Frequency‐dependent selection acting on the widely fluctuating sex ratio of the aphid Prociphilus oriens

Abstract

Frequency-dependent selection is a fundamental principle of adaptive sex ratio evolution in all sex ratio theories but has rarely been detected in the wild. Through long-term censuses, we confirmed large fluctuations in the population sex ratio of the aphid Prociphilus oriens and detected frequency-dependent selection acting on these fluctuations. Fluctuations in the population sex ratio were partly attributable to climatic factors during the growing season. Climatic factors likely affected the growth conditions of host plants, which in turn led to yearly fluctuations in maternal conditions and sex ratios. In the process of frequency-dependent selection, female proportion higher or lower than ca. 60% was associated with a reduction or increase in female proportion, respectively, the next year. The rearing of aphid clones in the laboratory indicated that mothers of each clone produced an increasing number of females as maternal size increased. However, the mean male number was not related to maternal size, but varied largely among clones. Given genetic variance in the ability to produce males among clones, selection should favour clones that can produce more numerous males in years with a high female proportion. Population-level sex allocation to females was on average 71%-73% for three localities and more female-biased when maternal conditions were better. This tendency was accounted for by the hypothesis of competition among foundresses rather than the hypothesis of local mate competition. We conclude that despite consistent operation of frequency-dependent selection, the sex ratio continues to fluctuate because environmental conditions always push it away from equilibrium.

Female–female competition leads to female‐biased sex allocation and dimorphism in brood sex composition in a gall‐forming aphid

“…Tetraneura sorini mothers produce either an all‐female brood or a mixed‐sex brood (including males and sexual females); the former type accounted for approximately half of the winged females in a population (Akimoto & Yamaguchi, ). Although this dimorphism has been found in other eriosomatine species (Akimoto & Yamaguchi, ; Li & Akimoto, ; Moran, ), previous studies based on the LMC hypothesis have failed to adequately explain the origin of this dimorphism.…”

“…Although this dimorphism has been found in other eriosomatine species (Akimoto & Yamaguchi, 2004;Li & Akimoto, 2017;Moran, 1993), previous studies based on the LMC hypothesis have failed to adequately explain the origin of this dimorphism.…”

“…In the wild, aphid clones compete severely, such that the extinction of rare clones and the prevalence of generalist clones have both been documented (Haack, Simon, Gauthier, Plantegenest, & Dedryver, ; Vorburger, ). In species where exploitative competition is common, mothers could take genetic advantage by producing a larger number of granddaughters in the first unisexual generation (Li & Akimoto, ). A larger number of granddaughters could provide the mother and her offspring with a head start for competition continuing through unisexual generations.…”

“…In another eriosomatine species, Prociphilus oriens , long‐term observations indicated that the sex allocation was strongly biased towards females (71%–73%) at the population level, which was attributed mainly to competition among unrelated foundresses (Li & Akimoto, ). In cyclically parthenogenetic animals, in which the bisexual generation is followed by unisexual generations, exploitative competition is expected to be severe throughout the unisexual generations (Williams, ).…”

“…Thus, we postulated that mothers in good condition could achieve higher fitness returns by producing more females than males because these mothers could then have more granddaughters in the first unisexual generation (the foundress generation). Because a male can inseminate more than 10 sexual females (Li & Akimoto, ), it is not disadvantageous for mothers to produce female‐biased sex ratios. However, evidence of competition among foundresses has not been obtained in P. oriens .…”