Behaviour (2016) DOI:10.1163/1568539X-00003350

brill.com/beh

Female mountain bluebirds (Sialia currucoides) paired
to more colourful males produce male-biased broods
Erica S. Bonderud, Nancy J. Flood, Jonathan D. Van Hamme,
Cameron A. W. Boyda and Matthew W. Reudink ∗
Department of Biological Sciences, Thompson Rivers University, Kamloops, BC, Canada
* Corresponding author’s e-mail address: mreudink@tru.ca
Accepted 6 February 2016; published online ???

Abstract
Sex allocation theory predicts that females should bias the sex ratio of their offspring in response
to differences in the reproductive value of sons versus daughters. Consistent with this prediction,
females of many species appear to bias offspring sex ratios in response to mate attractiveness
and condition. Male mountain bluebirds (Sialia currucoides) display full body UV-blue structural
plumage colouration, which is associated with attractiveness, condition, and reproductive success.
Over four breeding seasons, we found females paired with more colourful males produced increasingly male-biased broods and provisioned offspring at a higher rate. Surprisingly, however, we
also found females with duller plumage and those mated to first-year males produced more malebiased broods. These results provide support for sex allocation in mountain bluebirds and suggest
female reproductive decisions may be influenced by the attractiveness of her mate. However, this
system is clearly complex and more work is needed to understand the roles of male age and female
colouration in the signalling systems of mountain bluebirds.

Keywords
mountain bluebird, Sialia currucoides, sex ratio, sex allocation, plumage, structural colouration.

1. Introduction
When the reproductive value of sons and daughters differs, sex allocation
theory predicts that females should invest more heavily in the higher-value
gender and bias offspring sex ratios to incur fitness benefits (Trivers &
Willard, 1973). Which gender is of higher reproductive value to a female
depends on both intrinsic factors (e.g., her own condition) and extrinsic factors (e.g., mate quality and resource availability) (Trivers & Willard, 1973;
© Koninklijke Brill NV, Leiden, 2016

DOI 10.1163/1568539X-00003350

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Behaviour (2016) DOI:10.1163/1568539X-00003350

Burley, 1981). When males have high variance in reproductive success, females capable of producing high-quality offspring may benefit from producing more sons than daughters, while a female only capable of producing
low-quality offspring may benefit from producing more daughters than sons
(Trivers & Willard, 1973). In nature, biased sex allocation in response to
parental condition and habitat quality has been documented in many vertebrates, including mammals (Robert & Schwanz, 2011) and numerous bird
species (Alonso-Alvarez, 2006).
In taxa with genetic sex determination, such as birds, brood sex ratios
may be adjusted pre-laying, in the form of biased ovulation or fertilization,
or post-laying, in the form of biased offspring mortality (Pike & Petrie, 2003;
Alonso-Alvarez, 2006). During meiosis, sex chromosomes segregate in a
Mendelian fashion, which should result in an equal probability of producing
a son or a daughter (Pike & Petrie, 2003; Alonso-Alvarez, 2006; Bachtrog
et al., 2014). Consequently, it would seem unlikely that sex ratios could be
biased pre-laying, yet biased offspring sex ratios have been noted in many
bird species at laying (Alonso-Alvarez, 2006).
Birds exhibit ZW sex determination, in which males are the homogametic sex and the sex chromosome inherited from the mother determines
offspring sex. Previous studies of avian sex allocation have found that female birds appear to modify brood sex ratios in response to factors such as
individual condition or quality, mate condition or quality, and habitat quality (Alonso-Alvarez, 2006). Though the physiological mechanisms allowing
females to control sex-specific egg development are poorly understood (reviewed in Pike & Petrie, 2003; Alonso-Alvarez, 2006; Navara, 2013), the
environmental factors associated with biased sex ratios are being unravelled
on a species-specific basis.
Much research into variation in brood sex ratio among birds has focused
on the role of male attractiveness. In species with female mate choice, male
attractiveness is often associated with sexually-selected plumage characteristics, with attractive males being those that display more exaggerated forms
of plumage (Burley, 1986). Male plumage can signal the direct (e.g., parental
care, resource holding potential) and/or indirect (e.g., good genes) benefits a
female will gain by mating with a particular male (Griffith & Pryke, 2006).
Thus, a female paired to an attractive male may benefit from producing a
male-biased brood if sons inherit the features of the male parent. Because females experience relatively low variation in reproductive success, a daughter

