Introduction
In many taxa, individuals use multiple sources of information to search for mates and engage in copulations . Along the years, several hypotheses have been put forward to explain the role of different cues in mate decision (see detailed classifications in : a) each cue may convey information about different mate qualities, the cues together increasing the accuracy of assessment, b) cues can be redundant but together improve discrimination, reducing errors associated to each cue, and/or c) cues can work differently in distinct environments and/or at dissimilar distances. The use of multiple cues is particularly useful in varying and complex environments , as information transfer to receivers may be disrupted in such environments due to excess noise and/or a mismatch between cues .
Mismatches among cues can occur when cues have different susceptibilities to changes in the environment, or when they persist for different periods of time . For instance, during development, the butterfly Pieris rapae relies on both temperature and the photoperiod to evaluate climatic conditions at adult emergence. Climate warming promotes the mismatch between these two cues, affecting temperature but not the photoperiod, which can result in a sub-optimal wing melanisation phenotype upon emergence . Likewise, mate quality can be perceived via both ephemeral cues (e.g., behavioural traits), and more permanent cues such as morphological traits . That is the case of the field cricket (Gryllus campestris ) that uses both body size and chirp rate in males as indicators of mate quality, typically giving priority to body size, the most permanent cue . In variable environments, however, fixed cues may become unreliable indicators of male quality , in which case the use of ephemeral cues may be favoured.
Whereas the use of multiple cues can be beneficial in many contexts, their use also come at some costs. First, processing information stemming from multiple cues is expected to lead to increased energetic and cognitive investment . Second, when there is mismatched information, using multiple cues may lead to an inaccurate response from the receiver. When this perception of cues concerns mate choice, costs for receivers are likely to be associated with missing opportunities of mating with a suitable mate or with investing in matings with unsuitable mates . For example, in Gryllus integer males the stimuli of heterospecific females compromise conspecific chemical cues detection during mating trials, leading to equal intensity of heterospecific and conspecific courting . Therefore, the optimal use of multiple cues and corresponding mating behaviour should depend on the balance between the costs of acceptance and rejection errors .
The existence of cues mismatch in mate choice can be particularly disadvantageous in species with first male sperm precedence, where female mating status discrimination is essential for male mating success. Indeed, under this pattern of sperm precedence, mating with mated females provides low, if any, fertilization opportunities, whereas mating with virgin females strongly contributes to reproductive success . Accordingly, it has been shown that males of these species have the ability to discriminate female mating status, preferring the virgins, and modulate their reproductive behaviour based on the cues presented by females . Yet, the behaviour of males when discordant information concerning the female mating status is provided, as well as the associated costs thereof, remain largely unknown.
To fill this gap, we observed the mating behaviour of male and female two-spotted spider mites (Tetranychus urticae) in environments with information concerning the female mating status coming from two sources, the female itself and the cues it leaves in the substrate. Spider mites have first male sperm precedence and, accordingly, males prefer to mate with virgins, basing their decision upon volatiles released by females into the air and/or substrate cues remaining on the patches . Furthermore, matings with virgin females take less time to start, are longer, and induce more survival costs in males than matings with mated females . All this suggests that male reproductive investment in matings with virgins and with mated females is not the same. However, matings involving mated females are frequently observed in laboratory populations , despite often leading to lower fecundity . This suggests that discrimination in this species is not perfect and may depend on the composition of cues present in the environment. Spider mite populations occur in variable environments, as they colonize seasonal resources such as agricultural crops . Moreover, they disperse among patches after a variable number of generations in the same patch, following a subdivided haystack population structure . This results in a scenario of cyclic waves of virgin and mated females across time within the same plant, which fosters the conditions for a temporal mismatch between the different cues signalling female mating status. Here, we tested the consequences of information mismatch within this context. We predict that, in an environment with information mismatches, the chance of mating with less favourable females and losing valuable mating opportunities is higher than in environments with concordant information, which should influence the overall mating costs suffered by males.