Kin-Mediated Male Choice and Alternative Reproductive Tactics in Spider Mites

SIMPLE SUMMARY: Evolutionary-grounded theories predict that any mating-related behavior should be influenced by the degree of genetic relatedness between the involved interactants. Close genetic relatedness may have beneficial and detrimental effects on evolutionary fitness. To optimize these trade-offs, mates should be able to discriminate kin and non-kin and adjust their behaviors accordingly. Here, we assessed kin-dependent mate choice and adjustment of alternative reproductive tactics (ARTs) in male spider mites. Our experiments suggest that male spider mites can assess kinship of rivals and prospective mates. Mate choice and expression of ARTs (fighting versus sneaking) were driven by direct and indirect fitness benefits arising from the degree of kinship of available mates and rival males competing for access to females. Depending on the social context (choice vs. no-choice, w/wo competition) and achievable fitness benefits, males seemed to use novelty as absolute decision rule and/or comparative evaluation in mate choice. Close kinship among rivals mitigated the males’ fighting propensity and favored adoption of the sneaking tactic. Overall, our study highlights kin-mediated plasticity in male choice and expression of ARTs and emphasizes the importance to consider different contexts and inclusive fitness benefit/cost trade-offs when interpreting mating preferences. ABSTRACT: Optimal outbreeding and kin selection theories state that the degree of kinship is a fundamental determinant in any mating system. However, the role of kinship in male choice and alternative reproductive tactics (ARTs) is poorly known. We assessed the influence of kinship on male choice and expression of ARTs in two populations of two-spotted spider mites Tetranychus urticae. Male spider mites guard premature females, which is an indicator of mate choice, and may conditionally adopt fighting or sneaking tactics to secure access to females. Males competing with kin or non-kin were offered one kin or non-kin female (experiment 1) and single males were presented a choice of kin and non-kin females (experiment 2). Under kin competition, males of both populations were more prone to guard non-kin than kin females at a 3:1 fighter:sneaker ratio. Under non-kin competition, all males were fighters. Under no-choice, males used novelty as indicator of genetic dissimilarity, serving as absolute decision rule for outbreeding. Under choice, comparative evaluation allowed males to preferentially guard females with higher reproductive potential. Overall, our study suggests that male spider mites can assess kinship of rivals and prospective mates. Kin discrimination allows adaptive, context-specific non-random mating preference and adjustment of ARTs.