultative endosymbionts (Candidatus Regiella insecticola, Candidatus Fukatsuia symbiotica (X-type; PAXS), and Candidatus Hamiltonella defensa) to investigate how these species respond to heat stress and whether their presence affects the fitness of the host or the obligate symbiont. We exposed aphid lines to a single high temperature event and measured lifetime fecundity and population densities of both obligate and facultative symbionts. Heat shock reduced aphid fecundity, but for aphids infected with two of the facultative symbionts (Regiella or Fukatsuia), this reduction was less than in uninfected aphids. The population density of Buchnera was also reduced after heat shock, and only recovered in aphids infected with Regiella or Fukatsuia but not in uninfected aphids or those with Hamiltonella. Although heat shock initially reduced the densities of two of the facultative symbionts (Hamiltonella and Fukatsuia), all facultative symbiont densities recovered by adulthood. Two of the facultative symbionts tested therefore aided the recovery of the obligate symbiont and the host, and we discuss possible underlying mechanisms. Our work highlights the beneficial effects of protective symbionts on obligate symbiont recovery after heat stress and how facultative symbionts may affect the wider ecological community.

Does getting defensive get you anywhere?—Seasonal balancing selection, temperature, and parasitoids shape real‐world, protective endosymbiont dynamics in the pea aphid

“…Since Hamiltonella reached its highest frequency in 2012 right after a time exceeding the upper critical thermal limit for pea aphid development (Siddiqui et al, 1973), we find it fully plausible that this symbiont confers thermal tolerance under natural conditions. However, some pea aphid studies have found no evidence for thermal tolerance services of Hamiltonella (Heyworth et al, 2020), suggesting a need for further research and that, perhaps, our in-field temperature correlations were driven by baseline Hamiltonella benefits, with costs emerging only under cool temperatures. Accordingly, one Hamiltonella strain related to the Pennsylvania-enriched strain-A was found to drastically reduce the fitness of pea aphid clones under cooler temperatures (18°C) and short day lengths (Simon et al, 2011;Figure S2).…”

Effect of the Genotypic Variation of an Aphid Host on the Endosymbiont Associations in Natural Host Populations

“…Additionally, variations in the strength of protection against the fungal pathogen P. neoaphidis have also been observed among different endosymbiont strains of R. insecticola studied in two S. avenae clones [ 56 ]. Other endosymbiont-related functions have been recently suggested for heat stress by R. insecticola in the pea aphid [ 71 ], but such a protective effect differs from previous studies [ 59 , 72 ], suggesting that effects mediated by facultative endosymbionts can be dependent on symbiont and host genotypes or their interaction [ 71 ].…”

Dynamics of Insect–Microbiome Interaction Influence Host and Microbial Symbiont

“…However, this reduction is significantly less in aphids that are infected with either of the two facultative symbionts Regiella insecticola or Fukatsuia symbiotica. Moreover, it was observed that the reduced population density of the obligate symbiont, Buchnera, as a result of heat shock, could be successfully recovered in aphids infected with Regiella or Fukatsuia, but not in uninfected insects (Heyworth et al, 2020). Thus implying that sensitivity of Buchnera to heat shock, as a consequence of extreme gene loss, is compensated by the co-residing facultative symbionts.…”