Heritable microbes represent an important component of the biology, ecology and evolution of many plants, animals and fungi, acting as both parasites and partners. In this review, we examine how heritable symbiont-host interactions may alter host thermal tolerance, and how the dynamics of these interactions may more generally be altered by thermal environment. Obligate symbionts, those required by their host, are considered to represent a thermally sensitive weak point for their host, associated with accumulation of deleterious mutations. As such, these symbionts may represent an important determinant of host thermal envelope and spatial distribution. We then examine the varied relationship between thermal environment and the frequency of facultative symbionts that provide ecologically contingent benefits or act as parasites. We note that some facultative symbionts directly alter host thermotolerance. We outline how thermal environment will alter the benefits/costs of infection more widely, and additionally modulate vertical transmission efficiency. Multiple patterns are observed, with symbionts being cold sensitive in some species and heat sensitive in others, with varying and non-coincident thresholds at which phenotype and transmission are ablated. Nevertheless, it is clear that studies aiming to predict ecological and evolutionary dynamics of symbiont-host interactions need to examine the interaction across a range of thermal environments. Finally, we discuss the importance of thermal sensitivity in predicting the success/failure of symbionts to spread into novel species following natural/engineered introduction.

Ecologically important traits of insects are often affected by facultative bacterial endosymbionts. This is best studied in the pea aphid Acyrthosiphon pisum, which is frequently infected by one or more of eight facultative symbiont species. Many of these symbiont species have been shown to provide one ecological benefit, but we have little understanding of the range of effects that a single strain can have. Here, we describe the phenotypes conferred by three strains of the recently discovered bacterium known as X‐type (Enterobacteriaceae), each in their original aphid genotype which also carries a Spiroplasma symbiont. All comparisons are made between aphids that are coinfected with Spiroplasma and X‐type and aphids of the same genotype that harbour only Spiroplasma. We show that in all cases, infection with X‐type protects aphids from the lethal fungal pathogen Pandora neoaphidis, and in two cases, resistance to the parasitoid Aphidius ervi also increases. X‐type can additionally affect aphid stress responses – the presence of X‐type increased reproduction after the aphids were heat‐stressed. Two of the three strains of X‐type are able to provide all of these benefits. Under benign conditions, the aphids tended to suffer from reduced fecundity when harbouring X‐type, a mechanism that might maintain intermediate frequencies in field populations. These findings highlight that a single strain of a facultative endosymbiont has the potential to provide diverse benefits to its aphid host.

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.

Many insects carry facultative bacterial symbionts, which provide benefits including resistance to natural enemies and abiotic stresses. Little is known about how these beneficial phenotypes are affected when biotic or abiotic threats occur simultaneously. The pea aphid (Acyrthosiphon pisum) can host several well-characterized symbiont species. The symbiont known as X-type can protect against both parasitoid wasps and heat stress. Here, we used three pea aphid genotypes that were naturally infected with X-type and the symbiont Spiroplasma sp. We compared aphids coinfected with these two symbionts with those cured from X-type and infected with only Spiroplasma to investigate the ability of X-type to confer benefits to the host when two threats are experienced simultaneously. Our aim is to explore how robust symbiont protection may be outside a benign laboratory environment. Aphids were subjected to heat shock either before or after attack by parasitoid wasps. Under a benign temperature regime, the aphids carrying X-type tended to be better protected from the parasitoid than those cured. When the aphids experienced a heat shock before being parasitized aphids carrying X-type were more susceptible than those cured. Regardless of infection with the symbiont, the aphids benefitted from being heat shocked after parasitization. The results demonstrate how resistance to parasitoid wasps can be strongly environment-dependent and that a beneficial phenotype conferred by a symbiont under controlled conditions in the laboratory does not necessarily equate to a consistently useful effect in natural populations.

Heteroplasmy is the coexistence of more than one type of mitochondria in an organism. Although widespread sequencing has identified several cases of transient or low-level heteroplasmy that primarily occur through mutation or paternal leakage, stable, high-titer heteroplasmy remains rare in animals. In this study we present a unique, stable and high-level heteroplasmy in male and female flies belonging to the neotropical Drosophila paulistorum species complex. We show that mitochondria of D. paulistorum are polyphyletic and form two clades, α and β, with two subclades each. Mitochondria of the α2 subclade appear functional based on their genomic integrity but are exclusively found in heteroplasmic flies and never in homoplasmy, suggesting that they are a secondary mitotype with distinct functionality from the primary mitochondria. Using qPCR, we show that α2 titer do not respond to energetic demands of the cell and are generally higher in males than females. By crossing hetero- and homoplasmic flies, we find that α2 can be transmitted to their offspring via both parents and that levels are dependent on nuclear background. Following α2 mitotype levels during embryogenesis, we demonstrate that this secondary mitotype replicates rapidly just after fertilization of the egg in a period when primary mitochondria are dormant. This so-called “Replication precox” mitochondrial phenotype likely prevents the α2 mitotype from being outcompeted by the primary mitotype – and thereby secures its persistence and further spread as a selfish mitochondrion, we hereby designate “Spartacus”. Finally, we reconstruct the evolutionary history of mitochondria in the willistoni subgroup uncovering signs of multiple mitochondrial losses and introgressions. Our data indicate an α-like mitochondrial ancestor in the willistoni subgroup, with the β mitotype likely acquired via introgression from an unidentified donor. We hypothesize that the selfish characteristics of α2 might have emerged as a response to competition for inheritance with the introgressed β mitotype.