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Abstract

Polymorphic warning signals in aposematic species are enigmatic because predator learning and discrimination should select for the most common coloration, resulting in positive frequency-dependent survival selection. Here, we investigated whether differential mating success could create sufficiently strong negative frequency-dependent selection for rare morphs to explain polymorphic (white and yellow) warning coloration in male wood tiger moths (Parasemia plantaginis). We conducted an experiment in semi-natural conditions where we estimated mating success for both white and yellow male moths under three different morph frequencies. Contrary to expectations, mating success was positively frequency-dependent: white morph males had high relative fitness when common, likewise yellow morph males had high relative fitness when instead they were common. We hence built a model parameterized with our data to examine whether polymorphism can be maintained despite two sources of positive frequency dependence. The model includes known spatial variation in the survival advantage enjoyed by the yellow morph, and assumes that relative mating success follows our experimentally derived values. It predicts that polymorphism is possible under migration for up to approximately 20% exchange of individuals between subpopulations in each generation. Our results suggest that differential mating success combined with spatial variation in predator communities may operate as a selection mosaic that prevents complete fixation of either morph.
Colour polymorphism torn apart by opposing positive
frequency-dependent selection, yet maintained in
space
Swanne P. Gordon
1
*, Hanna Kokko
2
, Bibiana Rojas
1
, Ossi Nokelainen
1,3
and
Johanna Mappes
1
1
Centre of Excellence in Biological Interactions, Department of Biological and Environmental Sciences, University of
Jyv
askyl
a, yv
askyl
a, Finland;
2
Institute of Evolutionary Biology and Environmental Studies, University of Zurich,
Zurich, Switzerland; and
3
Department of Zoology, University of Cambridge, Cambridge, UK
Summary
1. Polymorphic warning signals in aposematic species are enigmatic because predator learning
and discrimination should select for the most common coloration, resulting in positive fre-
quency-dependent survival selection.
2. Here, we investigated whether differential mating success could create sufficiently strong
negative frequency-dependent selection for rare morphs to explain polymorphic (white and
yellow) warning coloration in male wood tiger moths (Parasemia plantaginis).
3. We conducted an experiment in semi-natural conditions where we estimated mating success
for both white and yellow male moths under three different morph frequencies.
4. Contrary to expectations, mating success was positively frequency-dependent: white morph
males had high relative fitness when common, likewise yellow morph males had high relative
fitness when instead they were common. We hence built a model parameterized with our data
to examine whether polymorphism can be maintained despite two sources of positive fre-
quency dependence. The model includes known spatial variation in the survival advantage
enjoyed by the yellow morph and assumes that relative mating success follows our experimen-
tally derived values. It predicts that polymorphism is possible under migration for up to
approximately 20% exchange of individuals between subpopulations in each generation.
5. Our results suggest that differential mating success combined with spatial variation in
predator communities may operate as a selection mosaic that prevents complete fixation of
either morph.
Key-words: aposematism, coloration, mating success, modelling, predation, sexual selection,
spatial mosaic
Introduction
A fundamental question in evolutionary biology is what
processes drive the origin and maintenance of genetic
polymorphisms in the wild. Polymorphisms indicate the
potential for unusual types of selection because they devi-
ate from simpler cases where one genotype has a consis-
tent advantage over another and natural selection drives
the winning type to fixation (Calsbeek, Bonvini & Cox
2010). If a genotype’s relative fitness improves with its rel-
ative frequency (positive frequency dependence), polymor-
phisms typically cannot be explained: here selection acts
against rare alleles, and the population is consequently
expected to evolve towards one of alternative stable states
but not towards a stable polymorphism (Mallet & Joron
1999; Lehtonen & Kokko 2012). Negative frequency
dependence on the other hand has the opposite effect: a
genotype is selected against when common and selected
for when rare, making it easier to maintain polymor-
phisms (Sinervo & Lively 1996). Gene flow, that links
populations undergoing spatially heterogeneous selection,
can also make alternative morphs persist within an envi-
ronment: in this case, a locally suboptimally performing
morph can avoid extinction because of continual immigra-
tion from elsewhere, where it is selected for (divergent
selection, Gray & McKinnon 2007).
*Correspondence author. E-mail: swanne.gordon@jyu.fi
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society
Journal of Animal Ecology 2015 doi: 10.1111/1365-2656.12416
Being easily measured and tracked, animal colours rep-
resent some of the best-studied examples of trait polymor-
phisms (McKinnon & Pierotti 2010). Colours are often
strongly linked to fitness in many different contexts such
as crypsis (Steward 1977; Rothschild 1981; Endler &
Greenwood 1988) and thermoregulation (Clusella-Trullas,
Van Wyk & Spotila 2007; Hegna et al. 2013). Colour is
also often used a warning signal of unprofitability (Poul-
ton 1890; Cott 1940; Stevens & Ruxton 2012), and in this
context, theoretical expectations (Servedio 2000; Endler &
Mappes 2004) as well as empirical studies (review, Allen
1988; Mallet & Barton 1989; Borer et al. 2010) point to
positive frequency-dependent survival selection. It is easier
for predators to learn to discriminate against signals that
are not only highly recognizable and memorable, but also
common (‘strength in numbers’); this selects against poly-
morphism (Mu
¨ller 1878; Mallet & Joron 1999; Lindstr
om
et al. 2001; Rowland et al. 2007). This renders it enig-
matic why numerous polymorphic aposematic colour sig-
nals from a range of taxa are known in nature (e.g.
O’Donald & Majerus 1984; Nokelainen et al. 2012; Rojas
& Endler 2013).
Recent research has investigated the effect of various
processes that can maintain polymorphisms and hence
also impact prey fitness. In many cases, these mechanisms
are not mutually exclusive and instead work in concert to
achieve polymorphisms (S
anchez-Guill
en et al. 2011).
These range from spatio-temporal variation in predation
(Endler & Rojas 2009; Stevens & Ruxton 2012; Noke-
lainen et al. 2014) or sexual selection (Maan & Cummings
2009; Nokelainen et al. 2012) to frequency-dependent
selection (Svensson, Abbott & Hardling 2005; Olendorf
et al. 2006). Gene flow (Rosenblum 2006) and genetic
drift (Hoffman et al. 2006; Gray & McKinnon 2007) add
to the mix of effects that can impact the stability of
polymorphisms.
Research on colour polymorphisms in aposematic spe-
cies has focused on the role of predator learning and
signal evolution, due to the strong selection exerted by
the high cost of conspicuousness when predators are naive
(Lindstr
om et al. 2001; Mappes et al. 2014). Here, we
show that full understanding into the maintenance of
warning colour polymorphisms may require considering
multiple forces and their interaction. Our particular inter-
est lies in understanding potential trade-offs between nat-
ural and sexual selection (Kotiaho et al. 1998; Maan &
Cummings 2009; Nokelainen et al. 2012; Cummings &
Crothers 2013; Finkbeiner, Briscoe & Reed 2014) and in
the arguably understudied interaction of frequency-depen-
dent selection and gene flow (Joron & Iwasa 2005; Cals-
beek, Bonvini & Cox 2010).
Colour in aposematic organisms may serve multiple
functions: thermoregulation, defence against predators
and mate attraction. This highlights the possibility that
both natural and sexual selection can be frequency-de-
pendent (Gray & McKinnon 2007; Sinervo & Calsbeek
2006; Roulin & Bize 2007), and it is known from gen-
eral theory that when different types of frequency
dependence interact, the diversity of dynamic outcomes
can be far greater than predicted under one source of
selection only (Sinervo & Calsbeek 2006). Here, we com-
bine information from a mating experiment with pub-
lished estimates of survival selection in order to examine
their interaction and the potential role of frequency-de-
pendent selection on the maintenance of colour poly-
morphism in an aposematic organism. The results aim
to confirm an idea previously expressed by Roulin &
Bize (2007): it is difficult to explain polymorphisms if
the common morph derives a mating advantage, but in
a spatially structured population, some degree of gene
flow could potentially counteract the predicted loss of
genetic variation. Interestingly, a modelling study of a
particular colour polymorphism Mu
¨llerian mimicry
shows that too high gene flow can again break down a
polymorphism, because the system then effectively
behaves like one unit with averaged parameter values
(Joron & Iwasa 2005). We therefore also include a mod-
elling component to investigate the range of dispersal
values that could protect a polymorphism in a system
where natural and sexual selection interact and also vary
spatially.
