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Evolutionary biology
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Opposite differential allocation by males
and females of the same species
Tobias Limbourg, A. Christa Mateman and C. M. Lessells
Netherlands Institute of Ecology (NIOO-KNAW), PO Box 50, 6700 AB Wageningen, The Netherlands
Research
Cite this article: Limbourg T, Mateman AC,
Lessells CM. 2013 Opposite differential
allocation by males and females of the same
species. Biol Lett 9: 20120835.
http://dx.doi.org/10.1098/rsbl.2012.0835
Received: 4 September 2012
Accepted: 5 November 2012
Subject Areas:
behaviour, evolution
Keywords:
differential allocation, reproductive
compensation, parental effort, UV coloration,
blue tits, mate attractiveness
Author for correspondence:
C. M. Lessells
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2012.0835 or
via http://rsbl.royalsocietypublishing.org.
Differential allocation (DA)—the adjustment of an individual’s parental
investment in relation to its mate’s attractiveness—is increasingly recognized
as an important component of sexual selection. However, although DA is
expected by both sexes of parents in species with biparental care, DA by
males has rarely been investigated. We have previously demonstrated a
decrease in the feeding rates of female blue tits Cyanistes caeruleus when
their mate’s UV coloration was experimentally reduced (i.e. positive DA). In
this study, we used the same experimental protocol in the same population
to investigate DA by male blue tits in relation to their female’s UV coloration.
Males mated to UV-reduced females had higher feeding rates than those mated
to control females (i.e. negative DA). Thus, male and female blue tits display
opposite DA for the same component of parental effort (chick provisioning),
the first time that this has been reported for any species.
1. Introduction
Differential allocation (DA) is the adjustment of an individual’s parental investment in relation to the attractiveness of its mate [1–4]. Such differential
investment is expected when a mate’s sexual attractiveness is a signal of the offspring’s expected reproductive value. For example, sexually attractive males
may have ‘good genes’ which they pass on to their offspring [2,4]. In its broadest current use, DA encompasses responses by males, as well as females, to their
mate’s attractiveness [4], and may involve either increasing (‘positive DA’) or
decreasing (‘negative DA’, ‘reproductive compensation’) parental effort with
increasing mate attractiveness [3,4]. However, previous studies have focused
on DA by females, for whom there is ample experimental evidence for positive
DA in birds [5] and other taxa [2–4], and several examples of negative DA,
mostly involving maternal allocation into avian eggs [4]. In contrast, studies
of DA by males have rarely been carried out [6,7]. The role that female attractiveness plays in male parental investment decisions in species with biparental
care is therefore unclear.
We have studied DA in blue tits (Cyanistes caeruleus), a species with extensive biparental care in the form of parental feeding visits, and UV plumage
coloration that is an indicator of sexual attractiveness ([8,9], but see [10]),
male [11,12] and female [13] survival, and genetic quality ([11,14], but
see [15]). We have previously demonstrated DA by females: when male UV
chroma was experimentally reduced, females decreased their feeding rates
and growth of the young was reduced [16]. Thus not only was there positive
DA by female blue tits, but also an immediate effect on offspring condition.
This is consistent with a positive correlation between female feeding rates
and male UV chroma in the same population [17]. Intriguingly, our descriptive
study revealed a negative correlation between male feeding rates and female UV
chroma, raising the possibility of DA of opposite sign in males and females. The
aim of this study is to test whether there is indeed a negative causal relationship
between male feeding rates and female UV chroma in blue tits by experimentally reducing female UV chroma, and hence determine whether DA occurs
in opposite directions in males and females of the same species.
& 2012 The Author(s) Published by the Royal Society. All rights reserved.
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(b)
2
50
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mean feeds per 2 h (±s.e.)
(a)
40
30
females
males
females
Figure 1. Feeding rates (feeds per 2 h) by male and female blue tits in pairs in which either (a) foster-mothers (this study), or (b) foster-fathers (adapted from
[16]) were allocated to UV-reduced (filled circles) or control (open circles) treatments. The points shown are back-transformed estimates (mean + s.e.) from the
statistical models (see the electronic supplementary material, table S1 for figure 1a).
