Discussion
Here we examine the impact of multiple cues and the potential resulting information mismatch on the mating behaviour of spider mites. We found that the number of mating attempts was only influenced by cues left on the patch prior to the mating sessions, being higher in patches with cues of virgins. In turn, female acceptance was affected by both substrate cues and the mating status of the females, being the highest in patches with virgins and with substrate cues of virgin females and the lowest on patches with mated females and with substrate cues of mated females. As a consequence, the number of mating events was affected by both substrate cues and the mating status of the females, such that the number of copulations was intermediate in environments with mismatched information. Once copulation started, its duration seemed to depend mainly on the mating status of the female being fertilized, with the overall amount of time invested in mating being higher in matings with virgins than with mated females and intermediate in environments with mismatched information. Ultimately, male survival mirrored the reproductive investment of males, with patches in which there was mismatched information showing intermediate survival costs.
In species with first male sperm precedence, like spider mites and many spiders, the sperm from the first insemination sires most of the offspring, thus virgins are more valuable mates than mated females. Accordingly, males exhibit a preference for virgin females, in this and other species with the same pattern of sperm precedence . Such result is recapitulated here in patches with concordant cues, with mating eagerness, copulation duration and survival costs being the highest in patches with virgins.
When exposed to discordant information males based their pre-copulatory mating behaviour solely on the substrate cues on the patch. These cues are obviously less reliable determinants of the status of the female on those patches than information emanating from the female itself. Thus, the fact that pre-copulatory mating behaviour is triggered by substrate cues only suggests that these cues are the most far-reaching of the two, being beneficial in mate searching. A non-exclusive alternative is that this less accurate cue is cheaper to assess, in which case it may pay off to consider it alone (Fawcett and Johnstone 2003). In the field cricket (Gryllus integer ), calling songs are used as long-distance cues to find mates while short-range chemical cues are employed to assess mate quality (Lenard & Hedrick 2010). Interestingly, being exposed to attractive long-distance cues results in a quicker positive response to short-distance cues, which may suggest a reduced investment in the assessment of the latter cue in this species (Lenard & Hedrick 2010). A similar pattern could be taking place here. The use of more unreliable information in pre-copulatory mating behaviour might help explain why, in spider mites and perhaps in species with a similar pattern of sperm precedence, matings with mated females are frequently observed, despite their weak reproductive value.
Unlike male eagerness, female acceptance depended both on the substrate cues and on the females’ own mating status, with increased acceptance in mated females and reduced acceptance in virgins in environments with mismatched information, compared to concordant environments. Possibly mated females accept more matings in patches with substrate cues of virgins because those are the patches in which the number of male mating attempts is the highest and thus, resistance is expected to be more costly. This strategy, called “convenience polyandry”, should occur under intense harassment, when by accepting more mates than their optima, females suffer fewer costs than by resisting them . Such is the case for instance in female water striders that modify their mating rate based on the relative costs of mating and of resisting mating attempts . In turn, reduced acceptance of virgin females in patches with substrate cues of mated females could be a byproduct of male’s reduced eagerness to mate in those patches, that may result in meek, and thus easy to reject, mating attempts. Importantly, because females’ pre-copulatory behaviour depended both on their own mating status and on the substrate cues present but that of males only relied on substrate cues, the response of the two sexes was not aligned, resulting in intermediate number of mating events in environments with mismatched information.
Once copulation started, the response of males seemed to be more affected by the mating status of the female mating than by substrate cues present in the environment. This is probably because, once males reach the females, they have access to the more reliable cues emanating from the female itself, and can thus use those to accurately modulate their post-copulatory strategies. Still, substrate cues played a, albeit less significant, role in copulation duration. Indeed, when exposed to virgin cues, males mated for a longer period with both virgin and mated females than when exposed to cues of mated females. This suggests the information obtained before mating keeps influencing mating behaviour even when more accurate cues are available.
