Introduction
In many taxa, individuals use multiple cues 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.
Recent work has been consolidating the importance of studying the role
of multiple cues in varying and complex environments , under the
assumption that individuals often experience fluctuations in their
environment, such as changes in resource availability or in the density,
quality and sex ratio of conspecific and heterospecific individuals. In
such varying and complex environments, relying on multiple cues may
contribute to an accurate and fast response by the receiver across
environmental conditions . However, a disruption in the information
transfer between signallers and receivers, via excess noise or a
mismatch between cues, is also more likely in complex environments .
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 example, mate quality can be perceived
simultaneously via ephemeral cues, like many behavioural traits, and
more permanent cues such as some morphological traits, with the former
functioning as indicators of current condition thus changing with the
environment, and the latter indicating lifetime performance and
remaining virtually unchanged . That is the case of the field cricket
(Gryllus campestris ) that uses both body size and chirp rate as
cues for mate choice, 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. A similar phenomenon is observed in thePieris rapae. During development, this butterfly relies on both
temperature and photoperiod to predict 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, provided both cues continue
to be used . The mismatches between cues can also occur because of
sexual conflicts , with signallers emitting dishonest signals owning to
diverging interests between sexes . Under all these scenarios,
perceiving more than one cue can increase, rather than reduce,
uncertainty about which decision to make.
While the costs of emitting multiple cues are extensively described ,
the costs for receivers are less well studied, especially when
considering mismatches between cues. Besides the expected costs
associated with increased energetic and cognitive effort needed to
process more than one cue , costs for receivers are likely to be
associated with missing opportunities of mating with a suitable mate or
with attempting to mate with unsuitable mates . For instance, cues used
to assess conspecific mate quality sometimes overlap with those used for
species recognition, or kin recognition . This is the case inGryllus integer males for which the stimuli of heterospecific
females overrides conspecific chemical cues during mating trials . To
avoid losing suitable mates, one possibility is to evolve a lower mate
acceptance threshold in environments with discordant cues , conceivably
at the expense of accepting less desired mates . The same reduction in
the acceptance threshold can be observed when the costs of assessing
multiple cues are higher than the benefits of using them to only mate
with suitable mates, in which case individuals can ignore the least
reliable cues and accept a certain level of uncertainty . The opposite
is expected if the goal is to prevent matings conferring little to no
reproductive success. Therefore, the optimal use of cues and
corresponding behaviour should depend on the balance between the costs
of acceptance and rejection errors .
So far, the studies exploring the response of individuals to mismatches
between cues in the context of mate choice have largely disregarded
cases in which males are receivers and females are signallers of cues.
Addressing this issue can be particularly relevant 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 evolved the ability to discriminate
female mating status and modulate their reproductive behaviour based on
the cues presented by females . Yet, the behaviour of males when cues
provide discordant information concerning the female mating status, 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
volatile and substrate cues .
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 mismatch between the different cues
signalling female mating status. Here, we tested the consequences of cue
mismatch within this context.