3. Results
Males with UV-reduced females had higher feeding rates
than males with control females, as shown by the significant
UV-treatment effect on male feeding rates (see figure 1a and
electronic supplementary material, table S1a), while there
was no difference in female feeding rates between groups
(see figure 1a and electronic supplementary material, table
S1b). We found a similar pattern in our previous experiment
[16] manipulating male UV chroma: individuals of the
manipulated sex did not change their feeding rates, but their
mates did. However, females decreased their feeding rate
when mated to UV-reduced males (treatment effect on
female feeding rate ¼ 20.255 + 0.084; unpublished estimate
from the analysis in [16]), whereas in the current experiment
11.2
16.8
11.0
16.6
10.8
10.6
16.4
10.4
mass (g) (± s.e.)
To test for a causal relationship between male feeding rates
(number of feeding visits per 2 h) and female UV coloration we conducted an experiment in May and June 2003 in the Hoge Veluwe
National Park, The Netherlands, using the same protocol as our
previous experiment [16] but manipulating females instead of
males. Females’ crown feathers were manipulated on days –2
and 7 (where day 0 is the hatching date of a brood), and the feeding
behaviour of the adults video-recorded on days 10 and 14.
To minimize maternal effects mediated by egg composition,
we cross-fostered whole clutches with similar clutch size and
expected hatching date on day – 3. We caught females on day
– 2 (and day 7 when the treatment was reapplied) and allocated
them at random to treatment with a mixture of either
UV-blocking chemicals and duck preen gland fat (UV-reduced
group) or only duck preen gland fat (control group) [18]. This
resulted in significantly lower UV-chroma (R3202400/R3202700,
the proportion of reflectance in the UV part of blue tits’ visible
spectrum (wavelengths of 320 – 700 nm)) in UV-reduced females
(mean UV chroma immediately after treatment: UV-reduced
females: 0.194 + 0.008 (s.e.); control females: 0.258 + 0.002
(s.e.); change in UV chroma in UV-reduced females: ANOVA,
F1,32 ¼ 51.02, p , 0.0001). On days 10 and 14, we videotaped parental feeding behaviour for 3 h, and scored the number of
feeding visits by each parent in the last 2 h of the recording
(feeds per 2 h). To assess the effect of treatment on offspring
growth, chicks were sexed using DNA analysis [19] of blood
samples taken on day 3, and offspring tarsus length and mass
measured on day 15.
Statistical methods are described in the electronic
supplementary material.
tarsus length (mm) (± s.e.)
2. Material and methods
16.2
10.2
tarsus
mass
Figure 2. Mean fledgling tarsus length and mass of broods in which fostermothers were allocated to UV-reduced (filled circles) or control (open circles)
treatments. The points shown are estimates (mean + s.e.) from the repeated
measure analysis (see the electronic supplementary material, table S2).
males increased their feeding rates when mated to UV-reduced
females (treatment effect on female feeding rate ¼ 0.153 +
0.056; t for difference in estimates ¼ 4.041, p ¼ 0.0002).
In addition to the overall effect of the manipulation on
male feeding rates, there was also an interaction with hatching date (see the electronic supplementary material, table
S1a and figure S1): males in control pairs decreased, and in
female UV-reduced pairs increased, their feeding rates as
hatching date became later in the season.
Chicks of UV-reduced foster-mothers had marginally
non-significantly longer tarsi (see figure 2 and electronic supplementary material, table S2a), but were not significantly
heavier (see figure 2 and electronic supplementary material,
table S2b).
4. Discussion
Males increased their feeding rates when mated to UVreduced females. Females were manipulated after pair formation and clutch completion, and UV-reduced females did
not alter their own feeding rates, so we can unequivocally
interpret the males’ response as negative DA [2,16]. In
addition, there was also an interaction of treatment with
hatching date, such that males mated to control females
decreased their feeding rate in relation to hatching date,
while those mated to UV-reduced females did the opposite.
Biol Lett 9: 20120835
males
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This work was supported by a grant from NWO-ALW.
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‘good investment opportunity’ equates to high-expected fitness, but it is actually the marginal rate of gain in fitness in
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find opposite DA in the two sexes.
Negative DA by males raises the question why females do
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coloration might be genetically correlated between the sexes,
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mate choice), or high UV coloration might be costly in males,
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opposite DA in males and females of the same species.
Although we are unable to identify the adaptive explanation,
our results raise intriguing questions and emphasize the need
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and females in species with biparental care, and theoretical
work identifying the kinds of factors that could explain the
pattern of DA that we have found.
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One possible explanation is that early breeding males sought
additional reproductive opportunities rather than increasing
their parental effort when faced with a sudden change
in their mate’s appearance. Alternatively, the effect of the
UV-treatment may have been dependent on the weather:
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