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Enhanced male coloration after immune challenge increases reproductive potential

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In many animal species, females select a mate on the basis of the expression of secondary sexual traits. A prevalent theory suggests that male ornaments are reliable indicators of immunocompetence, because the cost of immune function prevents cheating. However, sexual signalling is a component of male reproductive effort, and an immune challenge may also alter his perceived future prospects and hence signalling effort. In this study, blue-footed booby males (Sula nebouxii) were inoculated with a diphtheria–tetanus vaccine during courtship to investigate the consequences of mounting an immune response on signalling effort. We found that, after this immune challenge, on average, males increased their signalling effort but lost more body mass compared with control males. Importantly, vaccination affected the partner's reproductive decisions: compared with control females, females paired with vaccinated males laid eggs earlier and increased clutch volume in pairs that laid early. Overall, our results suggest that blue-footed booby males invest more in sexual signals when future breeding opportunities are at risk, eliciting a greater reproductive investment by their partners. Increased signalling effort by infected individuals may contrast the idea of sexual ornaments as signals of infection status.
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Enhanced male coloration after immune challenge increases
reproductive potential
A.VELANDO*,R.BEAMONTE-BARRIENTOS
1
&R.TORRES
*Departamento de Ecolox
ıa e Biolox
ıa Animal, Universidade de Vigo, Vigo, Spain
Departamento de Ecolog
ıa Evolutiva, Instituto de Ecolog
ıa, Universidad Nacional Aut
onoma de M
exico, M
exico DF, M
exico
Keywords:
coloration;
female investment;
immunity;
sexual signals;
terminal investment.
Abstract
In many animal species, females select a mate on the basis of the expression
of secondary sexual traits. A prevalent theory suggests that male ornaments
are reliable indicators of immunocompetence, because the cost of immune
function prevents cheating. However, sexual signalling is a component of
male reproductive effort, and an immune challenge may also alter his per-
ceived future prospects and hence signalling effort. In this study, blue-footed
booby males (Sula nebouxii) were inoculated with a diphtheriatetanus vac-
cine during courtship to investigate the consequences of mounting an
immune response on signalling effort. We found that, after this immune
challenge, on average, males increased their signalling effort but lost more
body mass compared with control males. Importantly, vaccination affected
the partner’s reproductive decisions: compared with control females, females
paired with vaccinated males laid eggs earlier and increased clutch volume
in pairs that laid early. Overall, our results suggest that blue-footed booby
males invest more in sexual signals when future breeding opportunities are
at risk, eliciting a greater reproductive investment by their partners.
Increased signalling effort by infected individuals may contrast the idea of
sexual ornaments as signals of infection status.
Introduction
In iteroparous organisms, resources allocated into cur-
rent reproduction reduce future reproductive prospects;
therefore, individuals commonly restrict their current
effort to maximize lifetime success (Curio, 1983;
Stearns, 1992). In many species, male reproductive suc-
cess depends on the expression of sexually selected
traits (Andersson, 1994), which often are costly to pro-
duce and maintain (Kotiaho, 2001; Maynard-Smith &
Harper, 2003; Cotton et al., 2004). Thus, sexual signal-
ling is a component of reproductive effort (Getty,
2006), and the amount of resources invested into cur-
rent sexual advertisement probably results in reduced
residual reproductive value (Kokko, 1997; Hunt et al.,
2004; Getty, 2006). Hence, optimal sexual signalling
effort will depend on both future breeding opportuni-
ties and current probabilities of success (Lindstr
om
et al., 2009).
A prevalent theory of sexual selection suggests that
ornaments honestly reflect the individual’s genetic abil-
ity to resist parasites and pathogens (Hamilton & Zuk,
1982; Folstad & Karter, 1992). Parasites and pathogens
are likely to be one of the major extrinsic causes of
mortality among wild animals (Grenfell & Dobson,
1995). Infectious organisms activate immune defences
of hosts (Pastoret et al., 1998), and this activation is
energetically costly and induces oxidative stress
(reviewed in Hasselquist & Nilsson, 2012). Immune up-
regulation diverts resources from other functions such
as sexual signals (Faivre et al., 2003; Alonso-Alvarez
et al., 2004; Garamszegi et al., 2004; Peters et al., 2004;
Fitze et al., 2007; Cote et al., 2010). Costs associated
with immune activation can prevent ‘cheating’ because
only superior healthy males may be able to produce
elaborate ornaments. Furthermore, current evidence
suggests that activation of the immune system may cue
organisms about the risk of infections that threaten
Correspondence: Alberto Velando, Departamento de Ecolox
ıa e Biolox
ıa
Animal, Campus As Lagoas, Universidade de Vigo, 36310 Spain.
