Physiological costs of facultative endosymbionts in aphids assessed from energy metabolism

Abstract Many insect species harbour heritable bacterial endosymbionts. Some facultative endosymbionts provide benefits to their hosts under certain environmental conditions. Facultative endosymbionts are expected to impose additional energetic expenditures to their host, reducing host fitness. While there is accumulating evidence in plant sucking insects that facultative endosymbionts reduce the fitness of their host under permissive conditions, no direct energy costs associated with facultative endosymbionts have been identified. Using the standard metabolic rate (SMR) as a measure of the energy cost of self‐maintenance, we investigated whether two common facultative endosymbionts Hamiltonella defensa or Regiella insecticola increase the maintenance cost of the pea aphid Acyrthosiphon pisum which could translate into host fitness reduction (‘compensation hypothesis’). In addition, we tested if there was a link between SMR and the aphid fitness and whether it depended on endosymbiont density and aphid energetic reserves. Finally, we measured SMR at different temperatures to assess the impact of suboptimal thermal conditions on physiological cost of endosymbionts. In the presence of facultative endosymbionts, aphids expressed generally a lower fitness and a higher SMR compared to uninfected ones, in accordance with the ‘compensation hypothesis’. However, the SMR difference between infected and uninfected aphids tended to decrease with increasing temperature. Complex host genotype‐by‐symbiont genotype‐by‐temperature interactions on SMR were also revealed. Energetic budget of adult aphids appeared weakly influenced by the aphid genotype and endosymbiont species, suggesting that facultative endosymbionts primarily impact the consumption of energy resources rather than their acquisition. Density of facultative endosymbionts varied largely among aphid lines but was not associated with the fitness nor metabolic rate of aphids. This work supports the energy basis of facultative endosymbiont associated fitness costs and raises new questions about the effect of facultative endosymbionts on the energy metabolism of their host. Read the free Plain Language Summary for this article on the Journal blog.