Both male and female identity influence variation in male signalling effort.

Abstract

Male sexual displays play an important role in sexual selection by affecting reproductive success. However, for such displays to be useful for female mate choice, courtship should vary more among than within individual males. In this regard, a potentially important source of within male variation is adjustment of male courtship effort in response to female traits. Accordingly, we set out to dissect sources of variation in male courtship effort in a fish, the desert goby (Chlamydogobius eremius). We did so by designing an experiment that allowed simultaneous estimation of within and between male variation in courtship, while also assessing the importance of the males and females as sources of courtship variation.
Although males adjusted their courtship depending on the identity of the female (a potentially important source of within-male variation), among-male differences were considerably greater. In addition, male courtship effort towards a pair of females was highly repeatable over a short time frame.
Despite the plasticity in male courtship effort, courtship displays had the potential to reliably convey information about the male to mate-searching females. Our experiment therefore underscores the importance of addressing the different sources contributing to variation in the expression of sexually-selected traits.

Full text

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Both male and female identity influence variation
in male signalling effort
Lehtonen et al.
Lehtonen et al. BMC Evolutionary Biology 2011, 11:233
http://www.biomedcentral.com/1471-2148/11/233 (9 August 2011)

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RESEARCH ARTICLE Open Access
Both male and female identity influence variation
in male signalling effort
Topi K Lehtonen1,2*, P Andreas Svensson1,3and Bob BM Wong1
Abstract
Background: Male sexual displays play an important role in sexual selection by affecting reproductive success.
However, for such displays to be useful for female mate choice, courtship should vary more among than within
individual males. In this regard, a potentially important source of within male variation is adjustment of male
courtship effort in response to female traits. Accordingly, we set out to dissect sources of variation in male
courtship effort in a fish, the desert goby (Chlamydogobius eremius). We did so by designing an experiment that
allowed simultaneous estimation of within and between male variation in courtship, while also assessing the
importance of the males and females as sources of courtship variation.
Results: Although males adjusted their courtship depending on the identity of the female (a potentially important
source of within-male variation), among-male differences were considerably greater. In addition, male courtship
effort towards a pair of females was highly repeatable over a short time frame.
Conclusion: Despite the plasticity in male courtship effort, courtship displays had the potential to reliably convey
information about the male to mate-searching females. Our experiment therefore underscores the importance of
addressing the different sources contributing to variation in the expression of sexually-selected traits.
Background
Males often rely on elaborate sexual displays to attract
females. Such displays can reveal important information
about the quality or motivation of the signaller [1,2].
Courtship displays are therefore commonly used by
females as cues when selecting a mate and, in so doing,
affect the regime of sexual selection [3,4]. Considerable
research attention has been given to understanding
among-male variation in signal expression due to its
potential in influencing male mating opportunities and
reproductive success. Less well studied - but just as
important - is the variation in signal intensity that can
occur within individuals [5,6] due to behavioural plasti-
city [e.g. [7]]. Such variation can arise, for example, in
response to life-history trade-offs between present and
future signalling effort, as in Drosophila [8] and three-
spined sticklebacks, Gasterosteus aculeatus [6,9], or
between different components of male reproductive
investment (e.g. mate attraction versus parental care), as
in collared flycatchers, Ficedula albicollis [10,11]. Males
might also be expected to adjust their courtship effort
strategically to maximise their reproductive payoffs,
especially if mating costs are high, if females vary greatly
in reproductive value, and if there is a good chance of
attracting high quality mates in the future [12]. In gen-
eral, both among- and within-individual variation in
courtship intensity can affect the evolutionary potential
of sexual selection by contributing to variance in repro-
ductive success [11].
One useful approach for investigating sexual displays
at the population level is to measure the display inten-
sity of several individuals more than once [13]. Such
data can then be used to estimate the fraction of varia-
tion in display behaviour that is due to differences
among individuals, that is, the ‘repeatability’ of the beha-
viour [14,15]. Repeatability has been widely used to
understand evolutionary processes (e.g. heritability),
with high repeatability values indicating high consistency
within, and large differences among, individuals [13-15].