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3

would be less affected by the inheritance of lower-quality genes than a son,
suggesting a female-biased brood would be adaptive when a female is paired
to a less attractive male. Male plumage ornamentation has been positively
correlated with male-biased broods in several species, including collared flycatchers (Ficedula albicollis; Ellegren et al., 1996), red-breasted flycatchers
(Ficedula parva; Mitrus et al., 2015), common yellowthroats (Geothlypis
trichas; Taff et al., 2011), blue tits (Cyanistes caeruleus; Sheldon et al., 1999;
Griffith et al., 2003; Delhey et al., 2007), and barn swallows (Hirundo rustica; Romano et al., 2015).
Although many studies have found evidence supporting the idea that birds
are able to adaptively manipulate brood sex ratios, others have failed to find
such evidence (Koenig & Dickinson, 1996; Saino et al., 1999; Ewen et al.,
2004; Rosivall et al., 2004; Korsten et al., 2006; Czyź et al., 2012). The
current literature is contradictory: one study will find a relationship in a
certain species, while another study on the same species, but on a different
population or during a different year will not (e.g., blue tit: Griffith et al.,
2003; Korsten et al., 2006; collared flycatcher: Ellegren et al., 1996; Rosivall
et al., 2004; barn swallow: Saino et al., 1999; Romano et al., 2015). These
conflicting results highlight the need for replication across populations and
over time.
Brood sex ratios have been studied in both western (Sialia mexicana;
Dickinson, 2004) and eastern bluebirds (Sialia sialis; Lombardo, 1982). No
evidence for adaptive brood sex ratio adjustment was observed in eastern
bluebirds (Lombardo, 1982); in western bluebirds, biased brood sex ratios
were related to the presence of helpers-at-the-nest (Dickinson, 2004). Although closely related, mountain bluebirds (Sialia currucoides) do not breed
cooperatively, suggesting brood sex ratios may be affected by different factors. Mountain bluebirds are sexually dimorphic and male UV-blue plumage
colouration is associated with body size and reproductive success (Balenger
et al., 2009a), suggesting that it may be adaptive for females to bias brood
sex ratios in response to male plumage colouration.
We studied a population of mountain bluebirds breeding in interior British
Columbia, Canada over four breeding seasons to ask whether female mountain bluebirds produce sex-biased broods in response to mate attractiveness.
In accordance with sex allocation theory (Trivers & Willard, 1973; Burley,
1981), we predicted that females paired with more colourful males will produce male-biased broods. In addition, we asked whether males or females

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Behaviour (2016) DOI:10.1163/1568539X-00003350

adjust parental investment (provisioning rate) in response to their offspring
sex ratio, and whether parental investment is associated with male plumage
colouration.
2. Materials and methods
2.1. Study species
Mountain bluebirds are medium-sized, secondary cavity nesting songbirds
that readily make use of nest boxes in open grasslands, often along fence
posts. Mountain bluebirds display UV-blue plumage and are sexually dimorphic (Power & Lombardo, 1996). Breeding males possess full-body UV-blue
plumage, while breeding females have a generally more subdued browngrey plumage, with UV-blue on their rump, tail, and flight feathers that is
duller than that of males (Power & Lombardo, 1996). Unlike carotenoid and
melanin based plumage, which depend primarily upon pigment deposition,
variation in UV-blue plumage is dependent upon melanin arrangement and
feather microstructure (Prum, 2006). An individual’s nutritional state during
moult can affect the resulting feather structure and colour (Keyser & Hill,
1999; Siefferman & Hill, 2005, 2007; Doyle & Siefferman, 2014). Consequently, structurally based plumage appears to be an honest signal of an
individual’s condition and quality, as is true for colours based on dietary
pigments (Keyser & Hill, 2000; Siefferman & Hill, 2003).
In a population of mountain bluebirds from Wyoming, USA, male
plumage colouration was positively correlated with male wing size and total
reproductive success (i.e., the sum of within-pair and extra-pair offspring),
suggesting that brightly coloured males are in better condition and of higher
quality than dull males (Balenger et al., 2009a). Mountain bluebirds are socially monogamous and show weak negative assortative mating in regard to
plumage colour (Morrison et al., 2014). Extra-pair paternity rates are high in
this species (72% of broods; Balenger et al., 2009b), and males that sire
extra-pair young have brighter UV-blue plumage than males that do not
(Balenger et al., 2009a; O’Brien & Dawson, 2011), suggesting the opportunity for sexual selection to act on male UV-blue plumage (Balenger et al.,
2009b).
2.2. Field methods
Field work for this project was conducted during the 2011–2014 breeding
seasons (May–July) in Kamloops, British Columbia, Canada (885–1116 m

