International audience1. The pea aphid, Acyrthosiphon pisum Harris, constitutes a complex of sympatric populations that are specialised to distinct species of Fabaceae. So far, 12 such populations have been characterised genetically as genetic clusters associated with one or few legumes species. These clusters form a continuum of genetic divergence linking host-associated races, which show moderate hybridization, to nascent species. They are also known to be associated with different species of endosymbiotic bacteria, which have environmentally dependent effects on aphid fitness2. Here, we report on the genetic characterisation of new host-associated populations in this species complex. We sampled pea aphids in eastern France on Genista tinctoria, G. sagittalis, Onobrychis viciifolia, and Hippocrepis comosa. Bayesian clustering methods based on genotypes obtained at 25 microsatellite loci showed that each sampled plant species hosted a specific pea aphid population. Comparison with previously characterised biotypes showed that the population associated with Hippocrepis comosa was no different from that on Securigera varia. Migrant aphids from other host plants and hybrids were found at various frequencies on the newly sampled plant species. They were particularly frequent on Onobrychis viciifolia, occasional between the two Genista-associated populations, and rare on Hippocrepis comosa.3. PCR-based screening of bacterial species revealed new associations between aphid biotypes and facultative endosymbionts, chiefly the combination of Serratia symbiotica and Hamiltonella defensa within most individuals collected on Genista.4. The newly identified biotypes, which add up to a total of 15 within the pea aphid complex, offer new material to study the mechanisms and genetic bases of host-specialisation and ecological speciation in this model aphid

Linking adaptive divergence to hybrid unfitness is necessary to understand the ecological factors contributing to reproductive isolation and speciation. To date, this link has been demonstrated in few model systems, most of which encompass ecotypes that occupy relatively early stages in the speciation process. Here we extend these studies by assessing how host-plant adaptation conditions hybrid fitness in the pea aphid, Acyrthosiphon pisum. We made crosses between and within five pea aphid biotypes adapted to different host plants and representing various stages of divergence within the complex. Performance of F1 hybrids and nonhybrids was assessed on a "universal" host that is favorable to all pea aphid biotypes in laboratory conditions. Although hybrids performed equally well as nonhybrids on the universal host, their performance was much lower than nonhybrids on the natural hosts of their parental populations. Hence, hybrids, rather than being intrinsically deficient, are maladapted to their parents' hosts. Interestingly, the impact of this maladaptation was stronger in certain hybrids from crosses involving the most divergent biotype, suggesting that host-dependent postzygotic isolation has continued to evolve late in divergence. Even though host-independent deficiencies are not excluded, hybrid maladaptation to parental hosts supports the hypothesis of ecological speciation in this complex.

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