Low values, by contrast, would indicate the opposite
pattern. Quite remarkably, while many studies of sexual
selection have assessed repeatability of male courtship
effort [13], very few have dissected different sources of
* Correspondence: topi.lehtonen@utu.fi
1School of Biological Sciences, Monash University, Victoria 3800, Australia
Full list of author information is available at the end of the article
Lehtonen et al. BMC Evolutionary Biology 2011, 11:233
http://www.biomedcentral.com/1471-2148/11/233
© 2011 Lehtonen et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.

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variation in male courtship and compared them directly,
despite the potential value of such comparisons [see
[16]].
The desert goby, Chlamydogobius eremius, is a fresh-
water fish endemic to the Lake Eyre drainage basin in
Central Australia. This small (≤ 8 cm), sexually-
dimorphic species (Figure 1) is locally abundant
throughout its range where it inhabits both permanent
and temporary bodies of water, from spring-fed pools to
ephemeral desert streams. Male desert gobies establish
nests under rock crevices and rely on conspicuous dis-
plays to attract passing females for mating. The court-
ship displays involve the raising of the colourful dorsal
and anal fins coupled with occasional jerky body move-
ments (Figure 1, additional file 1, [17]). Previously,
males were shown to adjust their courtship effort strate-
gically by courting larger females more intensely [17].
The aim of the current study was to simultaneously
assess potential sources of individual variation in male
courtship effort. Specifically, if male courtship is to be a
potentially useful sexual signal, we predict that, for a
given point in time, variation in signalling effort
observed among males should be greater relative to the
variation attributed to female identity, an important
source of within-male variation [17]. If, in turn, differ-
ences among males in courtship were small compared
to each male’s tendency to adjust his courtship effort, or
relative to short term within-male variability due to
other reasons, male courtship effort would be less reli-
able as a signal to females. We would also expect court-
ship effort to be repeatable (sensu Becker [14]).
Accordingly, we designed an experiment that could
compare the different sources of variation in male
courtship (male identity, female identity, and unidenti-
fied sources) directly, as well as assess the repeatability
of courtship effort (by also allowing us to partition the
total variation into within-male and among-male
sources).
Methods
Fish collection and housing
Experimental trials took place from January to May
2009. Desert gobies were collected as juveniles from
waterholes and springs west of Lake Eyre in South Aus-
tralia using dip and seine nets. During a two-day surface
transport to the laboratory, fish were kept in insulated
50-litre plastic tubs (coolers), filled with water to a
depth of 30 cm and provided with constant motorised
aeration. Back in the laboratory, fish were housed in 80
- 300 L aquaria and were separated by sex after matura-
tion. Aquaria were maintained at a temperature of 23 -
26°C, a salinity of 5 - 7‰ and on a 12 h light:dark cycle.
All fish were fed 1 - 2 times a day ad libitum on a diet
of commercially prepared pellets and frozen brine
shrimp (Artemia). After completion of the study, fish
were retained as stock for unrelated research.
Measurement of courtship effort and fish size
Male desert gobies were introduced into individual com-
partments (measuring 18 × 25 cm, with water depth of
approximately 20 cm) containing a halved clay flowerpot
as a nest (diameter = 6.5 cm, length = 6.5 cm). The
entrance of the nest was positioned to face a small (6 ×
25 cm), adjoining female compartment separated by a
clear Perspex divider (see also Figure 1B in [17]). The
bottom of both compartments was covered with a 3 cm
layer of sand.
After the male (total length ± standard error: 65 ± 1.4
mm, N = 40) was introduced into his compartment, he
was given three days to acclimate before we introduced
a stimulus female (53 ± 1.1 mm, N = 40) into the adja-
cent compartment. To standardise female reproductive
state, only ripe females were used, as determined by
their distended bellies. Data on fish behaviour was col-
lected following previously published methods [17,18].