The response of males to multiple cues, including both pre- and post-copulatory behaviours, must come at some costs. Previously, it was shown that, in male spider mites, survival is affected differently depending on the mating status of their reproductive partners : matings with virgin females result in high offspring yield but reduced male survival, while matings with mated females lead to no offspring but also fewer survival costs. Again, being exposed to discordant cues influenced this trait. First, we saw that, in patches occupied by mated females, males had lower survival when substrate cues were from virgins than when they were from mated females only. It seems that in these cases, the existence of a mismatch leads to an over-investment in ineffective matings. This behaviour could be maintained not to risk rejecting mating opportunities with suitable females, as proposed by Reeve . In his model, Reeve shows that males are expected to exhibit more permissive mating acceptance thresholds as the value of the desirable female increases and the costs of accepting a wrong female decreases, which are the exact conditions we find in this system. Indeed, virgin females are highly valuable compared to mated females and the costs for males of mating with mated females is quite low . An equivalent decrease of the acceptance threshold would be expected if assessing multiple cues was too costly, in which case one would expect individuals to neglect the least reliable cue , that is the cues left on the substrate by females.
Male survival in patches with mismatches between cues is higher than in patches with cues of virgins only. In these patches, the number of mating attempts is similar to that in patches with virgins, but the total number of matings and the total amount of time spent copulating is significantly lower. This suggests that the number of mating events and/or postcopulatory events are important determinants of male mating costs, ensuring a reduction in the costs of reproduction in mating with less valuable females. Moreover, male survival was higher in patches with virgin females but substrate cues of mated females, than in patches with cues of virgins only. Therefore, it seems that in these conditions, males invest less in effective matings, possibly via a reduction in the number of male mating attempts and in the total amount of time spent mating. However, we have not tested whether the observed reduction in copulation duration is translated into reduced mating success and previous results suggest copulation duration does not correlate positively with offspring production .
We did not measure the chemical composition of the different sources of information that males were exposed to, nor do we know exactly which cues are used by males to choose between virgin and mated females. Indeed, we know that substrate cues and volatiles emitted by females are sufficient for male choice (Rodrigues et al. 2017) but other cues, such as visual and tactile cues, not being necessary, may play a role (Royalty et al. 1993). In addition, substrate cues themselves, considered here as a unit of information, include web, faeces, eggs and any chemical compounds deposited by females in the patches. Web is used, among other functions, in mate searching behaviour (Penman and Cone 1972, 1974) but the role of other substances is unknown. Still, we can make a few inferences from the patterns observed in male behaviour upon exposure. For example, we do not know whether the chemicals used by males to assess females themselves are the same present on the substrate. This is however not very likely, as different components of male mating behaviour react differently to the different combinations of cues from virgins and/or mated females. Another possibility is that only virgin females produce cues. Our results are compatible with this possibility. Regardless, this would still mean that males are exposed to situations in which the information stemming from the females themselves and the substrate they occupy are either concordant or discordant.
The optimal use of information and corresponding behaviour should depend on the balance between the costs of acceptance and rejection errors and this, in turn, should vary with the dynamics of the social and ecological environment, which set the stage for different selection pressures to operate upon mating cues and their perception (Alpedrinha et al. 2019). In spider mite populations, individuals disperse among patches after a variable number of generations in the same patch, following a subdivided haystack population structure . Such cycles of colonization-expansion foster the conditions for information mismatches within a patch. Indeed, while the information emitted by females will change simultaneously with the shift in mating status, the cues left on the patch should remain unaltered for some time after this shift. While these cues seem to be less reliable than the information provided by females themselves, they are probably accessible at a larger scale, allowing males to move in the direction of areas with suitable mates (i.e., virgins) before their competitors. This should be highly advantageous in species with first male sperm precedence. These findings could thus have important implications for mating system evolution, potentially helping to explain why female multiple mating is maintained in species with first male sperm precedence. Still, the benefit of using multiple, sometimes discordant, cues will hinge upon the frequency of discordance among them, which itself should vary with the dynamics of populations.
References
Figure 1. Male and female pre-copulatory mating behaviour and the corresponding number of mating events in response to substrate cues and female mating status. a) Number of male mating attempts, b) proportion of mating attempts accepted by females and c) number of mating events. Males were exposed for 1 hour to 5 virgin or mated females in patches impregnated with cues of virgin or mated females. Circles represent individual replicates. Black circles –patches with mated females; grey circles – patches with virgin females; open circles – patches with cues of virgin females; full circles – patches with cues of mated females.