Tel.: +34 986812550; fax: +34 986812556; e-mail: avelando@uvigo.es
1
Present address: Centro Tlaxcala de Biolog
ıa de la Conducta,
Universidad Aut
onoma de Tlaxcala, Tlaxcala, M
exico.
ª2014 THE AUTHORS. J. EVOL. BIOL.
1
JOURNAL OF EVOLUTIONARY BIOLOGY ª2014 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
doi: 10.1111/jeb.12416
future survival and reproduction (Moret, 2003; Bon-
neaud et al., 2004; Velando et al., 2006a). According to
life history theory, individuals with declining future
reproductive prospects should increase their investment
in current reproduction (Williams, 1966; Pianka & Par-
ker, 1975; coined as ‘terminal investment’, Clutton-
Brock, 1984). Thus, paradoxically, infected individuals
might increase their signalling effort (i.e. dishonestly
signalling their infection status; Polak & Starmer, 1998;
Sadd et al., 2006; Nielsen & Holman, 2012; Copeland &
Fedorka, 2012).
Signalling effort may be strategically adjusted espe-
cially in labile sexual traits, such as song rate or colour
in integuments. In many monogamous species, these
labile traits continue to be exhibited after pair formation
(see Torres & Velando, 2003, 2010), and it has been sug-
gested that the presence of ornaments after pairing
might stimulate partner investment (Wachtmeister,
2001; Servedio et al., 2013). In species with biparental
care, there is potential conflict between male and female
parents over how much parental investment each
should provide (sexual conflict; Lessells, 1999). Dynamic
signals indicative of current reproductive effort are
expected to evolve as signalling strongly affects the
negotiation between mates over offspring care (McNa-
mara et al., 1999; Morales et al., 2009). Thus, in species
with biparental care, high investment in signalling prob-
ably increases partner contribution to current reproduc-
tion (Velando et al., 2006b), at the cost of reducing
future breeding opportunities (Candolin, 2000a).
The blue-footed booby (Sula nebouxii), a long-lived
socially monogamous seabird, is a good model species
to examine the effect of immune activation on male
signalling effort and partner’s breeding response. In this
species, parental effort is high, both parents incubate
and feed the chicks for a long period (up to 145 days;
Torres & Drummond, 1999; Guerra & Drummond,
1995), and the probability of success depends on the
partner contribution to brood care (Velando & Alonso-
Alvarez, 2003). After pairing, there is an extended
courtship period (up to 40 days; Osorio-Beristain &
Drummond, 1998), which probably serves for partner
evaluation (Torres & Velando, 2010). Males (especially)
have conspicuous and variably coloured feet that are
exhibited prominently during pair courtship (Nelson,
1978; Torres & Velando, 2010).
In this species, foot colour varies from bright blue
green to dull blue as a result of the combined effects of
collagen arrays and carotenoid pigments (Velando et al.,
2006b). Females prefer males with greener feet (Torres
& Velando, 2003, 2010), which result from high carot-
enoid deposition into foot integument (Velando et al.,
2006b; Torres & Velando, 2010). Several experimental
studies suggest that the mate signalling effort (i.e. carot-
enoid deposition) affects female courtship and copula-
tion rates and reproductive decisions (Torres &
Velando, 2003; Velando et al., 2006b; Dentressangle
et al., 2008; see Torres & Velando, 2010). As carote-
noids have antioxidant and immunomodulatory proper-
ties (Blount et al., 2003; McGraw & Ardia, 2003),
individuals should optimize pigment allocation into
integuments according to the trade-off between physio-
logical requirements and reproductive benefits.
