Incomplete species recognition entails few costs in spider mites, despite first-male precedence

Abstract: 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 statement: In species where the first male fertilizes all the offspring (first-male 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.