Loss of Photoperiodic Control of Juvenile-Hormone Signaling Pathway Underlying the Evolution of Obligate Parthenogenesis in the Pea Aphid

Phenotypic plasticity, the ability of organisms to change their phenotype depending on external stimuli, enables their survival in fluctuating environments. An extreme example is polyphenism, in which a single genotype produces discrete phenotypes in response to external cues. However, under persistent environmental conditions, natural selection would favor reduced plasticity. This study focused on the loss of reproductive polyphenism and revealed the underlying mechanism in the pea aphid <i>Acyrthosiphon pisum</i>. Although most populations exhibit reproductive polyphenism, known as cyclical parthenogenesis, with a seasonal shift between parthenogenesis and sexual reproduction, some exhibit obligate parthenogenesis. To investigate the potential role of changes in the environmental sensitivity of the juvenile hormone (JH) pathway during this evolutionary shift, we analyzed the expression of genes involved in JH synthesis and degradation. We found that five of seven JH-related genes exhibited photoperiodic responses in one cyclical-parthenogenetic strain, whereas none of them responded to photoperiod in the two obligate-parthenogenetic strains. Notably, <i>CYP15A</i> and <i>JHEH</i> genes, which are involved in the final step of JH synthesis and in the initiation of JH degradation, respectively, showed strong photoperiodic responses in the cyclical-parthenogenetic strain but showed no responses in the obligate-parthenogenetic strains. Acetone treatment induces male production in obligate-parthenogenetic strains, suggesting that the developmental pathway for male production remains functional in these strains. These results suggest that the loss of the photoperiodic response in both JH synthesis and degradation pathways is a key mechanism underlying the elimination of the sexual phase, resulting in the loss of reproductive polyphenism in aphids.