In this study, we inoculated blue-footed males with
nonpathogenic antigens (diphtheriatetanus vaccine)
early in the courtship period to investigate the conse-
quences of mounting an immune response on signal-
ling effort (foot colour) and the partner’s reproductive
responses. The diphtheriatetanus vaccine activates the
immune system in birds without inducing the negative
effects of pathogens (Svensson et al., 1998; R
aberg et al.,
2000). In birds, the acute phase of immune activation
lasts a few days and the physiological responses proba-
bly end within 2 weeks (Svensson et al., 1998; Verhulst
et al., 2005). The acute phase of an immune response
leads to diversion of resources to combat immediate
and unavoidable physiological costs (see Hasselquist &
Nilsson, 2012). After injection, we recaptured males
during the expected duration of physiological responses
(911 days) and again later during early incubation,
likely sufficient time to allow recovery from the physio-
logical costs of mounting a defence (Verhulst et al.,
2005).
We expected that the negative effects of immune
activation on male coloration (if any) will be evident at
first recapture, when carotenoids are needed to palliate
the cost of immune up-regulation (Torres & Velando,
2007). In contrast, if immune activation is a cue to the
risk of infection and declining reproductive prospects
(Bonneaud et al., 2004; Velando et al., 2006a), immu-
nologically challenged males may increase their signal-
ling effort (Sadd et al., 2006) to motivate the partner’s
contribution to current reproduction (Torres & Velando,
2010). Thus, we also studied reproductive responses
(laying probability, laying date and clutch investment)
of females paired with vaccinated males.
Materials and methods
The study was carried out in the breeding colony of the
blue-footed booby Sula nebouxii at Isla Isabel (21°520N,
105°540W), Nayarit, Mexico, from January to March
2004. In January, 40 paired courting males were cap-
tured and randomly assigned to the experimental or
control treatments (n=20 in each treatment). Males
were captured during two consecutive nights (January
89), on average 29 days before laying (range 17
49 days). The birds were captured and manipulated at
night to reduce disturbance. Males were ringed with a
numbered metal ring and marked by painting a black
spot on the neck (with a nontoxic marker) to facilitate
resighting and future recaptures. Experimental
males were injected in the pectoral muscle with 200 lL
of diphtheriatetanus vaccine (Ditantrix vaccine,
ª2014 THE AUTHORS. J. EVOL. BIOL. doi: 10.1111/jeb.12416
JOURNAL OF EVOLUTIONARY BIOLOGY ª2014 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
2A. VELANDO ET AL.
GlaxoSmithKline, Madrid, Spain; diphtheria toxoid
8 IU and tetanus toxoid 0.8 IU mixed with aluminium
hydroxide at 3.0 mgmL
1
and 0.9% NaCl solution).
Control males were injected with an identical volume
of 0.9% NaCl solution. The diphtheriatetanus vaccine
contains two toxoid antigens novel to the birds, so the
effects are only derived from activating the host
humoral immune defence system (Svensson et al.,
1998; Ilmonen et al., 2000). Nest sites were inspected
daily until the eggs were laid. On the laying day, eggs
were marked with a pencil, and their length (L) and
width (W) were measured (accuracy 0.1 mm) to calcu-
late egg volume (V =0.51LW
2
; Hoyt, 1979). Overall, 29
females paired with focal males laid eggs (see Results).
Nine to eleven days after manipulation (hereafter
10 days), 30 males were recaptured (14 control and 16
experimental), and then during the first 2 weeks of
incubation, 24 incubating males were again recaptured
(11 control and 13 experimental). In the three capture
events (prior to manipulation, first recapture [10 days
later] and second recapture [during incubation]), birds
were weighed and their foot colour was determined by
taking three measurements on the foot web using a
spectrophotometer that analyses the reflectance spec-
trum from 360 to 740 nm wavelength at 10-nm inter-
vals (MINOLTA CM-2600d, Minolta Co. Ltd, Osaka,
Japan). From the foot-colour spectrum, we calculated
green chroma as the proportion of reflectance between
460 and 620 nm (the range of highest visual sensitivity
in blue-footed boobies; Reed, 1987; Velando et al.,
2006b). In this species, males displaying greener feet
during courtship are more attractive to females (Torres
& Velando, 2003, 2010; Velando et al., 2006b).
