The operational sex ratio experienced by mothers modulates the expression of sons’ alternative reproductive tactics in spider mites

Abstract: Intense male competition for access to females has often led to the evolution of alternative reproductive tactics (ARTs) such as sneaking, female mimicking, and satellite behavior. In many cases, which tactic a male expresses will depend upon intrinsic condition and/or environmental factors. Parental effects are also expected to play a critical role in ART expression when the parental environment is predictive of the offspring environment. Such parental effects on ARTs have remained largely unexplored. Here, we investigated maternal effects associated with operational sex ratio (OSR) on male ARTs (fighter and sneaker) in two-spotted spider mites Tetranychus urticae. In this mite species, mothers can anticipate the future male competition intensity (the future OSR) based upon the present OSR. To adjust local mate competition (LMC) among sons, mothers produce proportionally more sons under female-biased OSR and vice versa. We manipulated the maternal OSR and found that changes in maternal OSR did not alter the sneaker: fighter ratio among sons, but sneaker sons from mothers that experienced female-biased OSR started to guard females more quickly. Sneakers stay motionless on the dorsum of molting females, which is an advantageous position for mating with the emerging adult, and appear to deceive rival fighter males because they are not challenged. Earlier guarding by sneakers is advantageous for securing matings under intense male competition—as would be anticipated from the female-biased maternal OSR. We conclude that mothers anticipate the level of male competition in the next generation and influence their sons’ mating behavior accordingly. Significance statement: In response to intense male competition for access to females, males often evolve alternative reproductive tactics (ARTs) such as sneaking behavior. Parental effects are widespread and expected to play an important role in the determination of offspring’s ARTs when the parental environment is predictive of the offspring environment. We focus on operational sex ratio (OSR) as a predictor of male competition intensity in the next generation and found that female-biased OSR in the parental generation induces earlier guarding by sneaker sons in two-spotted spider mites. Mothers produce proportionally more sons under female-biased OSR, resulting in intense male competition in the next generation, and improve the odds of early guarding sneakers. Overall, our study suggests that spider mite mothers adjust their sons’ mating behavior by anticipating the intensity of male competition in the next generation from the present OSR.