Our study species is the aposematic wood tiger moth
(Parasemia plantaginis). Males of this species exhibit dis-
crete wing coloration on both local and on a broad geo-
graphical scale (Hegna, Galarza & Mappes 2015).
European populations feature two distinct genetic male
morphs, yellow and white (Galarza et al. 2014). In Fin-
nish populations, the more conspicuous yellow male
morph has been shown to have greater warning signal
efficacy, such that viability selection mediated by preda-
tion favours this morph (Nokelainen et al. 2012, 2014).
White adult males, on the other hand, sometimes appear
to have better mating success than yellow males, espe-
cially in instances where mating incurs high costs (Noke-
lainen et al. 2012). However, mating success has so far
only been evaluated in a context of equal frequency of
both morphs, and under small laboratory conditions as
opposed to more natural settings. To test for the effects
of potential frequency dependence in the context of sex-
ual selection, we conducted an experiment in semi-natu-
ral conditions where we estimated mating success under
three different morph frequencies. We next integrate our
data from this experiment with known estimates of pre-
dation against both morphs in a simple spatial model.
The combination of both mating experiment and model
is based on the suggested trade-off between natural and
sexual selection described above driving the evolution
and maintenance of colour polymorphism in our system.
This trade-off is particularly interesting and unexplored
in a case where both natural and sexual selection are
potentially frequency-dependent in aposematic organisms,
as never before has variation in frequency dependence
across fitness components been considered in this con-
text.
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society, Journal of Animal Ecology
2S. P. Gordon et al.
Materials and methods
study system
The wood tiger moth system (Parasemia plantaginis) is well stud-
ied in terms of the evolution of warning signals (e.g. Ojala, Lind-
str
om & Mappes 2007; Lindstedt, Lindstr
om & Mappes 2009;
Lindstedt et al. 2010; Nokelainen et al. 2012, 2014; Nokelainen,
Lindstedt & Mappes 2013). Wood tiger moths are easy to rear
and maintain in a laboratory setting and can be collected and
manipulated with relative ease in semi-wild or wild conditions.
They overwinter as larvae in the wild and naturally go through
one generation a year per life cycle. Adult wood tiger moths are
capital breeders and hence do not feed (but drink) during adult-
hood. Although laboratory-reared femalemale ratio at eclosion
is very close to the 50 : 50 ratio, in the field the operational sex-
ratio is much more male biased (Gordon et al. In prep.). This is
likely based on the fact that females in the laboratory live on
average only a few days, whereas males can live up to two weeks
(Santostefano & Mappes, In prep.), which likely reflect their life
span differences in wild. Adult females are also conspicuous,
avoided by bird predators, and, unlike the discrete coloration in
males, exhibit a continuous range of wing coloration from yellow
to orange and to red (Lindstedt et al. 2011). Like most moths,
mature female moths emit a sexual pheromone call to attract
males. Once fertilized, wood tiger moth females can lay approxi-
mately 300 eggs in one clutch (Ojala, Lindstr
om & Mappes
2007). Females appear choosy, as males attempting to mate can
be rejected if not preferred by females (pers. obs.). All wood tiger
moths used in the enclosure experiment (see below) were labora-
tory-raised from stock collected from wild moths caught in Fin-
land in 2010 and reared under greenhouse conditions at the
University of Jyv
askyl
a for multiple generations (for more details
on laboratory rearing see Lindstedt, Lindstr
om & Mappes 2008).
enclosure experiment
In order to examine the effect of frequency-dependent selection
on mating in wood tiger moths, we ran a large-scale outdoor
enclosure experiment in Konnevesi research station of the
University of Jyv
askyl
a (Finland), from 4 July 2012 until 24 July
2012. A 20 m 930 m (3 m high) enclosure was divided into six
separate cage compartments, approximately 6 m 910 m each.
The floor of each compartment was open with natural foliage,
and the top and two of the sides were made of white mesh, open
to natural light. The other two sides were covered with a plastic
green tarp to block visual contact between the cages and to limit
the spread of mating pheromones exuded by the calling females.
We performed 10 individual runs, each involving three treat-
ments: a balanced morph ratio (12 white males and 12 yellow
males); a white-biased treatment (16 white males and eight yellow
males); and a yellow-biased treatment (16 yellow males and eight
white males). Every male and female used in the entire experi-
ment was individually marked using a paint dot on the underside
of both the top and bottom portion of the fore and hind wing.
Each run used 24 virgin males and five virgin females per treat-
ment (in order to closely mimic natural male-biased sex ratios in
the wild), totalling 72 males and 15 females per run. Treatments
within each run were randomly assigned to three of the six
compartments, and all males and females used in each run were
randomly assigned to their treatment. However, to achieve the
desired sample sizes, some unmated males had to be re-used in
the next subsequent run. To see whether this logistical constraint
had an effect, we analysed the mating success of each male cate-
gorized as na
ıve vs. re-used; we found no effect (for white male
morphs: effect =0294 0436, z=674, P=0500; and for
yellow morph: effect =0018 0460, z=0038, P=0970). In
total, we used 720 male measurements of which 590 involved
na
ıve males and 130 were re-used.
The five females were tethered to a string in an open Styrofoam
box (one female per box), which allowed them to move and fly
but not escape the box. Behavioural assessments of the females
prior to and during the experiment did not reveal any changes in
behaviours that would limit them from escaping harassment from
males if they so chose (Rojas et al. In prep.), and tethering them
allowed us the opportunity to count all their eggs reliably. If free
female choice was, however, impacted negatively by tethering, this
impact should be spread equally across all three treatments.
The boxes, that offered protection from the wind and rain,
were placed at equidistant points around the corners of every
cage. Females were allowed to acclimatize for approximately one
hour. Given past information on ideal mating times in these
moths (S. Gordon pers. obs.), males were then released in the
middle of each cage at approximately 4:00 pm. All moths were
collected again at 8:00 am the next morning. The time window
hence includes the time when matings naturally occur in this spe-
cies (Nokelainen et al. 2012). Cages were watched from the
beginning to the end of each run by one observer in each cage.
Data about general hourly weather conditions, moth behaviours
and the ID’s of mated pairs upon the onset of mating were col-
lected by observers. Because females may mate multiply, the total
number of matings was not fixed. Males, however, were only
found to mate maximally once, with a few exceptions: there were
two double matings involving each one Y and one W male mated
to same female, and one mating of the same white male to two
females. As males were individually marked and identified after
the onset of every mating, we could confidently assign paternity
to all matings (except for the doubly mated pair, where we were
able to assign paternity to the most likely father based on the col-
oration of the adult offspring for the basis of analyses). At the
end of each experimental run, all mated females were brought to
the greenhouse at the University of Jyv
askyl
a and their egg num-
ber and hatching success were measured.
statistical analyses
Male age and size
As females may choose males based on differences in age and
size, we first calculated the spread of male characteristics across
treatments to assess any bias the assignment of individuals into
treatments may have produced. We used pupal weight as a good
proxy for adult weight (as adults do not eat). We ran an ANOVA
with age (days since pupation) and pupa weight as response vari-
ables and treatment by morph interaction as explanatory factors
(using function ‘aov’ in Program Rv215, 2013).
Mating success
We measured the mating success of the W and the Y morph
using generalized linear mixed effect models, first combined, and
then separately (one for each morph). In each model, the number
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society, Journal of Animal Ecology
Positive frequency dependence and polymorphism 3
of matings in each cage was the response variable (binomial vari-
able where 1 is mated and 0 means not mated in all cases). Pupa
weight, male age and treatment (and their interaction) were the
explanatory variables. We included enclosure cage as a random
effect to account for the non-independence of matings within
each enclosure.
Fitness
The relative fitness of individual males (estimated morph siring
success) was calculated as simply a measure of the proportion of
larval recruits (out of the total number of enclosure recruits) that
were sired by each male (i.e. proportional to its contribution to the
next generation) relative to the total number of males in the focal
enclosure. It was obtained by dividing the number of hatched lar-
vae sired by a given male by the total number of hatched larvae in
each enclosure. This led to every male in each of the 30 unique
enclosures having a measure of relative fitness. We then again ran
a binomial generalized linear mixed effect model (morphs were not
also separated as above because here there were no significant
three-way interactions) where fitness was the response variable.
Morph frequency (treatment), morph and their interaction were
the explanatory variables, age and pupa weight were added covari-
ates, and enclosure compartment was a random effect.
