Evolutionary consequences of loss of sexual reproduction on male-related traits in parthenogenetic lineages of the pea aphid.

Transition from sexual reproduction to parthenogenesis constitutes a major life-history change with deep evolutionary consequences for sex-related traits, which are expected to decay. The pea aphid Acyrthosiphon pisum shows intraspecific reproductive polymorphism, with cold-resistant cyclically parthenogenetic (CP) lineages that alternate sexual and asexual generations and cold-sensitive obligately parthenogenetic (OP) lineages that produce only asexual females but still males. Here, the genotyping of 219 pea aphid lineages collected in cold-winter and mild-winter regions revealed contrasting population structures. Samples from cold-winter regions consisted mostly of distinct multilocus genotypes (MLGs) usually represented by a single sample (101 different MLGs for 111 samples) and were all phenotyped as CP. In contrast, fewer MLGs were found in mild-winter regions (28 MLGs for 108 samples), all but one being OP. Since the males produced by OP lineages are unlikely to pass on their genes (sexual females being rare in mild-winter regions), we tested the hypothesis that their traits could degenerate due to lack of selection by comparing male production and male reproductive success between OP and CP lineages. Male production was indeed reduced in OP lineages, but a less clear pattern was observed for male reproductive success: females mated with OP males laid fewer eggs (fertilized or not) but OP and CP males fertilized the same proportion of eggs. These differences may stem from the type of selective forces: male production may be counter-selected whereas male performances may evolve under the slower process of relaxed selection. The overall effective reproductive capacity of OP males could result from recent sex loss in OP lineages or underestimated reproductive opportunities.

A major-effect genetic locus, ApRVII, controlling resistance against both adapted and non-adapted aphid biotypes in pea.

KEY MESSAGE: A genome-wide association study for pea resistance against a pea-adapted biotype and a non-adapted biotype of the aphid, Acyrthosiphon pisum, identified a genomic region conferring resistance to both biotypes. In a context of reduced insecticide use, the development of cultivars resistant to insect pests is crucial for an integrated pest management. Pea (Pisum sativum) is a crop of major importance among cultivated legumes, for the supply of dietary proteins and nitrogen in low-input cropping systems. However, yields of the pea crop have become unstable due to plant parasites. The pea aphid (Acyrthosiphon pisum) is an insect pest species forming a complex of biotypes, each one adapted to feed on one or a few related legume species. This study aimed to identify resistance to A. pisum and the underlying genetic determinism by examining a collection of 240 pea genotypes. The collection was screened against a pea-adapted biotype and a non-adapted biotype of A. pisum to characterize their resistant phenotype. Partial resistance was observed in some pea genotypes exposed to the pea-adapted biotype. Many pea genotypes were completely resistant to non-adapted biotype, but some exhibited partial susceptibility. A genome-wide association study, using pea exome-capture sequencing data, enabled the identification of the major-effect quantitative trait locus ApRVII on the chromosome 7. ApRVII includes linkage disequilibrium blocks significantly associated with resistance to one or both of the two aphid biotypes studied. Finally, we identified candidate genes underlying ApRVII that are potentially involved in plant-aphid interactions and marker haplotypes linked with aphid resistance. This study sets the ground for the functional characterization of molecular pathways involved in pea defence to the aphids but also is a step forward for breeding aphid-resistant cultivars.