Abstract
Defences against parasites are typically associated with costs to the host that contribute to the maintenance of variation in resistance. This also applies to the defence provided by the facultative bacterial endosymbiont Hamiltonella defensa, which protects its aphid hosts against parasitoid wasps while imposing life-history costs. To investigate the cost–benefit relationship within protected hosts, we introduced multiple isolates of H. defensa to the same genetic backgrounds of black bean aphids, Aphis fabae, and we quantified the protection against their parasitoid Lysiphlebus fabarum as well as the costs to the host (reduced lifespan and reproduction) in the absence of parasitoids. Surprisingly, we observed the opposite of a trade-off. Strongly protective isolates of H. defensa reduced lifespan and lifetime reproduction of unparasitized aphids to a lesser extent than weakly protective isolates. This finding has important implications for the evolution of defensive symbiosis and highlights the need for a better understanding of how strain variation in protective symbionts is maintained.
Highlights
Life-history costs associated with defences against parasites are well documented [1], and represent a key determinant of host–parasite coevolutionary processes and population dynamics [2,3,4]
Our experiment confirmed that in black bean aphids, the strength of protection provided by different isolates of the facultative symbiont H. defensa depends on the genotype of the attacking parasitoid
Genotype-by-genotype interactions on the outcome of infection are a common observation in host–parasite systems [39,40], but notably, in the present case, they are driven by a genetic interaction between the parasitoid and the host’s heritable endosymbiont rather than the host itself [16,22,34]
Summary
Life-history costs associated with defences against parasites are well documented [1], and represent a key determinant of host–parasite coevolutionary processes and population dynamics [2,3,4]. We compared the effects of 11 different isolates of H. defensa on resistance to parasitoids and aphid life-history traits These isolates were obtained from 11 different field-collected clones of A. fabae harbouring natural infections with this symbiont. One aphid nymph was removed from each of eight colonies of all 24 aphid sublines (three from the first two experimental blocks, two from the third block), yielding 192 nymphs in total These nymphs were transferred singly to new plants and used to measure three life-history traits: weight at adulthood, lifespan and total lifetime reproduction. To detect possible relationships between protection and costs to the host conferred by the different H. defensa isolates, we calculated Pearson correlations between life-history traits and rates of parasitism averaged across aphid genotypes and parasitoid lines. Linear models were used to test for the effects of aphid genotype, symbiont isolate (or symbiont haplotype—see Results) and their interactions on relative symbiont density (symbiont gene copy number divided by aphid gene copy number)
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