Results
effect of male age and sizes
Yellow males used in the experiment tended to be
younger than white males (ANOVA F
1,701
=14610,
P<0001), yet this effect was not different between treat-
ments (F
2, 701
=0223, P=0800). The same pattern was
found for pupal weight, which was smaller for yellow
males (ANOVA F
1,706
=9367, P=0002), yet equally so for
all treatments (F
2,706
=0273, P=0761). Due to this,
both male age and pupa weight were included as covari-
ates in all analyses.
mating success
The model for mating success of white male moths
showed a significant positive effect of weight (model effect
size =0016 0006, z=2722, P=0006) but none of
age (effect size =0011 0044, z=0242, P=0809) or
treatment (P>07867). The model for the mating success
of yellow males likewise showed a significant effect of
weight (effect size =00323 0011, z=0011, P=
0002), treatment (driven by this morph’s significantly
lower mating success in the white-biased treatment, see
below; effect size =6404 3181, z=2013, P=0044)
and a significant interaction between weight and
treatment: yellow males had lower mating success in the
white-biased treatment (no difference in the yellow-biased
treatment), with large males suffering more from this
effect (effect size =0038 0017, z=2191,
P=0028). Age was also an insignificant covariate in the
model for mating success of yellow males (effect
size =0040 0050, z=0803, P=0422).
We should note that the model combining both morphs
model showed comparable results for age and size, but
had no overall effect of morph (effect size of White
morph vs. Yellow morph =4640 2692, z =1728,
P=0085). The only significant interactions were a white-
biased treatment by morph interaction (model effect
size =8886 3995, z =2224, P=0026); that is, the
yellow morph had significantly lower mating success in
the white-biased treatment, driven mainly by larger males
doing worse in this regard (significant weight by white-bi-
ased treatment by yellow morph interaction: effect
size =0052 0022, z=2403, P=00163).More
importantly, however, a Type III Chi-square ANOVA shows
an overall significant effect of the three-way interaction
between morph, weight and treatment (Chi-sq =585,
P=005), implying that morphs responded differently to
all aspects we were evaluating (treatment and weight).
Therefore, for greater clarity, we will only focus on the
separated morph model results in the discussion.
fitness
Fitness, which consider the mating success as well as
the ultimate offspring sired hatching success, show that
the yellow male morph have significantly lower fitness in
the white-biased treatment compared to the other treat-
ments (Fig. 1). This result is opposite for the white male
morph. Analyses found no significant differences between
treatments (t=1318, P=0188), but a significant treat-
ment 9morph interaction (t=2214, P=0027). Age
was again insignificant in the model (t=0206,
P=0837), whereas weight was significant (t=3195,
P=0002).
In order to better examine whether the differences
between morphs in both high-frequency treatments were
significant, we ran a similar model but excluded the bal-
anced ratio treatment. Results show that in the white-bi-
ased treatment, yellow males have marginally lower fitness
compared to white males (1408 0792, t=1777,
P=0076), while this pattern was reversed in the yellow-
biased treatment (2292 0998, t=2295, P=0022).
modelling the consequences
Our results surprisingly indicate positively frequency-de-
pendent mating success: males of the white morph had
high relative fitness when common, likewise yellow males
had high relative fitness when they formed the majority of
the males (Fig. 2). As both natural and sexual selection
therefore appear positively frequency-dependent, the most
straightforward theoretical prediction is that a population
should evolve towards one of two possible alternative
equilibria (Lehtonen & Kokko 2012): either white only or
yellow only. The existence of large geographic areas with
polymorphisms therefore led us to consider the role of
spatially varying selection, for which there is evidence
based on variation in bird communities (Nokelainen et al.
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society, Journal of Animal Ecology
4S. P. Gordon et al.
of matings in each cage was the response variable (binomial vari-
able where 1 is mated and 0 means not mated in all cases). Pupa
weight, male age and treatment (and their interaction) were the
explanatory variables. We included enclosure cage as a random
effect to account for the non-independence of matings within
each enclosure.
Fitness
The relative fitness of individual males (estimated morph siring
success) was calculated as simply a measure of the proportion of
larval recruits (out of the total number of enclosure recruits) that
were sired by each male (i.e. proportional to its contribution to the
next generation) relative to the total number of males in the focal
enclosure. It was obtained by dividing the number of hatched lar-
vae sired by a given male by the total number of hatched larvae in
each enclosure. This led to every male in each of the 30 unique
enclosures having a measure of relative fitness. We then again ran
a binomial generalized linear mixed effect model (morphs were not
also separated as above because here there were no significant
three-way interactions) where fitness was the response variable.
Morph frequency (treatment), morph and their interaction were
the explanatory variables, age and pupa weight were added covari-
ates, and enclosure compartment was a random effect.
Results
effect of male age and sizes
Yellow males used in the experiment tended to be
younger than white males (ANOVA F
1,701
=14610,
P<0001), yet this effect was not different between treat-
ments (F
2, 701
=0223, P=0800). The same pattern was
found for pupal weight, which was smaller for yellow
males (ANOVA F
1,706
=9367, P=0002), yet equally so for
all treatments (F
2,706
=0273, P=0761). Due to this,
both male age and pupa weight were included as covari-
ates in all analyses.
mating success
The model for mating success of white male moths
showed a significant positive effect of weight (model effect
size =0016 0006, z=2722, P=0006) but none of
age (effect size =0011 0044, z=0242, P=0809) or
treatment (P>07867). The model for the mating success
of yellow males likewise showed a significant effect of
weight (effect size =00323 0011, z=0011, P=
0002), treatment (driven by this morph’s significantly
lower mating success in the white-biased treatment, see
below; effect size =6404 3181, z=2013, P=0044)
and a significant interaction between weight and
treatment: yellow males had lower mating success in the
white-biased treatment (no difference in the yellow-biased
treatment), with large males suffering more from this
effect (effect size =0038 0017, z=2191,
P=0028). Age was also an insignificant covariate in the
model for mating success of yellow males (effect
size =0040 0050, z=0803, P=0422).
We should note that the model combining both morphs
model showed comparable results for age and size, but
had no overall effect of morph (effect size of White
morph vs. Yellow morph =4640 2692, z =1728,
P=0085). The only significant interactions were a white-
biased treatment by morph interaction (model effect
size =8886 3995, z =2224, P=0026); that is, the
yellow morph had significantly lower mating success in
the white-biased treatment, driven mainly by larger males
doing worse in this regard (significant weight by white-bi-
ased treatment by yellow morph interaction: effect
size =0052 0022, z=2403, P=00163).More
importantly, however, a Type III Chi-square ANOVA shows
an overall significant effect of the three-way interaction
between morph, weight and treatment (Chi-sq =585,
P=005), implying that morphs responded differently to
all aspects we were evaluating (treatment and weight).
Therefore, for greater clarity, we will only focus on the
separated morph model results in the discussion.
fitness
Fitness, which consider the mating success as well as
the ultimate offspring sired hatching success, show that
the yellow male morph have significantly lower fitness in
the white-biased treatment compared to the other treat-
ments (Fig. 1). This result is opposite for the white male
morph. Analyses found no significant differences between
treatments (t=1318, P=0188), but a significant treat-
ment 9morph interaction (t=2214, P=0027). Age
was again insignificant in the model (t=0206,
P=0837), whereas weight was significant (t=3195,
P=0002).
In order to better examine whether the differences
between morphs in both high-frequency treatments were
significant, we ran a similar model but excluded the bal-
anced ratio treatment. Results show that in the white-bi-
ased treatment, yellow males have marginally lower fitness
compared to white males (1408 0792, t=1777,
P=0076), while this pattern was reversed in the yellow-
biased treatment (2292 0998, t=2295, P=0022).
modelling the consequences
Our results surprisingly indicate positively frequency-de-
pendent mating success: males of the white morph had
high relative fitness when common, likewise yellow males
had high relative fitness when they formed the majority of
the males (Fig. 2). As both natural and sexual selection
therefore appear positively frequency-dependent, the most
straightforward theoretical prediction is that a population
should evolve towards one of two possible alternative
equilibria (Lehtonen & Kokko 2012): either white only or
yellow only. The existence of large geographic areas with
polymorphisms therefore led us to consider the role of
spatially varying selection, for which there is evidence
based on variation in bird communities (Nokelainen et al.