Prior to the manipulation, foot colour and body mass
of males did not differ between treatments (green
chroma, t
40
=0.11, P=0.91; body mass, t
40
=1.18,
P=0.25). Changes in foot colour and body mass with
respect to the initial state (i.e. difference between the
values at recaptures after vaccination and initial values)
were analysed by mixed linear models (Littell et al.,
1996). The model included individual birds as subject
factor, the vaccination treatment as between-subject
factor, and the repeated measures at different recapture
events (i.e. first and second recapture) as within-subject
factor. The interaction between treatment and recap-
ture event was included in the models but removed
when nonsignificant.
The probability to establish a clutch and laying date
(Julian day) was analysed using generalized linear
models with binomial error distribution and a logit link
function and a Poisson error and log link, respectively.
The models included vaccination treatment as factor
and green chroma during courtship (initial capture and
first recapture event) as covariates. Clutch volume
(sum of volume of all eggs), a proxy of female invest-
ment (Morales et al., 2009), was analysed using a gen-
eral linear model that included vaccination treatment
as a factor, and laying date, and male green chroma
and body mass during incubation as covariates; two-
way interactions between covariates and treatment
were also tested. Models were simplified by backward
deletion procedure starting with two-way interaction
effects. Results are presented as means standard
error, and the significance level was set at 0.05.
Results
Change in body mass and foot colour
Vaccination treatment strongly influenced body mass
loss (F
1,31
=7.85, P=0.009). Vaccinated males lost, on
average, 10% of body mass, whereas control males lost
2.5% (Fig. 1a). Body mass change did not differ
between recapture events (F
1,20
=0.17, P=0.68), and
–250
–200
–150
–100
–50
0
Change in body mass (g)
Change in green chroma
(a)
(b)
–0.035
–0.030
–0.025
–0.020
–0.015
–0.010
–0.005
0.000
First recapture
(courtship)
Second recapture
(incubation)
Fig. 1 Effects of diphtheriatetanus vaccination on males (open
bars represent control males and closed bars vaccinated males)
recaptured during courtship (911 days after vaccination, n=30
males) and during the first two weeks of incubation (1741 days
after vaccination, n=24 males) on the change in (a) body mass
and (b) green chroma. Values are expressed as the difference
between recapture and initial values.
ª2014 THE AUTHORS. J. EVOL. BIOL. doi: 10.1111/jeb.12416
JOURNAL OF EVOLUTIONARY BIOLOGY ª2014 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Signalling effort after immune challenge 3
the interaction between recapture event and treatment
was not significant (F
1,19
=0.01, P=0.95).
Foot colour changed to duller blue as the season pro-
gressed (F
1,20
=4.37, P=0.049; Fig. 1b). Vaccination
had a significant effect on mean change of foot colour
(F
1,31
=6.37, P=0.017). Thus, green chroma faded on
average 2.5% in control males, but only 0.76% in vac-
cinated males (Fig. 1b). In the last (second) recapture,
none of the vaccinated males lost more than 2.5% of
initial foot colour, yet 54% of control males lost more
than 4% of initial colour. The interaction between
recapture event and treatment was not significant (F
1,19
=1.17, P=0.29).
Reproduction and partner investment
From 40 males initially captured during the courtship
period, only 29 (73%) established a clutch. Initial green
chroma influenced the probability of laying (v
2
=4.36,
P=0.037). Greener males prior to vaccination were
more likely to establish a clutch (Fig. 2). Treatment did
not influence the probability of reproduction (v
2
=0.13,
P=0.71). In those males that established a clutch, vac-
cinated males established a clutch 4.8 3.0 days earlier
than control males (v
2
=4.56, P=0.033; Fig. 3). Green
chroma before vaccination did not influence laying date
(P>0.10 in all cases).