Tanks were brightly lit from above, with the observer
seated in the dark away from the tank to prevent distur-
bance to the fish. Three minutes after the introduction
of the stimulus female, we measured the amount of
courtship directed by the male towards the female. This
was achieved by conducting spot samples every 10 sec-
onds over a 10 minute period. During each spot sample,
a male was recorded as courting the female if he was
within 5 cm of her compartment, with his body oriented
unambiguously towards her whilst engaged in courtship
behaviour (i.e. fin displays) [18]. At the end of the trial,
we tallied the total number of times the male was court-
ing the female as a measure of his signalling effort.
Male courtship effort was measured over two subse-
quent days so that two different males were each
Figure 1 Male desert goby (Chlamydogobius eremius) courting
a female.
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presented with the same pair of stimulus females. This
combination of four fish is hereafter referred to as an
experimental unit (N = 20). During the first day, both
males were tested once with each of the two stimulus
females within their experimental unit. Hence, during
the first day, each fish performed in two trials. There
was at least 45 minutes between each trial and the order
of trials was randomised. The same procedure (with a
new randomisation of the order of trials) was repeated
on the following day.
Our experimental design provides more detailed infor-
mation than the coefficient of intra-class variation (i.e.
‘repeatability’) alone and, importantly, allows testing of
multiple hypotheses within a single experimental set up.
Specifically, in order to estimate the variance compo-
nents of male courtship effort (in terms of the contribu-
tions of male identity and female identity to the total
variance in courtship intensity), we analysed the court-
ship data with linear mixed effects models, using the
‘lme4’ package in the R 2.10.1 software [19]. A model
was fitted using day (’1’ or ‘2’) as a fixed factor and
female ID and male ID as random factors (random
intercepts, common slopes). The statistical significance
of random and fixed effects was assessed by comparing
a full model with reduced models not containing the
factor of interest, using log-likelihood tests [20]. When
comparing models differing in their fixed factors, maxi-
mum likelihood was used to fit the models. In all other
cases, restricted maximum likelihood was used.
Total lengths were measured by photographing each
fish after the experiment in a container with 3 cm of
water and a piece of grid paper as a scale. We used an
Olympus C-5060 digital camera for photographs and
Image Tool 3.00 (The University of Texas Health
Science Institute, San Antonio, TX) software for the
image analysis. The size difference between the two
females within each experimental unit ranged from zero
to moderate (average length difference between the two
females: 4.9 ± 1.3 mm). Similarly, large size differences
between each of the two males were avoided (average
length difference between the two males: 5.4 ± 0.75
mm). We tested whether differences in body size, as
measured over the whole data-set, predicted patterns in
male courtship effort by regressions of courtship effort
as a function of body size, both for females and males.
One male did not engage in any courtship behaviour
and remained inactive over the whole period of the
experiment, and was therefore excluded from analyses.
Repeatability of courtship effort
In order to get an estimate for repeatability of male
courtship effort (and its standard error and 95% confi-
dence intervals), we analysed the total amount of court-
ship each male performed during days 1 and 2,
following the procedure of Becker [14]. Specifically, a
one-way ANOVA was used to partition the total var-
iance of courtship intensity into the variance among
males (S2A) and the variance within males (S2). The
ratio of the variance among males (S2A) to the total phe-
notypic variance (S2+ S2A) then gives an estimate of
repeatability, also called ‘the coefficient of intra-class
correlation’ sensu Lessells & Boag [15].
Ethical note
This study complies with all the relevant Federal and
State laws of Australia, adheres to the ASAB/ABS guide-
lines for the use of animals in research, and was con-
ducted under ethics permit ‘BSCI/2007/12’ from the
Biological Sciences Animal Ethics Committee of Monash
University.
Results
The linear mixed effects model revealed a significant
effect of ‘day’ on male courtship (with 15.9 ± 6.4% fewer
displays on the second day: model 1 vs. model 3, c2=
6.17, df = 1, P = 0.013; Figure 2; Table 1). There was
also a significant contribution of male ID (model 1 vs.
model 4, c2= 60.6, df = 1, P < 0.001; Figure 3; Table 1)
and of female ID (model 1 vs. model 2, c2= 4.45, df =
1, P = 0.035; Figure 4; Table 1) to the fit of the model.
