Abstract

Insect hosts and parasitoids are engaged in an intense struggle of antagonistic coevolution. Infection with heritable bacterial endosymbionts can substantially increase the resistance of aphids to parasitoid wasps, which exerts selection on parasitoids to overcome this symbiont-conferred protection (counteradaptation). Experimental evolution in the laboratory has produced counteradapted populations of the parasitoid wasp Lysiphlebus fabarum. These populations can parasitize black bean aphids (Aphis fabae) protected by the bacterial endosymbiont Hamiltonella defensa, which confers high resistance against L. fabarum. We used two experimentally evolved parasitoid populations to study the genetic architecture of the counteradaptation to symbiont-conferred resistance by QTL analysis. With simple crossing experiments, we showed that the counteradaptation is a recessive trait depending on the maternal genotype. Based on these results, we designed a customized crossing scheme to genotype a mapping population phenotyped for the ability to parasitize Hamiltonella-protected aphids. Using 1835 SNP markers obtained by ddRAD sequencing, we constructed a high-density linkage map consisting of six linkage groups (LGs) with an overall length of 828.3 cM and an average marker spacing of 0.45 cM. We identified a single QTL associated with the counteradaptation to Hamiltonella in L. fabarum on linkage group 2. Out of 120 genes located in this QTL, several genes encoding putative venoms may represent candidates for counteradaptation, as parasitoid wasps inject venoms into their hosts during oviposition.

Highlights

  • Interactions between organisms are important drivers of evolution

  • The fact that female offspring are only produced in crosses with R mothers is in line with H3, suggesting that counteradaptation is governed by the maternal genotype (Table 1)

  • This study represents the first attempt to investigate the genomic basis of the counteradaptation to symbiontconferred resistance in aphid parasitoids with a quantitative trait locus (QTL) approach

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Summary

Introduction

Host–parasite interactions represent intimate relationships between species (Windsor 1998). The reciprocal adaptation in host–parasite coevolution becomes mediated by symbionts (reviewed in Vorburger and Perlman 2018). For these adaptive changes to happen, genetic variation is required in both parasite and host populations. The advent of next-generation sequencing combined with laboratory-based experiments manipulating host–parasite systems has allowed to investigate this genetic diversity and address the genomic basis underpinning the mechanisms of coevolution (Schlötterer et al 2015)

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