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.

Automated summary

The transition from sexual reproduction to parthenogenesis has profound evolutionary consequences for sex-related traits, which are expected to decay. This study examined the population structures of pea aphids in cold-winter and mild-winter regions and found distinct multilocus genotypes (MLGs) representing cyclically parthenogenetic (CP) lineages in cold-winter regions and obligately parthenogenetic (OP) lineages in mild-winter regions. Male production was reduced in OP lineages, but there was no clear pattern observed for male reproductive success. These findings suggest that traits in OP lineages may degenerate due to lack of selection. The overall effective reproductive capacity of OP males may be due to recent sex loss or underestimated reproductive opportunities.