Clutch volume was affected by the interaction
between treatment and laying date (F
1,20
=4.37,
P=0.049). Females paired with vaccinated males laid
larger clutches than control males, but only in pairs that
laid early (Fig. 4a). Green chroma in the first recapture
had a positive effect on clutch volume (F
1,20
=5.48,
P=0.030). Thus, females paired with more colourful
males increased investment in the clutch (Fig. 4b).
Discussion
We found that, on average, vaccinated males lost more
body mass but maintained greener foot colour com-
pared with control males. Experimental males increased
their signalling effort after an immune challenge, prob-
ably because infection is a cue of declining reproductive
prospects (Bonneaud et al., 2004). Importantly, an
immune challenge on males affected the partner’s
0
0.2
0.4
0.6
0.8
1
0.5 0.51 0.52 0.53 0.54
Probability to establish a clutch
Green chroma
Fig. 2 Probability to establish a clutch according to foot green
chroma of males (n=40) captured during early courtship (initial
premanipulation capture).
25
27
29
31
33
35
37
39
41
43
Laying date (julian day)
Control Vaccinated
Fig. 3 Effect of diphtheriatetanus vaccination on laying date of
males that established a clutch (n=29).
Laying date
(a)
(b)
Early Late
0.49 0.5 0.51 0.52 0.53 0.54
Green chroma
60
80
100
120
140
50
70
90
110
130
150
170
Clutch volume (cm
3
)
Clutch volume (cm
3
)
Fig. 4 Female investment measured as clutch volume (cm
3
)
according to (a) vaccination treatment (open circles: control males;
closed bars: vaccinated males) and laying date (for illustrative
purposes, laying date was categorized in early and late according
to mean laying date); (b) green chroma of males in the first
recapture (courtship period; n=24).
ª2014 THE AUTHORS. J. EVOL. BIOL. doi: 10.1111/jeb.12416
JOURNAL OF EVOLUTIONARY BIOLOGY ª2014 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
4A. VELANDO ET AL.
reproductive decisions. Compared with control females,
females paired with vaccinated males laid eggs earlier,
and clutch volume was increased in early laying pairs.
Overall, these results suggest that by enhancing foot
coloration, vaccinated males induced a greater repro-
ductive investment from their partners. Thus, blue-
footed booby males invest more in sexual signals when
future breeding opportunities are at risk, enhancing
their current probabilities of breeding success.
In our study, courting blue-footed booby males were
immunologically challenged with diphtheria and teta-
nus toxoids. The acute phase after vaccination typically
lasts a few days and is characterized by a systemic
inflammatory response (Sorci & Faivre, 2009; Sorci,
2013). The second phase is the activation of humoral
immunity, with a peak response within 2 weeks (e.g.
Svensson et al., 1998). Immunized blue-footed booby
males lost more body mass 911 days after vaccination
(i.e. at first recapture, during the physiological
response) than saline injected males, a difference in
body mass that remained at least until the first 2-weeks
of incubation. Body mass decrease of immune-chal-
lenged males might result from energetic costs of
mounting an immune response (e.g. Ots et al., 2001).
Nevertheless, we cannot exclude the possibility that
body mass decline of vaccinated males resulted from
reduced feeding rates (e.g. Bonneaud et al., 2003;
reviewed in Hasselquist & Nilsson, 2012), or increased
mating effort.
According to theory, when male ornaments are reli-
able indicators of infection status, an immune challenge
should reduce the expression of sexual signals (Hamil-
ton & Zuk, 1982). Contrary to this prediction, in our
study, immunization did not reduce male coloration by
the time of the first recapture, when carotenoids were
expected to have been mobilized to palliate the cost of
immune activation (Torres & Velando, 2007). Instead,
we found that immunized males maintained greener
feet than control males, and this difference was more
pronounced at the second recapture, after the acute
phase of immune activation, roughly a month after
vaccination. Previous studies on birds have found that
an immune challenge resulted in the reduced expres-
sion of carotenoid-dependent bill colour (Faivre et al.,
2003; Alonso-Alvarez et al., 2004; Peters et al., 2004;
Cote et al., 2010). It is possible that context-dependent
effects and differences in the experimental procedure
(e.g. recapture time, doses, antigen used) might explain
the discrepancy between these studies and our results.
