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.

Although asexual linages evolved from sexual lineages in many different taxa, the genetics of sex loss remains poorly understood. We addressed this issue in the pea aphid Acyrthosiphon pisum, whose natural populations encompass lineages performing cyclical parthenogenesis (CP) and producing one sexual generation per year, as well as obligate parthenogenetic (OP) lineages that can no longer produce sexual females but can still produce males. A SNP-based, whole-genome scan of CP and OP populations sequenced in pools (103 individuals from six populations) showed that a single X-linked region controls the variation in reproductive mode. This 840-kb region is highly divergent between CP and OP populations (FST = 34.9%), with >2000 SNPs or short Indels showing a high degree of association with the phenotypic trait. Comparison of de novo genome assemblies built from long reads did not reveal large structural rearrangements between CP and OP lineages within the candidate region. This reproductive polymorphism still appears relatively ancient, as we estimated its age at ~0.25 million years from the divergence between cp and op alleles. The low genetic differentiation between CP and OP populations at the rest of the genome (FST = 2.4%) suggests gene flow between them. Males from OP lineages thus likely transmit their op allele to new genomic backgrounds. This contagious asexuality, combined with environment-induced selection (each reproductive mode being favored under different climates) probably contributes to the long-term persistence of the cp and op alleles.