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society, Journal of Animal Ecology
4S. P. Gordon et al.
flectance) have been found to actually attract attacks by
these predators (Lyytinen et al. 2001; Lyytinen, Lind-
str
om & Mappes 2004). On the other hand, dunnocks
(Prunellidae) tend to avoid white male moths and gener-
ally forage closer to the ground level in shaded boreal for-
ests. White coloration might be a more effective warning
signal in these circumstances because they have much
higher luminance values compared to the yellow morph
(Galarza et al. 2014).
model using both predation and mating
results
We consequently built our model assuming that the 60
sites sampled above represent the range of naturally
occurring spatial variation in morph-specific viabilities, as
estimated in Nokelainen et al. 2014. We considered a
world consisting of 60 patches, each producing 50 off-
spring in each generation. We only tracked the dynamics
of males, that is we assume that male offspring morph
frequencies are proportional to the frequency with which
males of each morph become sires (this only requires
assuming that inheritance via females does not bias pat-
terns of inheritance in either direction).
Given that differential predation based on wing colour
occurs during the adult time period, morph ratios are not
necessarily constant and the model needs to track morph
frequencies at the time when siring occurs. Having no pre-
cise information of this time dependency, we use the fol-
lowing logic to simulate the most likely pattern. Denote
by b
i
the survival advantage of the yellow morph in a cur-
rent patch i(e.g. if site 13 has b
13
=121 then in this site
a yellow individual’s daily risk of dying is 1/1121, that is
a fraction 089 of that of a white individual). Conse-
quently, if a local population starts with w
0
whites and y
0
yellows (the subscript 0 denoting that no male has had
the time to die yet), the probability that the next death
targets a yellow male is (y
0
/b)/[(y
0
/b)+w
0
], and the comple-
mentary probability that the next removed male is white
is w
0
/[(y
0
/b)+w
0
]. Thus, if a uniformly distributed random
number in the range [0,1] falls below (y
0
/b)/[(y
0
/b)+w
0
], we
subtract one individual from the local y(thus y
1
=y
0
1,
w
1
=w
0
), and otherwise from the local w(thus y
1
=y
0
,
and w
1
=w
0
1). We repeat this procedure until no males
of either morph are alive.
We then assume that females largely mate when mates
are numerous (i.e. mostly when the season is not nearly
over yet) and choose the mating time index of each female
by rounding down a random number that is exponentially
distributed with mean (y
0
+w
0
)/10. This result, denoted t,
describes that a female mates at a point in time when t
males have died and y
t
and w
t
are consequently still avail-
able for matings. The female mating time is thus designed
to follow mate availability, and the factor 10 was set to
make the proportion of females that attempt to mate when
no males are alive negligibly low (for y
0
+w
0
50 which
according to our assumptions is the approximate size of
local populations, this probability i.e. the probability
that the exponential distribution with mean (y
0
+w
0
)/10
produces a value that exceeds y
0
+w
0
, the number of deaths
it takes for all males to have died is approximately
045 910
5
). We assume that these exceedingly rare late
females in reality mate with the last available male, while
noting that our results remain virtually unchanged if we
instead assume that they completely fail to mate, as the
siring success this late in the season contributes minimally
to the mating success of either of the male morphs.
Populations were initiated such that 250 yellow and 250
white males were distributed randomly across the 60
patches, to yield initial patch-specific y
0
and w
0
values.
The above procedure was then used within each subpopu-
lation to determine siring times for 50 surviving offspring
per patch (for those patches that had at least one male;
we thus implicitly evoke density dependence: each occu-
pied patch is equally productive). We equate survival with
maturation.
The morph identity of each of the 50 sires was deter-
mined based on y
t
and w
t
at the siring time t, such that
Prob foffspring is yellowx
xþ1xðÞeaxþb:
Here, x=y
t
/(y
t
+w
t
) is the proportion of yellows in the
current population of potential sires. The parameters a
and bdefine the relative mating success advantage of
whites, determined by a least-squares regression of log
(mean eggs sired by white
mean eggs sired by yellow), values taken from the empirical part
of this paper against the treatment xvalues (x=1/3, 1/2
and 2/3) used in the experiments. Because a few females
mated once with a yellow and once with a white male, we
computed three different values for aand b, to cover the
entire range of uncertainty caused by this behaviour: (i)
the first regression assumed that these females all con-
tributed only to their white mate’s success, (ii) the second
assumed that these females all contributed only to their
yellow mate’s success, and (iii) the third assumed that
these females had half their eggs sired by the white mate,
and half by the yellow mate.
This procedure of determining offspring morph was
repeated across all patches. We then assumed that a pro-
portion dof offspring disperse, and others stay in their
current patch. A dispersed offspring was assumed to land
in any other than its natal patch. Dispersal completed a
generation, and the entire procedure was then run for
1000 generations for a variety of different values of d, for
each of the assumptions (i), (ii) and (iii).
model results
We depict a large collection of single-run outcomes at
generation 1000 rather than averaging over several repli-
cates per parameter value. The latter approach would not
be able to distinguish between a scenario with alternative
non-polymorphic equilibria and a protected polymor-
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society, Journal of Animal Ecology
6S. P. Gordon et al.
phism (e.g. 05 could then, confusingly, mean either
equally many ‘yellow fix’ and ‘white fix’ cases, or all runs
having stabilized at a yellow-white polymorphism). Our
approach shows that a polymorphism would never be
maintained if the populations were assumed panmictic
(d=1) or, more generally, if the dispersal rate dexceeded
approximately 02 (Fig. 2). The model then mostly pre-
dicts that the yellow morph disappears, but this conclu-
sion proved sensitive to how we assumed paternity to be
divided in those cases when a female mated multiply. If
we made the yellow-favouring assumption, then some-
times the yellow morph fixed (Fig. 2), and polymorphism
also prevailed at slightly higher values of dthan in the
other cases.
When dispersal was less frequent (d<02), the model’s
behaviour was consistent across a large range of dispersal
rates and also across the different assumptions regarding
multiple mating. Both morphs persisted, with no clear
trend other than that if a morph was assumed to gain
more paternity with doubly mated females in our estima-
tion of aand b, this morph was able to shift its frequency
somewhat upwards from the scenario of equal paternity
(the difference between the open and filled symbols in
Fig. 2). Thus, we predicted an approximate 1 : 1 morph
ratio when we made the yellow-favouring assumption,
approximately 40% yellow males when we made the equal
paternity assumption, and approximately 30% yellow
males when we made the white-favouring assumption.
Discussion
Aposematism is assumed, and in many organisms shown,
to be under positive frequency-dependent selection leading
to monomorphism (Mallet & Barton 1989; Lindstr
om
et al. 2001). In our study system, the wood tiger moth,
the more conspicuous yellow male morph, survives as a
whole better against predators than the white male morph
(Nokelainen et al. 2012). However, it appears that this
survival advantage is dependent on the local predator
community (Nokelainen et al. 2014). In our case, this is
important because male fitness proves to have not only
one (predation), but potentially two (predation and sexual
selection) positively frequency-dependent components.
Our enclosure experiment shows that white males have
an advantage over yellow males in mating probabilities,
but this appears to occur only at high frequencies of white
males. However, when we analyse overall individual fit-
ness, both morphs have an advantage when common that
disappears when at a balanced ratio. These results may
overall suggest some sampling artefact where there is a
higher probability of finding higher quality males in the
high-frequency morph group. However, this reason seems
unlikely because aspects of male quality shown to affect
mating success in the past (male age and size) were
already included in our analyses to test their effects; and
only male age had a small treatment effect (and only in
the Y-biased treatment). Instead, two plausible and not
mutually exclusive reasons could be responsible for our
results.
First, both morphs could trade off on certain aspects of
reproduction. For example, yellow males have low mating
success when in white male-dominated environments, but
compensate for this by siring more eggs and having a
higher hatching success of offspring compared to white
males (see Appendix S1, Supporting Information). This
difference in strategy could be related to morph-related
differences in fitness-related traits we have not measured
here. For example, a recent study found that white wood
tiger moth males fly for longer stretches of time, whereas
yellow males tend to focus their flying around the peak
calling activity of female moths (Rojas et al. In review).
This is probably due to the white males compensating
their less efficient signal to predators by increased to flight
to escape predation attempts, or yellow males being lim-
ited in flight because of physiological limitations from
producing their more efficient, yet costly chemical defence
(Rojas et al. unpublished data). Regardless of the specific
reason that difference in flight activity between the two
morphs may lead to disproportionate chances for the
white morph to achieve more matings, especially when
common, and in return select over time for the yellow
males who leave more sired eggs once they achieve mat-
ing.