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5

asl; 50°37′ N, 120°19′ W), using nest box routes established and maintained
by the Kamloops Naturalist Club. Nest boxes were monitored every one to
three days to determine first egg date, clutch size, hatch date, number of
nestlings and fledging success. Five to ten days after eggs hatched, adult
males and females were captured at the nest using nest box traps. Adults were
banded with a single Canadian Wildlife Service (CWS) aluminium band and
a unique combination of three plastic colour bands. We classified adults as
either second-year (SY) or after-second-year (ASY) by examining the moult
limits of the primary and greater coverts, as described by Pyle (1997). To
evaluate individual body size and condition, we measured mass, unflattened
wing chord, tail length and tarsus length. For colour analysis, we collected
ten rump feathers and a single tail feather from each adult. Nestlings were
banded with a single CWS aluminium band 9 to 13 days after hatching. At
the time of banding, we collected blood samples from adults and nestlings by
piercing the ulnar vein and drawing 15–25 µl of blood into a micro-capillary
tube.
All work was approved by the Thompson Rivers University Animal Care
and Use Committee and was conducted under a Canadian Federal Master
Banding Permit and Scientific Collection Permit.
2.3. Parental care
To examine patterns of parental care, we conducted video recordings of
morning provisioning trips for two-hour periods during the early (3–5 days
after hatching) and late (14–16 days after hatching) nestling phases, for a
total of four hours per nest. Nest watch videos were recorded using a Handycam DCR-SX45 (Sony, Tokyo, Japan) or a HD Hero2 or 3 (GoPro, San
Mateo, CA, USA). Nest watches started between 06:20 and 12:45 (mean ±
SD = 09:17 ± 85 min). Video cameras were placed on the ground approximately two meters in front of the nest box and aimed at the box entrance.
A trained observer analysed nest watch videos to determine rates of provisioning by the male and female (separately). Provisioning rates were measured as the number of trips to the nest per hour per nestling, following
Morrison et al. (2014). Female visits to the nest during the early nestling
phase that lasted longer than 30 s were recorded as brooding. Adults were
not captured at nests within 48 h prior to nest watches to avoid modification
of parental behaviour.

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Behaviour (2016) DOI:10.1163/1568539X-00003350

2.4. Feather colour analysis
We mounted rump and tail feathers on low-reflectance black paper. Rump
feathers were mounted in an overlapping pattern that mimicked the way
feathers would normally lie on the bird. We quantified male and female
plumage colouration by measuring reflectance across the avian visual spectrum (300–700 nm) using an Ocean Optics JAZ spectrometer (Dunedin, FL)
with a PX-2 xenon light source. The fibre optic probe was held in a nonreflective probe holder to measure feathers from a standard 90° angle and
5.9 mm distance. We took ten readings for each plumage area (tail and rump)
from haphazard locations within the blue regions.
Using the R-based colour analysis program RCLR v.28 (Montgomerie,
2008), we calculated three colour variables for each feather reading (brightness, hue and chroma) and then, for each of these variables, averaged the
values obtained over the ten readings from each feather sample. Brightness
was measured as the average percent reflectance across the avian visual spectrum (300–700 nm). Chroma was measured as the proportion of reflectance
within the blue range (400–510 nm) and ultraviolet range (300–400 nm) relative to the total light reflected across the avian visual range. Finally, hue was
measured as the wavelength at maximum reflectance. Due to high colinearity among these three colour variables, we used principal component analysis
to collapse the three variables into a single factor. Because the first principal component (PC1) explained most of the variance for each plumage area,
we used PC1 to represent overall plumage colouration variation (Table 1).
A greater PC1 value corresponded to increases in brightness and chroma,
but a decrease in hue (i.e., maximum reflectance shifted more towards the
UV end of the spectrum).
2.5. Molecular methods
We stored blood taken from adults and nestlings at 4°C in ethanol (2011–
2014) or dried on filter paper (2014 only). Total genomic DNA was extracted
using the standard protocol for the E.Z.N.A Blood DNA Mini Kit (Omega
Bio-Tek, Norcross, GA, USA) and stored at −20°C.
We determined nestling sex by using polymerase chain reaction (PCR) to
amplify two homologous avian sex chromosome genes. P8 (5′ -CTCCCAAG
GATGAGRAAYTG-3′ ) reverse and P2 (5′ -TCTGCATCGCTAAATCCTTT3′ ) forward primers were used to amplify the chromo-helicase-DNA-binding

