Alternative reproductive tactics (ARTs) represent distinct behavioral phenotypes to maximize reproductive success within the same sex, primarily males, and may be genetically and/or conditionally determined. Across animals, intragenerational determinants of conditional ARTs are relatively well understood but transgenerational (non-genetic) effects of parental ARTs on filial ARTs are largely unknown.

Here, we assessed parental effects of conditional male ARTs on sons’ ARTs in arrhenotokous spider mites Tetranychus urticae. Arrhenotoky, i.e. males arising from unfertilized and females from fertilized eggs, sets the stage for sexual and transgenerational conflicts between male mates and females and their sons. Male ARTs of T. urticae are dichotomous, fighting and sneaking, and apparent in male-male combat and pre-copulatory guarding behavior. Due to haplodiploidy, male ARTs can only exert non-genetic effects on sons of their mates.

We hypothesized that parental ART effects are likely to occur in T. urticae because maternal ART mating status (unmated, sneaker- or fighter-mated) is indicative of the offspring’ social environment and ART flexibility rather prevails in younger than older males.

Fighter-mated mothers produced more offspring than unmated mothers and had a more daughter-biased offspring sex ratio than sneaker-mated mothers. Sons of fighter-mated mothers were 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 were quicker to start guarding than were fighter sons.

Proximately, parental ART effects on sons’ ARTs were most likely mediated by differences in seminal fluids. Ultimately, observed alterations of sons’ ARTs represent adaptive maternal responses to ART phenotypes rather than manipulation by male mates.

Fighter-mated mothers tuned filial ARTs to male-competitive environments whereas unmated and sneaker-mated mothers tuned them to benign environments. Observed alterations in reproductive traits of fighter-mated mothers suggest adaptive manipulation by the fighter phenotype or aligned male and female interests.

Overall, our study documents previously unknown transgenerational ART effects on haploid sons’ ARTs.