Secondly, wood tiger moths may display flexible mating
preferences, depending on morph frequencies, which
would have led to our results. Sampling of natural popu-
lations shows that most populations of wood tiger moths
have an admixture of both morphs (Hegna, Galarza &
Mappes 2015). For example, in Finland alone, there are
populations that are white dominated (such as in Central
Finland where much of our laboratory stock in this
experiment was taken from) and others that are yellow
dominated (Southern Finland), and much gene flow
occurs between populations (Nokelainen et al. 2012;
Galarza et al. 2014). Adaptive coloration also varies spa-
tially as well as temporally in our system, and viability
strongly favours one morph over the other via predation,
immunocompetence response to disease (Nokelainen,
Lindstedt & Mappes 2013) and potentially other pres-
sures. This may make it adaptive to avoid mating with
rare morphs, potentially explaining why female wood
tiger moths in our experiment appear to either choose
mates (or lay more eggs) for the male morph with the
more common phenotype (i.e. the morph with seemingly
higher viability). Short-lived polyandrous species like
wood tiger moths may easily track male morph frequen-
cies via the social interactions that occur between calling
females and courting males (McLain 2005; Westerman
et al. 2014).
Some examples of flexible mate choice have been con-
firmed experimentally, and in each case, its occurrence is
linked with systems that have natural variations in morph
frequencies. For example, female soldier beetles (Chauliog-
nathus pennsylvanicus) possess flexible mate preferences
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society, Journal of Animal Ecology
Positive frequency dependence and polymorphism 7
flectance) have been found to actually attract attacks by
these predators (Lyytinen et al. 2001; Lyytinen, Lind-
str
om & Mappes 2004). On the other hand, dunnocks
(Prunellidae) tend to avoid white male moths and gener-
ally forage closer to the ground level in shaded boreal for-
ests. White coloration might be a more effective warning
signal in these circumstances because they have much
higher luminance values compared to the yellow morph
(Galarza et al. 2014).
model using both predation and mating
results
We consequently built our model assuming that the 60
sites sampled above represent the range of naturally
occurring spatial variation in morph-specific viabilities, as
estimated in Nokelainen et al. 2014. We considered a
world consisting of 60 patches, each producing 50 off-
spring in each generation. We only tracked the dynamics
of males, that is we assume that male offspring morph
frequencies are proportional to the frequency with which
males of each morph become sires (this only requires
assuming that inheritance via females does not bias pat-
terns of inheritance in either direction).
Given that differential predation based on wing colour
occurs during the adult time period, morph ratios are not
necessarily constant and the model needs to track morph
frequencies at the time when siring occurs. Having no pre-
cise information of this time dependency, we use the fol-
lowing logic to simulate the most likely pattern. Denote
by b
i
the survival advantage of the yellow morph in a cur-
rent patch i(e.g. if site 13 has b
13
=121 then in this site
a yellow individual’s daily risk of dying is 1/1121, that is
a fraction 089 of that of a white individual). Conse-
quently, if a local population starts with w
0
whites and y
0
yellows (the subscript 0 denoting that no male has had
the time to die yet), the probability that the next death
targets a yellow male is (y
0
/b)/[(y
0
/b)+w
0
], and the comple-
mentary probability that the next removed male is white
is w
0
/[(y
0
/b)+w
0
]. Thus, if a uniformly distributed random
number in the range [0,1] falls below (y
0
/b)/[(y
0
/b)+w
0
], we
subtract one individual from the local y(thus y
1
=y
0
1,
w
1
=w
0
), and otherwise from the local w(thus y
1
=y
0
,
and w
1
=w
0
1). We repeat this procedure until no males
of either morph are alive.
We then assume that females largely mate when mates
are numerous (i.e. mostly when the season is not nearly
over yet) and choose the mating time index of each female
by rounding down a random number that is exponentially
distributed with mean (y
0
+w
0
)/10. This result, denoted t,
describes that a female mates at a point in time when t
males have died and y
t
and w
t
are consequently still avail-
able for matings. The female mating time is thus designed
to follow mate availability, and the factor 10 was set to
make the proportion of females that attempt to mate when
no males are alive negligibly low (for y
0
+w
0
50 which
according to our assumptions is the approximate size of
local populations, this probability i.e. the probability
that the exponential distribution with mean (y
0
+w
0
)/10
produces a value that exceeds y
0
+w
0
, the number of deaths
it takes for all males to have died is approximately
045 910
5
). We assume that these exceedingly rare late
females in reality mate with the last available male, while
noting that our results remain virtually unchanged if we
instead assume that they completely fail to mate, as the
siring success this late in the season contributes minimally
to the mating success of either of the male morphs.
Populations were initiated such that 250 yellow and 250
white males were distributed randomly across the 60
patches, to yield initial patch-specific y
0
and w
0
values.
The above procedure was then used within each subpopu-
lation to determine siring times for 50 surviving offspring
per patch (for those patches that had at least one male;
we thus implicitly evoke density dependence: each occu-
pied patch is equally productive). We equate survival with
maturation.
The morph identity of each of the 50 sires was deter-
mined based on y
t
and w
t
at the siring time t, such that
Prob foffspring is yellowx
xþ1xðÞeaxþb:
Here, x=y
t
/(y
t
+w
t
) is the proportion of yellows in the
current population of potential sires. The parameters a
and bdefine the relative mating success advantage of
whites, determined by a least-squares regression of log
(mean eggs sired by white
mean eggs sired by yellow), values taken from the empirical part
of this paper against the treatment xvalues (x=1/3, 1/2
and 2/3) used in the experiments. Because a few females
mated once with a yellow and once with a white male, we
computed three different values for aand b, to cover the
entire range of uncertainty caused by this behaviour: (i)
the first regression assumed that these females all con-
tributed only to their white mate’s success, (ii) the second
assumed that these females all contributed only to their
yellow mate’s success, and (iii) the third assumed that
these females had half their eggs sired by the white mate,
and half by the yellow mate.
This procedure of determining offspring morph was
repeated across all patches. We then assumed that a pro-
portion dof offspring disperse, and others stay in their
current patch. A dispersed offspring was assumed to land
in any other than its natal patch. Dispersal completed a
generation, and the entire procedure was then run for
1000 generations for a variety of different values of d, for
each of the assumptions (i), (ii) and (iii).
model results
We depict a large collection of single-run outcomes at
generation 1000 rather than averaging over several repli-
cates per parameter value. The latter approach would not
be able to distinguish between a scenario with alternative
non-polymorphic equilibria and a protected polymor-
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society, Journal of Animal Ecology
6S. P. Gordon et al.
sity of Jyv
askyl
a were also kind to read and comment on earlier versions
of this manuscript. Funding was provided by the Academy of Finland via
the Centre of Excellence in Biological Interactions (Project: 2100000256 to
J.M. and Project: 21000027441 to S.G.).
Data accessibility
Data available from the Dryad Digital Repository: http://dx.doi.org/
10.5061/dryad.nn493 (Gordon et al. 2015).
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Received 15 January 2015; accepted 22 June 2015
Handling Editor: Stewart Plaistow
Supporting Information
Additional Supporting Information may be found in the online version
of this article.
Appendix S1. Egg number and hatching success.
©2015 The Authors. Journal of Animal Ecology ©2015 British Ecological Society, Journal of Animal Ecology
10 S. P. Gordon et al.
... For example temporally and spatially varying interspecific interactions can result in geographically variable patterns of polymorphism (McLean & Stuart-Fox 2014), particularly when coupled with limited amounts of gene flow between differentially selected populations (e.g. Merilaita, 2001;Gordon et al., 2015;Aubier and Sherratt, 2015). Often these mechanisms are thought to act simultaneously, or alternate in time or space Gray and McKinnon, 2007;Stevens and Ruxton, 2012) creating a geographic mosaic of selection (Thompson, 2005). ...
... Although both theoretical (e.g. Gordon et al., 2015;Aubier and Sherratt, 2015;Holmes et al., 2017) and experimental work (e.g. Willink et al., 2014;Aluthwattha et al., 2017) have identified several mechanisms that allow multiple morphs to persist, there is no conclusive evidence from the field and the relative importance of different selective agents is not well understood (Stevens and Ruxton, 2012;Chouteau et al., 2016). ...
... The variation in the degree of warning colour polymorphism shown by the wood tiger moth (Arctia plantaginis) across the Western Palaearctic provides an excellent system to study how warning signal variation is maintained in the wild (Hegna et al., 2015). At a local scale, predator community structure and sexual selection Gordon et al., 2015) have been found to alter the direction of selection on white and yellow male morphs, but no previous studies have addressed selection on a wide geographical scale and including A. plantaginis females, which are red or yellow. We exposed artificial moths representing the three hindwing colour morphs (white, yellow, red), to local predators in a field experiment spanning across four countries, while monitoring the abundance and community structure of local predator species. ...