Interestingly, in all of these studies, males were main-
tained in captivity with no access to females, whereas
in our study, birds were only captured for a few min-
utes in their natural environment. Animals are
expected to maximize reproductive effort, so maintain-
ing costly carotenoid-dependent coloration may not be
the best strategy when the chances of reproduction are
low. Additionally, differences in other life history traits
such as patterns of parental care and age-dependent
variation in optimal allocation of resources to the
immune function and reproduction might explain some
of the variability among studies (e.g. Cote et al., 2010).
In a previous study, we found that blue-footed booby
middle-aged males, but not senescent males, were able
to maintain their foot colour 1 week after immune acti-
vation, during the acute phase (Torres & Velando,
2007). Overall, our results suggest that, with the excep-
tion of senescent males that are probably physiologi-
cally limited, blue-footed booby males maintain
colourful feet during several weeks after the acute
phase of an immune challenge.
Carotenoid supplementation in blue-footed boobies
increases immune function and foot colour (Velando
et al., 2006b; Beamonte-Barrientos et al., 2014), sug-
gesting that these pigments are a limiting factor for
both functions. As carotenoid-dependent integuments
continuously demand carotenoid pigments (Alonso-
Alvarez et al., 2004), our results suggest that immu-
nized males prioritized reproductive effort over other
functions. For blue-footed booby males, continuous
allocation of carotenoids to foot colour during courtship
may influence the probability of being cuckolded (Tor-
res & Velando, 2003) and female reproductive decisions
(Torres & Velando, 2010). Thus, vaccinated males prob-
ably increased their signalling effort to improve their
current reproductive success.
The increased signalling effort of vaccinated males
suggests that pathogen exposure changed their life his-
tory strategy. Activation of the immune system is an
important cue to the risk of infections that may threa-
ten survival (Bonneaud et al., 2004). When perceived
future prospects are low, for example after a pathogen
threat, organisms should increase their reproductive
effort (Williams, 1966; Clutton-Brock, 1984). Accord-
ingly, several studies have documented an increase in
reproductive effort after experimental activation of the
immune system (e.g. Bonneaud et al., 2004; Hanssen,
2006; Velando et al., 2006b; Weil et al., 2006; Bowers
et al., 2012). An increase in sexual advertisement after
an immune challenge has also been reported in three
invertebrate species (Polak & Starmer, 1998; Sadd et al.,
2006; Copeland & Fedorka, 2012; Nielsen & Holman,
2012).
This life history strategy has potentially important
implications for the evolution of sexual signals. Sexual
signalling effort depends on the trade-off between cur-
rent reproduction and future breeding opportunities
(Getty, 2006). Infected individuals, with low future
prospects, may increase their effort to improve their
current probabilities of mating (Kokko, 1997; Candolin,
2000b; Lindstr
om et al., 2009). In Drosophila nigrospira-
cula, experimentally parasitized males increased their
courtship rate but lived shorter than unparasitized con-
trol males (Polak & Starmer, 1998). In species with no
parental care, potential sexual conflict arises because
ª2014 THE AUTHORS. J. EVOL. BIOL. doi: 10.1111/jeb.12416
JOURNAL OF EVOLUTIONARY BIOLOGY ª2014 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Signalling effort after immune challenge 5
females may pay a cost when mating with more orna-
mented males that display increased investment in sex-
ual signalling after an infection (e.g. Sadd et al., 2006;
Copeland & Fedorka, 2012). In species with parental
care, female response to mate signalling effort by
infected individuals might be adaptive if signalling
effort also correlates with parental effort.