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Table 1.
Results from a principal components analysis of measures of rump and tail plumage colouration (brightness, hue and chroma).
Eigenvalue

Proportion
of variance

Colour variable

Factor
loading

Male tail PC1

1.84

0.61

Brightness
UV + blue chroma
Hue

1.68

0.56

Brightness
UV + blue chroma
Hue

0.64
0.51
−0.57

Female tail PC1

Male rump PC1

2.07

0.69

Brightness
UV + blue chroma
Hue

Female rump PC1

2.17

0.72

Brightness
UV + blue chroma
Hue

0.54
0.54
−0.65
0.49
0.64
−0.60
0.45
0.64
−0.63

Because the first principal component (PC1) was found to explain most of the variation,
PC1 was used to represent overall plumage colour variation.

(CHD) genes of the Z (CHD-Z) and W (CHD-W) sex chromosomes (Griffiths et al., 1998). Due to the inclusion of an intron, the P8 and P2 primers
amplify regions approximately 300 and 375 bp in size from the CHD-Z and
CHD-W genes, respectively, allowing for amplicon separation and sex determination (Griffiths et al., 1998). Following separation, we identified males
by the presence of a single 300-bp band and identified females by the presence of both a 300-bp band and a 375-bp band.
PCR amplification was carried out in a total volume of 25 µl, the final reaction conditions being: 10.35 µl H2 O; 3.0 µl (3.0 mM) MgCl2 ; 5.0 µl (1×)
buffer; 0.5 µl (0.2 mM) nucleotide mix; 0.15 µl (0.75 U) Taq polymerase;
2.5 µl (1 µM) each P2 and P8 primers; 1 µl genomic DNA (mean ± SD =
233 ± 193 ng/µl). All reagents were supplied in the GoTaq PCR Core System II (Promega, Madison, WI, USA). An initial denaturing step at 94°C for
5 min was followed by 30 cycles of 94°C for 30 s, 51°C for 45 s, and 72°C
for 45 s. A final run of 48°C for 1 min and 72°C for 5 min completed the program. PCR products were separated by gel electrophoresis for 90–120 min
at 90 V in a 2.5% agarose gel (10 × 7 cm) stained with GelRed Nucleic
Acid Stain (Biotium, Hayward, CA, USA). When tested using DNA from

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Behaviour (2016) DOI:10.1163/1568539X-00003350

