Similar cost of Hamiltonella defensa in experimental and natural aphid‐endosymbiont associations

Abstract

Endosymbiont‐conferred resistance to parasitoids is common in aphids, but comes at a cost to the host in the absence of parasitoids. In black bean aphids (Aphis fabae), costs in terms of reduced lifespan and lifetime reproduction were demonstrated by introducing 11 isolates of the protective symbiont Hamiltonella defensa into previously uninfected aphid clones. Transfection of H. defensa isolates into a common genetic background allows to compare the costs of different endosymbiont isolates unconfounded by host genetic variation, but has been suggested to overestimate the realized costs of the endosymbiont in natural populations, because transfection creates new and potentially maladapted host–symbiont combinations that would be eliminated by natural selection in the field. In this experiment, we show that removing H. defensa isolates from their natural host clones with antibiotics results in a fitness gain that is comparable to the fitness loss from their introduction into two new clones. This suggests that estimating cost by transfecting endosymbiont isolates into a shared host genotype does not lead to gross overestimates of their realized costs, at least not in the two recipient genotypes used here. By comparing our data with data reported in previous publications using the same lines, we show that symbiont‐induced costs may fluctuate over time. Thus, costs estimated after extended culture in the laboratory may not always be representative of the costs at the time of collection in the field. Finally, we report the accidental observation that two isolates from a distinct haplotype of H. defensa could not be removed by cefotaxime treatment, while all isolates from two other haplotypes were readily eliminated, which is suggestive of variation in susceptibility to this antibiotic in H. defensa.

Physiological costs of facultative endosymbionts in aphids assessed from energy metabolism

“…Despite the establishment and maintenance of the lines used in this study for several years in the laboratory, they are representative of the preferential associations between the clover biotype of A. pisum and the endosymbiont R. insecticola , as well as the association between the alfalfa biotype and H. defensa commonly found in natural populations of A. pisum in various countries (Ferrari et al, 2012; Russell et al, 2013; Simon et al, 2003) and over years (Leclair et al, 2021; Smith et al, 2015). However, it has been recently highlighted that symbiont‐associated fitness costs can fluctuate through long‐time period in laboratory culture putatively due to variations in symbiont densities (Kaech et al, 2022), suggesting that our results may under‐ or over‐estimate symbiont‐associated fitness costs of current natural populations depending on changes in symbiont population sizes since collection.…”

“…However, it has been recently highlighted that symbiont-associated fitness costs can fluctuate through long-time period in laboratory culture putatively due to variations in symbiont densities (Kaech et al, 2022), suggesting that our results may under-or over-estimate symbiont-associated fitness costs of current natural populations depending on changes in symbiont population sizes since collection.…”

Facultative symbionts are potential agents of symbiont-mediated RNAi in aphids

“…Furthermore, the protections conferred by facultative symbionts are costly. In the absence of stresses, these infections decrease aphid fitness ( Gwynn et al, 2005 ; Vorburger, 2013 ; Kaech et al, 2022 ), hence, there exists a trade-off between the costs and benefits of facultative symbionts to aphids.…”

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).…”