Our results indirectly show that female reproductive
decisions depended on mate’s coloration. In a previous
study, we found that males with colourful feet early in
the courtship period were paired with high-quality
females, in terms of body condition (Torres & Velando,
2003). Accordingly, in the present study, males with
greener foot colour in the first capture (prior to experi-
mental manipulation) had greater probabilities to estab-
lish a clutch, suggesting that foot colour influences
mate choice. Nevertheless, female breeding decisions do
not end at pairing. In our experiment, females paired
with vaccinated males laid earlier in the season and laid
larger clutches early in the season compared with
females paired with control males. Both of these life
history traits, laying date and egg investment have a
strong impact on fitness in the blue-footed booby
(Drummond et al., 2003; D’Alba & Torres, 2007; Torres
et al., 2011). Furthermore, our present results confirm
previous experimental studies. During the egg laying
period in three different years, when male coloration
was modified to a duller blue, females consistently
responded by reducing second-egg volume (Velando
et al., 2006b; Dentressangle et al., 2008; Torres & Velando,
2010). Hence, increased signalling effort of vaccinated
males probably led to an increase in reproductive invest-
ment by females.
In many species, females use male ornaments to
adjust their current investment (Horv
athov
aet al.,
2012). As it is thought that male sexual signals indicate
male genetic quality, this flexible strategy has been
traditionally explained as an adaptive adjustment to the
expected returns on investment (i.e. differential alloca-
tion hypothesis; Burley, 1988; Sheldon, 2000). Further-
more, in species with biparental care, negotiation
models suggest that females may adaptively adjust their
current investment depending on their partner’s contri-
bution (Lessells & McNamara, 2012). Additionally,
displays after pair-bond formation might evolve essen-
tially to stimulate partner’s investment in offspring,
often leading to cooperation (Servedio et al., 2013). In
the blue-footed booby, previous studies suggest that
females adjust their reproductive investment according
to parental ability of their mates (Velando & Alonso-
Alvarez, 2003; Torres & Velando, 2010). Importantly,
offspring condition strongly correlates with father’s foot
colour during chick rearing (Velando et al., 2005), sug-
gesting that foot colour may be indicative of parental
effort. Overall, this experimental study, together with
previous results (Torres & Velando, 2010), reveals the
existence of a mechanism mediated by sexual signals to
fine-tune communication between mates over parental
care (see also Morales et al., 2012); whether this
exchange of information results from sexual conflict or
stimulation remains to be studied.
In conclusion, this study found that immune-chal-
lenged males increased their signalling effort, thus
enhancing female investment in current reproduction.
The existence of enhanced sexual advertisement by
infected males challenges the generality of the long-
lasting idea of sexual ornaments as signals of parasite
resistance (Hamilton & Zuk, 1982; Folstad & Karter,
1992). Sexual signals and female responses are compo-
nents of reproductive investment of individuals subject
to complex life history tradeoffs (Kokko, 1997; Getty,
2006; Lindstr
om et al., 2009). Manipulation, coopera-
tion or negotiation scenarios should be explored by
future studies to disentangle the persistence of
enhanced signalling exhibited by immunologically chal-
lenged individuals.
Acknowledgments
Logistic support was provided by the staff from the Par-
que Nacional Isla Isabel and the fisherman from San
Blas and Camichin. We are grateful to Christoph Haag,
Andreanna Welch and two anonymous reviewers for
comments on the manuscript. The study was supported
by UNAM (IN230603, IN211406), CONACYT (47599)
and the Spanish Ministerio de Ciencia e Innovaci
on
(CGL2006-10 357-C02-01 and CGL2012-40229-C02-
02). The authors declare that they have no conflicting
interests.
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... 61 The highest investment in reproduction under unfavorable conditions, as we have observed in the Pb exposed females, has been explained by mechanisms defined as "terminal investment" 63 or reproductive compensation. 62,64 In the case of the terminal investment, Velando et al. 63 observed that immunologically challenged bluefooted booby males (Sula nebouxii) increased their signaling effort but lost body mass, which affected the partner's reproductive decisions (e.g., earlier laying and increased clutch volume). These authors 63 suggest that males invest more in sexual signals when future breeding opportunities are at risk, eliciting a greater reproductive investment by their partners. ...
... 62,64 In the case of the terminal investment, Velando et al. 63 observed that immunologically challenged bluefooted booby males (Sula nebouxii) increased their signaling effort but lost body mass, which affected the partner's reproductive decisions (e.g., earlier laying and increased clutch volume). These authors 63 suggest that males invest more in sexual signals when future breeding opportunities are at risk, eliciting a greater reproductive investment by their partners. Similarly, the hypothesis of reproductive compensation predicts that reproduction under constrains results in an increased parental reproductive effort and investment in offspring (e.g., enhanced female fecundity, greater egg size and increased male sperm number per ejaculate) to ensure its viability, but individuals that compensate have lower survival probabilities. ...
