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The consequences of heterospecific matings may hinge on interspecies interactions, but also on characteristics of the intraspecies mating system, namely sperm precedence. Indeed, first-male precedence may entail costs of heterospecific matings that are usually overlooked in other systems, such as fertilization of oocytes that become unavailable to subsequent conspecific males or a decrease in female receptivity. Here, we used a system composed of two co-occurring haplodiploid spider-mite species with first-male precedence, Tetranychus urticae and Tetranychus evansi, to investigate (a) the potential costs of heterospecific matings and (b) whether mites avoid heterospecific mates. We found that heterospecific matings did not result in fertilized offspring (i.e. females). Moreover, fecundity (i.e. male offspring) of heterospecifically mated females did not differ from that of virgins, indicating that oocyte viability was not affected by heterospecific males. Furthermore, heterospecific matings did not trigger behavioural changes that typically derive from conspecific matings, namely reduced female receptivity for subsequent matings. In avoidance tests, we found that T. evansi females and T. urticae males mated as often with conspecifics as with heterospecifics, whereas T. evansi males and T. urticae females mated assortatively more often. Also, latency to copulation in virgin and mated females did not differ between conspecific and heterospecific matings, but matings between T. urticae individuals lasted longer than heterospecific matings. Therefore, heterospecific matings result in few costs despite first-male precedence and, concomitantly, species discrimination is low. Still, this study highlights the need to account for intraspecific mating systems in tests of the reproductive consequences of mating with heterospecifics. Significance statementIn species where the first male fertilizes all the offspring (firstmale precedence), mating with individuals from other species often yields few benefits and entails potential costs in terms of future mating events. Yet, several species exhibit incomplete recognition of conspecifics. We here show that this is the case among two spider-mite species that co-occur under natural conditions. However, we also demonstrate that the cost of mating with the 'wrong' species is low, even though they exhibit first-male precedence.

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Different patterns of sperm precedence are expected to entail different costs and benefits of mating for each sex that translate into distinct predictions regarding mating system evolution. Still, most studies addressing these costs and benefits have focused on species with mixed paternity or last male precedence, neglecting first‐male sperm precedence. We attempted to understand whether this latter pattern of sperm precedence translates into different costs and benefits for each sex in the haplodiploid spider mite Tetranychus urticae, a species in which female multiple mating is prevalent but most offspring are sired by first males. First, we assessed the stability of the sperm precedence pattern. To do so, we measured offspring paternity after exposing females to a different number of matings and mating intervals. Next, to determine the potential costs or benefits of multiple mating for females under different contexts, we measured the fecundity and survival of females that re‐mated at different time points. To measure the potential costs of multiple mating for males, we analysed male survival in the presence of different numbers of virgin or mated females. We also tested whether males can reduce offspring production of their competitors, by reducing the production of fertilized offspring of mated females. We found no change in the pattern of sperm precedence, independently of the mating interval between matings and the number of matings. Females paid a cost of mating, as multiply‐mated females laid fewer eggs than once‐mated females. However, while males had reduced survival when exposed to an intermediate number of virgin females, they paid no additional costs of mating with mated females. Moreover, females that mated multiple times produced fewer fertilized offspring than females that mated once. Thus, males that copulated with mated females reduced the fitness of other males, potentially leading to a relative fitness benefit for themselves. Our results show that complex costs and benefits may arise in males in species with first‐male sperm precedence. How these costs and benefits affect the maintenance of selection for polyandry remains an open question.