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Warning signals are predicted to develop signal monomorphism via positive frequency‐dependent selection (+FDS) albeit many aposematic systems exhibit signal polymorphism. To understand this mismatch, we conducted a large‐scale predation experiment in four countries, among which the frequencies of hindwing warning coloration of the aposematic moth, Arctia plantaginis, differ. Here we show that selection by avian predators on warning colour is predicted by local morph frequency and predator community composition. We found +FDS to be the strongest in monomorphic Scotland and lowest in polymorphic Finland, where the attack risk of moth morphs depended on the local avian community. +FDS was also found where the predator community was the least diverse (Georgia), whereas in the most diverse avian community (Estonia), hardly any models were attacked. Our results support the idea that spatial variation in predator communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection. A geographic mosaic of selection by predators could explain the paradoxical maintenance of warning signal variation, but direct ecological evidence is scarce and focused on tropical systems. We monitored local avian predators and attacks on 4000 + moth models representing red, yellow or white warning colour morphs in a temperate moth system with natural variation in local morph frequencies. We found positive frequency‐dependent selection to be strongest in monomorphic populations and the direction and strength of selection to be significantly associated with local predator community composition and diversification, which can explain not only geographic variation (polytypism) but also local polymorphism when coupled with gene flow.
... By using real individuals, and a spatial scale that allowed for clear observations of predator attacks and behavior, we found that wood tiger moths with white and red hindwing warning coloration showed a strong survival advantage when common, while the survival of the yellow color morph was not significantly affected by its frequency. Our findings support a recent study using moth plasticine models in the field (Rönkä et al., 2020), a previous spatial model (Gordon et al., 2015) in the system, and others outside of the system (e.g. Chouteau et al. 2016) which suggest that warning signals are subject to positive frequency dependent selection. ...
... While a generalist feeder, the wood tiger moth often shows a patchy distribution, and patches of different morph frequencies can occur on the local scale by chance. We know from prior experiments that positive frequency dependent mating selection Gordon et al., 2015), thermoregulation (Hegna et al., 2013), and predator community structure Rönkä et al., 2020), among other factors, have been found to directionally shift selection favoring either white or yellow male morphs in different patches. A spatial model parameterized with positive frequency dependence and varying predator communities, combined with small levels of gene flow between the spatial patches favoring one morph over another, showed for the first time that hindwing polymorphism can indeed persist under these conditions in this system (Gordon et al., 2015). ...
... We know from prior experiments that positive frequency dependent mating selection Gordon et al., 2015), thermoregulation (Hegna et al., 2013), and predator community structure Rönkä et al., 2020), among other factors, have been found to directionally shift selection favoring either white or yellow male morphs in different patches. A spatial model parameterized with positive frequency dependence and varying predator communities, combined with small levels of gene flow between the spatial patches favoring one morph over another, showed for the first time that hindwing polymorphism can indeed persist under these conditions in this system (Gordon et al., 2015). This gives even more weight to these fine-scale results. ...
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Polymorphic warning signals in aposematic systems are enigmatic because predator learning should favor the most common form, creating positive frequency-dependent survival. However, many populations exhibit variation in warning signals. There are various selective mechanisms that can counter positive frequency-dependent selection and lead to temporal or spatial warning signal diversification. Examining these mechanisms and their effects requires first confirming whether the most common morphs are favored at both local and regional scales. Empirical examples of this are uncommon and often include potentially confounding factors, such as a lack of knowledge of predator identity and behavior. We tested how bird behavior influences the survival of three coexisting morphs of the aposematic wood tiger moth Arctia plantaginis offered to a sympatric predator (great tit Parus major) at different frequencies. We found that although positive frequency-dependent selection is present, its strength is affected by predator characteristics and varying prey profitability. These results highlight the need to understand predator foraging in natural communities with variable prey defenses in order to better examine how behavioral interactions shape evolutionary outcomes.
... Experiments in more natural conditions where females have had a choice between several males suggest that variation in the reproductive success of white and yellow males is likely to be more complex and vary depending on the frequency of the male morphs (Gordon et al. 2015). Gordon et al. showed that the more frequent morph (white or yellow) had an advantage in mating success, but this advantage disappeared when the frequency of white and yellow males was more balanced (Gordon et al. 2015). ...
... Experiments in more natural conditions where females have had a choice between several males suggest that variation in the reproductive success of white and yellow males is likely to be more complex and vary depending on the frequency of the male morphs (Gordon et al. 2015). Gordon et al. showed that the more frequent morph (white or yellow) had an advantage in mating success, but this advantage disappeared when the frequency of white and yellow males was more balanced (Gordon et al. 2015). In future research, it would be important to test the effect of retaining the abdominal fluid until the mating is in a more natural setup where female choice and possible male-male competition between white and yellow males is not excluded. ...
... For example, in a previous experiment by (Nokelainen et al. 2012), white and yellow males differed in their probability to mate, which we did not measure here. We could expect to find lower mating success for depleted individuals but potentially also differences between yellow and white males that are not necessarily visible under laboratory conditions in no-choice mating experiments (Nokelainen et al. 2012;Gordon et al. 2015;Dougherty 2020). ...
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To understand how variation in warning displays evolves and is maintained, we need to understand not only how perceivers of these traits select color and toxicity but also the sources of the genetic and phenotypic variation exposed to selection by them. We studied these aspects in the wood tiger moth Arctia plantaginis, which has two locally co-occurring male color morphs in Europe: yellow and white. When threatened, both morphs produce defensive secretions from their abdomen and from thoracic glands. Abdominal fluid has shown to be more important against invertebrate predators than avian predators, and the defensive secretion of the yellow morph is more effective against ants. Here, we focused on the morph-linked reproductive costs of secretion of the abdominal fluid and quantified the proportion of phenotypic and genetic variation in it. We hypothesized that, if yellow males pay higher reproductive costs for their more effective aposematic display, the subsequent higher mating success of white males could offer one explanation for the maintenance of the polymorphism. We first found that the heritable variation in the quantity of abdominal secretion was very low (h2 = 0.006) and the quantity of defensive secretion was not dependent on the male morph. Second, deploying the abdominal defensive secretion decreased the reproductive output of both color morphs equally. This suggests that potential costs of pigment production and chemical defense against invertebrates are not linked in A. plantaginis. Furthermore, our results indicate that environmentally induced variation in chemical defense can alter an individual's fitness significantly.
... From an evolutionary standpoint, it is plausible that interplay between natural and sexual selection facilitates polymorphism in this species (Gordon et al., 2015Nokelainen et al., 2012;Rönkä et al., 2020). Since male wood tiger moths, which are actively searching for females in the vegetation, have limited ability to see differences in yellow-orange-red hues (Henze et al., 2018), it is unlikely that sexual selection alone would be responsible for the colouration of females, but we cannot exclude the possibility that male colouration could be used in intraspecific commu- For tetrachromatic avian vision uv, sw and lw sensitivities were used for blue, green and red channels respectively. ...
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The definition of colour polymorphism is intuitive: genetic variants express discretely coloured phenotypes. This classification is, however, elusive as humans form subjective categories or ignore differences that cannot be seen by human eyes. We demonstrate an example of a 'cryptic morph' in a polymorphic wood tiger moth (Arctia plantaginis), a phenomenon that may be common among well-studied species. We used pedigree data from nearly 20,000 individuals to infer the inheritance of hindwing colouration. The evidence supports a single Mendelian locus with two alleles in males: WW and Wy produce the white and yy the yellow hindwing colour. The inheritance could not be resolved in females as their hindwing colour varies continuously with no clear link with male genotypes. Next, we investigated if the male genotype can be predicted from their phenotype by machine learning algorithms and by human observers. Linear discriminant analysis grouped male genotypes with 97% accuracy, whereas humans could only group the yy genotype. Using vision modelling, we also tested whether the genotypes have differential discriminability to humans, moth conspecifics and their bird predators. The human perception was poor separating the genotypes, but avian and moth vision models with ultraviolet sensitivity could separate white WW and Wy males. We emphasize the importance of objective methodology when studying colour polymorphism. Our findings indicate that by-eye categorization methods may be problematic, because humans fail to see differences that can be visible for relevant receivers. Ultimately, receivers equipped with different perception than ours may impose selection to morphs hidden from human sight.