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... Our results showed that less ornamented and more parasitized grassquit males (i.e., low residual reproductive value) were able to perform sexual displays that are as intense as those performed by fully ornamented and healthier males in high predation risk contexts. Therefore, our data agree with one of the key predictions of the terminal investment hypothesis (Williams 1966;Trivers 1972;Pianka and Parker 1975): individuals with low residual reproductive value (i.e., reduced expectations of future reproduction) should increase their current reproductive effort when facing a high perceived risk of extrinsic mortality (Velando et al. 2006(Velando et al. , 2014Copeland and Fedorka 2012;Nielsen and Holman 2012). ...
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... Although the proximate mechanisms linking health to ornamentation are increasingly well explored, evidence that infection in natural populations is revealed by sexually selected traits continues to be mixed (Møller et al. 1999;Griffith and Pryke 2006). While parasitized males produce relatively dull or less elaborate ornaments in some species (Hill and Farmer 2005;Lumpkin et al. 2014;Balenger et al. 2015), in others, ornamentation and display behaviors appear to be unrelated to a male's infection status (Dufva and Allander 1995) or even positively related to parasite burden (Trigo and Mota 2016) or current/prior immune activation (Velando et al. 2014). ...
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... Environmental toxins can disrupt carotenoid bare-part coloration within 1 mo (Bortolotti et al. 2003, Pérez et al. 2010a, 2010b, and challenges to both the innate and acquired immune system typically result in duller carotenoid bare parts within days or weeks (Faivre et al. 2003a, Alonso-Alvarez et al. 2004, Peters et al. 2004a, Gautier et al. 2008, Rosenthal et al. 2012; but see Velando et al. 2014). Carotenoid bare parts may respond rapidly (within 6.5 hr) to stressors, including capture and captivity (Rosen and Tarvin 2006, Biard et al. 2009, Sternalski et al. 2010, Rosenthal et al. 2012, Vergara et al. 2015, and their color reflects indices of recent stress such as corticosterone levels or the heterophil:lymphocyte ratio (Roberts et al. 2007, Pérez-Rodríguez and Viñuela 2008, López et al. 2011, Kelly et al. 2012. ...
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Avian plumage has captivated scientists and the public alike for generations and has been a fundamental study system for research into signal evolution. By contrast, relatively little attention has been paid to avian bare parts such as exposed skin, bills, feet, and combs, despite considerable variation in structure and coloration within and between species. To better understand the potential signaling role of bare parts, we conducted a comprehensive literature search that returned 321 published studies. In reviewing these studies, we found that (1) bare-part color is widely distributed taxonomically and is produced by diverse mechanisms; (2) many bare parts are likely to be dynamic, honest signals of current condition or status and can also reflect genetic makeup and early developmental conditions; and (3) bare parts can function as pluripotent social signals, mediating interactions between competitors, mates, and kin. Differences between bare parts and plumage in phenology and information content support a multiple-messages interpretation of their respective signaling roles, in that bare parts may contain information that is complementary to, but distinctive from, information conveyed by plumage-based signals. We consider it likely that a great deal of barepart variation is ‘‘hidden in plain sight,’’ in that meaningful variation may not be recorded by many current studies. We urge more careful and extensive characterization of bare-part coloration in a wider range of species because of its potential to advance our understanding of signal function and constraints, with particular reference to the role of dynamic color signals and the evolution of multiple ornamentation.
... Parasites drain resources (including pigments and nutrients) from their hosts, which might otherwise be partly allocated to producing ornaments. Furthermore, in fighting parasites, hosts also mount immune responses that divert resources from other functions such as ornamentation (Rosenthal et al. 2012;Velando et al. 2014). Regardless of the underlying mechanism, parasitism should Figure 5 Changes in yellow-orange beak chroma (YO chroma ) in 20 male king penguins (Aptenodytes patagonicus) that endured a prolonged fast in captivity. ...
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