Trans-generational plasticity of alternative reproductive tactics in male spider mites

Abstract: Two-spotted spider mites Tetranychus urticae rank globally among the mostsignificant herbivorous crop pests. Their enormous success as pests is due to high adaptabilityand well-developed plasticity in responding to environmental variation. As case in point, herewe document trans-generationally mediated plasticity in reproductive behavior of male spidermites. In detail, we examined parental effects of the maternal fertilization status and thealternative reproductive tactics (ARTs) of the mother’s mate on the ARTs of haploid sons.Tetranychus urticae is arrhenotokous, i. e. diploid daughters arise from fertilized eggs whereashaploid sons arise from unfertilized eggs. Thus, the ART of a mother’s mate can only exertnon-genetic effects on sons. ARTs are widespread among both vertebrate and invertebrateanimals and represent distinct behavioral phenotypes to maximize reproductive success withinthe same sex. ARTs of T. urticae males are conditionally determined, dichotomous (fightingand sneaking), and apparent in male-male fighting and pre-copulatory guarding behavior. Weassumed that parental ART effects should occur in T. urticae because maternal ART matingstatus (unmated, sneaker- or fighter-mated) is indicative of the offspring’ social environmentand younger males are more flexible in ART adoption than are older males. Fighter-matedmothers produced more offspring than unmated mothers and had a more daughter-biasedoffspring sex ratio than unmated and sneaker-mated mothers. Sons of fighter-mated motherswere more likely to guard and did so earlier than sons of unmated and sneaker-mated mothers.Unmated and sneaker-mated, but not fighter-mated, mothers, produced sneaker sons that werequicker to start guarding than were fighter sons. Proximately, parental ART effects on sons’ARTs were most likely mediated by differences in seminal fluids. Ultimately, observedalterations of sons’ ARTs rather represent adaptive maternal responses to ART phenotypes thanmanipulation by male mates. We argue that fighter-mated mothers tuned sons’ ARTs to malecompetitiveenvironments whereas unmated and sneaker-mated mothers tuned them to benignenvironments. Observed alterations in reproductive traits of fighter-mated mothers point atadaptive manipulation by the fighter phenotype or aligned male and female interests. Overall,our study documents previously unknown trans-generational ART effects. This work wasfunded by the Japan Society for the Promotion of Science (invitation fellowship L18534 to PSand KAKENHI grant 17K07556 to YS).