... From an evolutionary standpoint, it is plausible that interplay between natural and sexual selection facilitates polymorphism in this species (Gordon et al., 2015Nokelainen et al., 2012;Rönkä et al., 2020). Since male wood tiger moths, which are actively searching for females in the vegetation, have limited ability to see differences in yellow-orange-red hues (Henze et al., 2018), it is unlikely that sexual selection alone would be responsible for the colouration of females, but we cannot exclude the possibility that male colouration could be used in intraspecific commu- For tetrachromatic avian vision uv, sw and lw sensitivities were used for blue, green and red channels respectively. ...
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Phenotypic variation is suggested to facilitate the persistence of environmentally growing pathogens under environmental change. Here we hypothesized that the intensive farming environment induces higher phenotypic variation in microbial pathogens than natural environment, because of high stochasticity for growth and stronger survival selection compared to the natural environment. We tested the hypothesis with an opportunistic fish pathogen Flavobacterium columnare isolated either from fish farms or from natural waters. We measured growth parameters of two morphotypes from all isolates in different resource concentrations and two temperatures relevant for the occurrence of disease epidemics at farms and tested their virulence using a zebrafish (Danio rerio) infection model. According to our hypothesis, isolates originating from the fish farms had higher phenotypic variation in growth between the morphotypes than the isolates from natural waters. The difference was more pronounced in higher resource concentrations and the higher temperature, suggesting that phenotypic variation is driven by the exploitation of increased outside‐host resources at farms. Phenotypic variation of virulence was not observed based on isolate origin but only based on morphotype. However, when in contact with the larger fish, the less virulent morphotype of some of the isolates also had high virulence. As the less virulent morphotype also had higher growth rate in outside‐host resources, the results suggest that both morphotypes can contribute to F. columnare epidemics at fish farms, especially with current prospects of warming temperatures. Our results suggest that higher phenotypic variation per se does not lead to higher virulence, but that environmental conditions at fish farms could select isolates with high phenotypic variation in bacterial population and hence affect evolution in F. columnare at fish farms. Our results highlight the multifaceted effects of human‐induced environmental alterations in shaping epidemiology and evolution in microbial pathogens.
... For example, key factors such as the life stage that expresses warning signals (larval vs. adult) (Willmott et al. 2011;Gaitonde et al. 2018) could have profound impacts on color evolution that are not typically considered in models for warning color evolution. Specifically, adult coloration of many aposematic taxa is often subject to positive frequency-dependent selection via not only predator learning, but also positive assortative mating by color (Summers et al. 1999;Jiggins et al. 2001;Reynolds and Fitzpatrick 2007;Gordon et al. 2015). Color-based mating preferences in the adults can impact warning coloration evolution in two ways. ...
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Our understanding of how novel warning color traits evolve in natural populations is largely based on studies of reproductive stages and organisms with endogenously produced pigmentation. In these systems, genetic drift is often required for novel alleles to overcome strong purifying selection stemming from frequency‐dependent predation and positive assortative mating. Here, we integrate data from field surveys, predation experiments, population genomics, and phenotypic correlations to explain the origin and maintenance of geographic variation in a diet‐based larval pigmentation trait in the redheaded pine sawfly (Neodiprion lecontei), a pine‐feeding hymenopteran. Although our experiments confirm that N. lecontei larvae are indeed aposematic—and therefore likely to experience frequency‐dependent predation—our genomic data do not support a historical demographic scenario that would have facilitated the spread of an initially deleterious allele via drift. Additionally, significantly elevated differentiation at a known color locus suggests that geographic variation in larval color is currently maintained by selection. Together, these data suggest that the novel white morph likely spread via selection. However, white body color does not enhance aposematic displays, nor is it correlated with enhanced chemical defense or immune function. Instead, the derived white‐bodied morph is disproportionately abundant on a pine species with a reduced carotenoid content relative to other pine hosts, suggesting that bottom‐up selection via host plants may have driven divergence among populations. Overall, our results suggest that life stage and pigment source can have a substantial impact the evolution of novel warning signals, highlighting the need to investigate diverse aposematic taxa to develop a comprehensive understanding of color variation in nature. This article is protected by copyright. All rights reserved
... Color polymorphism is defined as the sympatric coexistence of multiple discrete color variants in interbreeding populations independent of sex, age, and other state-dependent modifiers (Ford 1945). Multiple mechanisms can contribute to the balanced maintenance of color polymorphisms, including spatially heterogeneous selection in populations connected by gene flow (Hedrick et al. 1976;Hedrick 2006;Gordon et al. 2015), temporally fluctuating selection (Siepielski et al. 2009;Bell 2010), pleiotropic fitness trade-offs across different contexts (Roff and Fairbairn 2007), disassortative mating preferences (Roulin and Bize 2007;Wellenreuther et al. 2014), and negative-frequency dependent selection (for example by predators that form search images, Bond andKamil 1998, 2006;Bond 2007;Ruxton et al. 2019). But also matching habitat choice can contribute to the maintenance of phenotypic polymorphisms by equalizing fitness differences. ...
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Orthopteran insects are characterized by high variability in body coloration, in particular featuring a widespread green-brown color polymorphism. The mechanisms that contribute to the maintenance of this apparently balanced polymorphism are not yet understood. To investigate whether morph-dependent microhabitat choice might contribute to the continued coexistence of multiple morphs, we studied substrate choice in the meadow grasshopper Pseudochorthippus parallelus. The meadow grasshopper occurs in multiple discrete, genetically determined color morphs that range from uniform brown to uniform green. We tested whether three common morphs preferentially choose differently colored backgrounds in an experimental arena. We found that a preference for green backgrounds was most pronounced in uniform green morphs. If differential choices improve morph-specific performance in natural habitats via crypsis and/or thermoregulatory benefits, they could help to equalize fitness differences among color morphs and potentially produce frequency-dependent microhabitat competition, though difference appear too small to serve as the only explanation. We also measured the reflectance of the grasshoppers and backgrounds and used visual modeling to quantify the detectability of the different morphs to a range of potential predators. Multiple potential predators, including birds and spiders, are predicted to distinguish between morphs chromatically, while other species, possibly including grasshoppers themselves, will perceive only differences in brightness. Our study provides the first evidence that morph-specific microhabitat choice might be relevant to the maintenance of the green-brown polymorphisms in grasshoppers and shows that visual distinctness of color morphs varies between perceivers.
... In contrast, the temperate population studied here shows more continuous colour variation in both sexes, although mean male iridescent coverage remains higher than that of females. If these patterns are the result of differing selection pressures, be they natural or sexual, limited gene flow between the populations could maintain variation (Gordon et al., 2015). However, this pattern is further complicated by the temperature sensitive plasticity in coloration. ...
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Despite the fact their coloration functions as an aposematic signal, and is thus expected to be under stabilizing selection, hibiscus harlequin bugs (Tectocoris diophthalmus) show an impressive level of variation in their iridescent coloration both within and between populations. To date the heritability of coloration in this species remains unknown. Here we focus on a single population in New South Wales (the southern part of this species’ Australian range), with the greatest colour variation. We reared full-sib families of known pedigree in the laboratory and analysed the extent of iridescent coloration at adulthood. We then looked for evidence of heritability, condition dependence and antagonistic sexual selection acting on colour in this species. We found significant heritability in the extent of iridescent coloration for both sexes, as well as in development time and body size, but no evidence that condition dependence played a role in the determination of adult coloration. There was, however, a sex by genotype interaction for iridescent cover, in the form of a negative intersexual genetic correlation: in families where sons had high iridescent cover the daughters had low, and vice versa. Our results suggest that different selective pressures may act on coloration in males and females of this species.
... In invertebrates, such as beetles, Heliconius butterflies and day-flying moths, studies focus mostly on predator-imposed frequency-dependent selection on color variation. How variation in color interacts with chemical signals, such as those used as chemical defenses against predators, and sex pheromones, is now starting to be investigated (Gordon et al., 2015;Rojas et al., 2019). ...
