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.