Physiological costs of facultative endosymbionts in aphids assessed from energy metabolism

Abstract

1. Many insect species harbour heritable bacterial endosymbionts. Some facultative endosymbionts provide benefits to their hosts under certain environmental conditions.2. 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.3. Using the standard metabolic rate (SMR) as a measure of the energy cost of selfmaintenance, 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.4. 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.5. 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.

A rapidly spreading deleterious aphid endosymbiont that uses horizontal as well as vertical transmission

“…Unlike in species that normally reproduce sexually, endosymbionts in aphids cannot spread by mechanisms such as cytoplasmic incompatibility, which can drive an invasion by the endosymbiont despite fitness costs ( 55 ). Facultative endosymbionts typically have physiological costs ( 34 , 56 , 57 ), which makes invasion difficult in species that predominantly reproduce via parthenogenesis, unless there are context-specific fitness benefits ( 17 , 58 ).…”

Wolbachia improves the performance of an invasive fly after a diet shift

“…Depending on speci c host fruit availability and quality, Wolbachia presence could be more or less advantageous to D. suzukii. Wolbachia presence is also associated with cost that can offset the bene ts, such as costs related to the energy needed to host the endosymbiont (Clavé et al 2022). Further studies are required to investigate how the cost-bene ce balance is modulated in a multitrophic context, depending on the host plants.…”

Aphid populations are frequently infected with facultative endosymbionts

“…These endosymbionts can have a wide range of effects on their hosts, from protection against heat stress and parasitoid wasps, to adaptations to specific host‐plant species, to changing their host's body colour (Oliver et al, 2008; Rothacher et al, 2016). Endosymbionts can also be costly to maintain and have negative effects on their hosts, such as a shorter lifespan or lower lifetime reproduction (Clavé et al, 2022; Kaech et al, 2022).…”