‘Male ID’ explained 69.0% of the total variance in male
courtship, while ‘female ID’ (as a source of within-male
variation under special interest) explained 6.0% and ‘day’
explained 1.6%. The remaining 23.4% was left unex-
plained by the model (residual variance).
0
20
40
60
80
100
0 20
Time?spent?courting,?Day?1?(%)
40 6080 100
Time?spent?courting,?Day?2?(%)
Figure 2 Time spent courting by males on days 1 and 2. Each
data point (N = 39) represents the percentage of time an individual
male spent courting (as averaged for the two stimulus females, and
calculated from spot samples of male behaviour). The line indicates
identical courtship effort on the two days.
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There was no significant relationship between the size
of males and their total courtship effort as expressed
over the two days (linear regression, F1,37= 1.198, R2=
0.031, P = 0.28; Figure 3). Similarly, there was no signifi-
cant relationship between the size of females and the
amount of courtship that males directed toward them
(linear regression, F1,38= 0.680, R2= 0.018, P = 0.42;
Figure 4). Male courtship effort, averaged towards the
two females, was highly and significantly repeatable (the
associated F = 11.30, repeatability: r = 0.837, SE = 0.049,
95% confidence interval: 0.713 - 0.911, N = 39 males;
Figure 2).
Discussion
Our results show that desert goby males exhibit consid-
erable among-individual variation in courtship effort.
Moreover, over a short time frame (here one day), these
individual differences were also highly consistent. This is
important because such consistency provides a potential
for female choice (or, indeed, other forms of selection)
to work on traits that affect courtship rate [21]. In this
regard, both the level of heritable variation and the
degree of condition dependence are potentially relevant
[11]. Substantial individual variation in male courtship
effort seems to be widespread among taxa (e.g. fish:
[22]; frogs: [23]; arthropods: [24]; lizards: [25]) although
this variation is usually not as pronounced as what the
current study has shown for desert gobies (for points of
comparison, see [13]). The extensive variation among
desert goby males is unlikely to be due to differences in
body condition (see [26-29]) as all males were fed ad
libitum. Moreover, we did not find any effect of male
body size on courtship.
Within-male differences in the expression of sexual
signals can also be important. For example, previous
Table 1 The degree of model fit (AIC) in linear mixed
effects models of courtship effort in male desert gobies
Model Fixed factorsRandom factorsAIC
ΔAIC
1
2
3
4
Day
Day
Male ID, Female ID
Male ID
Male ID, Female ID
Female ID
1253
1255
1260
1311
0
2
7
58 Day
The ΔAIC is the difference in AIC values compared to the estimated best
model (at the top of the table).
0
20
40
60
80
100
5055 606570 7580 85
Male total length (mm)
Time spent courting (%)
Figure 3 Variation in male courtship effort, with males (N = 39) ordered according to their body size. The two vertically attached
symbols represent courtship effort towards the two stimulus females within a single focal male’s ‘experimental unit’. The larger of the two
females is indicated with a larger symbol and the smaller female with a smaller symbol. The two males within each unit (i.e. the two males that
courted the same pair of females) are identified by a shared combination of symbol colour and type.
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studies have found that environmental factors [23,30]
and variation in female reproductive state [25,31] can be
important sources of within-male variation in male sig-
nalling intensity. Indeed, in desert gobies, males are
known to adjust their courtship effort strategically
towards females of different reproductive value (based
on dichotomous assessment of female body size:
[17,18]). In the current study, however, controlled
laboratory conditions minimised environmental varia-
tion, while the experimental design controlled for order
effects. We also deliberately avoided large size differ-
ences between the two females seen by each male, as
well as variation in their reproductive state (all females
were ripe with eggs). Consequently, female size differ-
ences did not predict male courtship effort. We never-
theless found a significant effect of female identity on
the level of male courtship effort, indicating that the
males nonetheless perceived some difference between
the females. These between-female differences could, for
example, be related to colouration or behaviour (espe-
cially responsiveness), and provide an interesting avenue
for future research. Indeed, female identity, as a source
of within-individual variation in male courtship effort,
may be especially important because plasticity in the
expression of sexual signals can influence both signal
reliability [32] and the power of sexual selection [11].