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Colour is often used as an aposematic warning signal, with predator learning expected to lead to a single colour pattern within a population. However, there are many puzzling cases where aposematic signals are also polymorphic. The wood tiger moth, Arctia plantaginis , uses bright hindwing colours as a signal of unpalatability, and males have discrete colour morphs which vary in frequency geographically. In Finland, both white and yellow morphs can be found, and these colour morphs also differ in behavioural and life-history traits. Complex polymorphisms such as these are often explained by supergenes. Here, we show that male colour is linked to an extra copy of a yellow family gene that is only present in the white morphs. This white-specific duplication, which we name valkea , is highly upregulated during wing development, and could act to reduce recombination, thus potentially representing a supergene. We also characterise the pigments responsible for yellow, white and black colouration, showing that yellow is partly produced by pheomelanins, while black is dopamine-derived eumelanin. The yellow family genes have been linked to melanin synthesis and behavioural traits in other insect species. Our results add to only a few examples of seemingly paradoxical and complex polymorphisms which are associated with single genes.
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Muller's theory of warning color and mimicry, despite forming a textbook example of frequency-dependent selection, has rarely been demonstrated in the wild. This may be largely due to the practical and statistical difficulties of measuring natural selection on mobile prey species. Here we demonstrate that this selection acts in alpine beetle communities by using tethered beetles exposed to natural predators. Oreina gloriosa leaf beetles (Coleoptera: Chrysomelidae) possess chemical defense in the form of cardenolides, accompanied by what appears to be warning color in bright metallic blues and greens. Individuals that match the locally predominant color morph have increased survival, with odds of week-long survival increased by a factor of 1.67 over those that do not match. This corresponds to selection of 13% against foreign morphs. Such selection, acting in concert with variation in community composition, could be responsible for geographic variation in warning color. However, in the face of this purifying selection, the within-population polymorphism seen in many Oreina species remains paradoxical.
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Colour polymorphisms (CP's) continue to be of interest to evolutionary biologists because of their general tractability, importance in studies of selection and potential role in speciation. Since some of the earliest studies of CP, it has been evident that alternative colour morphs often differ in features other than colour. Here we review the rapidly accumulating evidence concerning the genetic mechanisms underlying correlations between CP and other traits in animals. We find that evidence for genetic correlations is now available for taxonomically diverse systems and that physical linkage and regulatory mechanisms including transcription factors, cis-regulatory elements, and hormone systems provide pathways for the ready accumulation or modification of these correlations. Moreover, physical linkage and regulatory mechanisms may both contribute to genetic correlation in some of the best-studied systems. These results raise the possibility that negative frequency-dependent selection and disruptive selection might often be acting on suites of traits and that the cumulative effects of such selection, as well as correlational selection, may be important to CP persistence and evolution. We consider additional evolutionary implications. We recommend continued efforts to elucidate the mechanisms underlying CP-correlated characters and the more frequent application of comparative approaches, looking at related species that vary in character correlations and patterns of selection. We also recommend efforts to elucidate how frequency-dependent selection may act on suites of characters.
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Insect communities consist of aposematic species with efficient warning colours against predation, as well as abundant examples of crypsis. To understand such coexistence, we here report results from a field experiment where relative survival of artificial larvae, varying in conspicuousness, was estimated in natural bird communities over an entire season. This takes advantage of natural variation in the proportion of naive predators: naivety peaks when young birds have just fledged. We show that the relative benefit of warning signals and crypsis changes accordingly. When naive birds are rare (early and late in the season), conspicuous warning signals improve survival, but conspicuousness becomes a disadvantage near the fledging time of birds. Such temporal structuring of predator-prey relationships facilitates the coexistence of diverse antipredatory strategies and helps explain two patterns we found in a 688-species community of Lepidoterans: larval warning signals remain rare and occur disproportionately often in seasons when predators are educated.
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Many plants and animals advertise unpalatability through warning signals in the form of colour and shape. Variation in warning signals within local populations is not expected because they are subject to directional selection. However, mounting evidence of warning signal variation within local populations suggests that other selective forces may be acting. Moreover, different selective pressures may act on the individual components of a warning signal. At present, we have a limited understanding about how multiple selection processes operate simultaneously on warning signal components, and even less about their temporal and spatial dynamics. Here, we examined temporal variation of several wing warning signal components (colour, UV reflectance, signal size, and pattern) of two co-occurring colour morphs of the aposematic wood tiger moth (Parasemia plantaginis). Sampling was done in four geographic regions over three consecutive years. We also evaluated each morph's temporal genetic structure by analysing mitochondrial sequence data and nuclear microsatellite markers. Our results revealed temporal differences between the morphs for most signal components measured. Moreover, variation occurred differently in the fore- and hindwings. We found no differences in the genetic structure between the morphs within years and regions, suggesting single local populations. However, local genetic structure fluctuated temporally. Negative correlations were found between variation produced by neutrally evolving genetic markers and those of the different signal components, indicating a non-neutral evolution for most warning signal components. Taken together, our results suggest that differential selection on warning signal components and fluctuating population structure can be one explanation for the maintenance of warning signal variation in this aposematic species.This article is protected by copyright. All rights reserved.
Article
AimTo investigate the phylogeography of the aposematic wood tiger moth (Parasemia plantaginis) across its Holarctic distribution and to explore how its genetic structure relates to geographical differences in hindwing warning coloration of males and females. Males have polymorphic hindwing coloration, while female hindwing coloration varies continuously, but no geographical analyses of coloration or genetic structure exist.LocationThe Holarctic.Methods We sequenced a fragment of the mitochondrial cytochrome c oxidase subunit I gene (COI) from 587 specimens. We also examined more current population structure by genotyping 569 specimens at 10 nuclear microsatellite loci. Species distribution modelling for present conditions and the Last Glacial Maximum (LGM) was performed to help understand genetic structure. Geographical patterns in hindwing warning coloration were described from 1428 specimens and compared to the genetic analyses.ResultsWe found only two instances of genetic divergence that coincided with distinct, yet imperfect, shifts in male hindwing coloration in the Caucasus region and Japan. A shift in female hindwing colour did not appear to be associated with genetic structure. A change from sexual monomorphism to sexual dimorphism was also observed. Mitogenetic (mtDNA) structure does not show the influence of glacial refugia during the LGM. Climate shifts following the LGM appear to have isolated the red Caucasus populations and other southerly populations. Populations at opposite ends of the moth's distribution showed high levels of differentiation in the microsatellite data analysis compared to the shallow mitogenetic structure, supporting a more recent divergence.Main conclusionsParasemia plantaginis populations appeared to have been historically well connected, but current populations are much more differentiated. This raises the possibility that incipient speciation may be occurring in portions of the species' distribution. Some changes in colour align to genetic differences, but others do not, which suggests a role for selective and non-selection based influences on warning signal variation.
Article
(1) Predation experiments were carried out in which frozen dead melanic and typical individuals of Biston betularia, Allophyes oxyacanthae and Diurnea fagella were exposed on trees at several different sites. For each species, the results of the experiments demonstrated selective predation of the morphs. In urban areas the melanic morphs were at an advantage over the typical form but this advantage was reduced or even reversed in more rural areas. (2) A mark/release experiment with D. fagella gave evidence of the differential survival of the melanic and typical forms and this, together with the results of the predation experiments carried out at the same site, indicated the importance of selective predation for a population under natural conditions. (3) Estimates were made of the relative crypsis of the morphs when placed on the trees used for the predation experiments. These observations showed that relative crypsis observations are efficient in predicting the selective predation of the morphs. (4) The melanic frequences of D. fagella and Allophyes oxyacanthae and the estimates of selective predation at the sites were consistent with the suggestion that selective predation is a major factor in determining melanic frequency. However, the results presented in this paper and those of previous studies, indicate that in certain parts of Britain non-visual selection is of greater importance than selective predation in determining the relative frequencies of the carbonaria and insularia forms of Biston betularia.
Article
Visual signaling in animals can serve many uses, including predator deterrence and mate attraction. In many cases signals used to advertise unprofitability to predators are also used for intraspecific communication. Although aposematism and mate choice are significant forces driving the evolution of many animal phenotypes, the interplay between relevant visual signals remains little explored. Here we address this question in the aposematic passion-vine butterfly Heliconius erato by using color- and pattern-manipulated models to test the contributions of different visual features to both mate choice and warning coloration. We found that the relative effectiveness of a model at escaping predation was correlated with its effectiveness at inducing mating behavior, and in both cases wing color was more predictive of presumptive fitness benefits than wing pattern. Overall, however, a combination of the natural (local) color and pattern was most successful for both predator deterrence and mate attraction. By exploring the relative contributions of color versus pattern composition in predation and mate preference studies, we have shown how both natural and sexual selection may work in parallel to drive the evolution of specific animal color patterns.This article is protected by copyright. All rights reserved.