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.