Even though desert goby males are capable of strategi-
cally adjusting their courtship (both in this study and
according to female size in [17,18]), the current results
indicate that courtship effort of a male is consistent
when he experiences a similar situation on two adjacent
days. Indeed, the differences among males were more
pronounced than short term variation within males
(with 69% of variation in courtship intensity being
explained by male ID versus 6% explained by female
ID). The consistency in male courtship effort was also
demonstrated by a high estimate for its repeatability (r
= 0.837). Thus, even though a male desert goby can
strategically adjust its courtship effort, his displays were
highly consistent when re-encountering the same
females.
If among-male differences in courtship are more
important than variation within males, females have the
potential to reliably assess males based on courtship
intensity. Indeed, in many species, female mating deci-
sions seem to be biased towards males that exhibit high
0
20
40
60
80
100
3540 4550 5560 6570
Female total length (mm)
Time spent courting (%)
Figure 4 Variation in male courtship effort due to female identity. The two vertically attached symbols represent courtship efforts by the
two males that courted the same stimulus female. The larger of these two males is indicated with a larger symbol and the smaller male with a
smaller symbol. The two females within each experimental unit (i.e. the two females that were courted by the same two males) are identified by
a shared combination of symbol colour and type.
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rates of courtship [3,33-35], and among-male differences
in courtship effort often translate into differences in
male mating success. However, in species where female
traits affect male courtship intensity, we might expect
courtship to be less informative of male attributes (such
as body condition, parental ability or genetic quality)
than in systems where courtship displays are less flex-
ible. Furthermore, even when courtship effort plays a
role in mate choice, the relationship between courtship
intensity and female preference is not always clear-cut
[36-38]. Females, for instance, could be using a suite of
different cues in mate choice [39,40] or they may be
inconsistent in their choice of potential mating partners
[13,21]. For example, in the sand goby, a species with a
mating system very similar to that of desert gobies,
females exhibit individually varying mate preferences
[16] that are dependent on social context [41] and also
fluctuate over time [42].
Conclusion
We found that among-male differences in courtship
effort in desert gobies were more pronounced than differ-
ences due to female identity or other within-male
sources. Thus, males were consistent in their investment
in courtship displays when confronted with the same two
females on adjacent days. The consistent among-male
differences also resulted in a high repeatability estimate
for courtship effort. Females, therefore, have the potential
to reliably assess males based on intensity of their court-
ship. Our study underscores the importance of paying
attention to each of the different sources of variation in
the expression of male sexual displays, and we offer a
robust experimental design for simultaneously estimating
these parameters. Future investigations should consider
the importance of male courtship for female mate choice
relative to other sexually-selected traits that may also be
important in guiding female mating decisions.
Additional material
Additional file 1: Desert goby courtship behaviour. Video footage on
courtship displays by a male desert goby (Chlamydogobius eremius).
Acknowledgements
We thank S. Hamilton-Brown for logistical support, and anonymous referees
for helpful comments. This study was supported by funding from the
Australian Research Council, Nature Conservation South Australia, The
Academy of Finland, and the Department of Biology at the University of
Turku.
Author details
1School of Biological Sciences, Monash University, Victoria 3800, Australia.
2Section of Ecology, Department of Biology, 20014 University of Turku,
Finland.3School of Life and Environmental Sciences, Deakin University,
Geelong, Victoria 3220, Australia.
Authors’ contributions
TKL designed the study, conducted the experiment, participated in data
analyses and wrote the bulk of the manuscript. PAS conducted the image
measurements, performed most of the data analyses and participated in
writing of the manuscript. BBMW guided the project, provided ideas
throughout the study and contributed to writing of the manuscript. All
authors read and approved the final manuscript.
Received: 15 April 2011 Accepted: 9 August 2011
Published: 9 August 2011
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doi:10.1186/1471-2148-11-233
Cite this article as: Lehtonen et al.: Both male and female identity
influence variation in male signalling effort. BMC Evolutionary Biology
2011 11:233.
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Lehtonen et al. BMC Evolutionary Biology 2011, 11:233
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