adult birds of known sex (N = 32; 21 females and 11 males), we found the
protocol to have 100% accuracy (32/32 birds correctly sexed).
2.6. Statistical analysis
Because we were interested in female control of brood sex ratio, rather than
differential offspring mortality, we restricted our analyses to broods containing four or more offspring. A minimum brood size of four offspring was
chosen due to increased bias in broods containing fewer nestlings. Of our total sample of 89 broods, 75 broods (84.3%) contained four or more nestlings.
We further restricted our analyses to broods from which both the male and
female attending the nest had been caught and identified (68 broods, 79%).
Here, we refer to population sex ratio as the overall proportion of male and
female nestlings in the population; brood sex ratio is based on the proportion
of male and female nestlings within a brood. Mean brood sex ratio for each
breeding season was calculated as the sex ratio averaged over all broods for
that year.
Statistical analyses were performed using JMP 12 statistical analysis software (SAS Institute, 2015). Because the data did not meet the assumptions
of normality, we used Wilcoxon signed-rank tests to determine if population
sex ratio and brood sex ratios deviated from unity. A Kruskal–Wallis test
was used to determine if brood sex ratios differed among years. To examine whether plumage colouration was associated with parental provisioning
rates, we constructed linear mixed models with provisioning rate (early male,
early female, late male, late female) as the response variable, rump PC1, tail
PC1, and age as main effects, with corresponding interaction terms, and individual identity (band number) as a random effect. To examine whether
plumage colouration predicted brood sex ratios, we constructed generalized
linear mixed models with binomial error distribution and a logit link function, using nestling sex (M/F) as the response variable, tail colour, rump
colour, and age as main effects and a random effect of nest ID nested within
female band number. Models were run for males and females separately and
we also included interaction terms, which were subsequently removed if nonsignificant. To ask whether parents adjusted provisioning rates in response to
offspring sex ratio, we constructed linear mixed models with provisioning
rate as the response variable, brood sex ratio as the main effect, and individual identity as a random effect. We also included an effect of nest watch time
and interaction terms, which were subsequently removed if non-significant.

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3. Results
3.1. Population and brood sex ratios
We determined the sex of 334 nestlings from 68 broods from the 2011–2014
breeding seasons (Table 2). We could not assign gender to nine nestlings
from eight broods because no DNA was available or because we failed to
obtain PCR products from those individuals. Broods included in the analysis
ranged in size from three to six nestlings (range, mean ± SD; overall: 3–6,
5.46 ± 0.68, N = 68; 2011: 4–6, 5.19 ± 0.75, N = 26; 2012: 4–6, 5.29 ±
0.73, N = 14; 2013: 3–6, 4.8 ± 0.91, N = 16; 2014: 4–6, 4.92 ± 0.51, N =
12). Brood sex ratios ranged from 0 (exclusively female) to 1 (exclusively
male) (Figure 1). Neither population nor mean brood sex ratios were found
to deviate from 0.50 within or across the four study years (Table 2). Because
mean brood sex ratio did not differ among years (H3 = 0.47, p = 0.93), data
were pooled in subsequent analyses (Table 2).
3.2. Parental plumage colour and brood sex ratio
When asking if male plumage colouration predicted brood sex ratios, we
found nests with males displaying more colourful tails contained a higher
proportion of male offspring (χ 2 = 7.29, p = 0.007; Table 3; Figure 2A).
This relationship was either significant or approached significance in three
out of four years (2011: χ 2 = 2.92, p = 0.09; 2012: χ 2 = 3.85, p = 0.05;
2013: χ 2 = 3.69, p = 0.05; 2014: χ 2 = 0.12, p = 0.73). We also found a
significant effect of male age; SY males had more male-biased broods than
Table 2.
Summary of mountain bluebird sex ratio data for the 2011–2014 breeding seasons.
Year

Broods

Nestlings
sexed

Population
sex ratio

W

p

Mean
brood sex
ratio ± SD

W

p

2011
2012
2013
2014

26
14
16
12

133
71
73
57

0.51
0.52
0.47
0.59

67.5
57.0
−95.0
165.0

0.86
0.73
0.57
0.15

29.5
13.5
5.5
14.5

0.46
0.53
0.85
0.23

Pooled

68

334

0.52

946.0

0.55

0.51 ± 0.20
0.54 ± 0.24
0.49 ± 0.23
0.58 ± 0.23

221.5

0.17

0.53 ± 0.22

Wilcoxon signed-rank tests were performed to determine if population sex ratios and brood
sex ratios deviated from unity.

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Behaviour (2016) DOI:10.1163/1568539X-00003350

Figure 1. Distribution of brood sex ratios (proportion of male offspring) for the 2011–2014
breeding seasons. The mean brood sex ratio (0.53) did not deviate from unity.

ASY males (Table 3). In addition, there was a marginal male age × male
rump PC1 interaction (p = 0.06). To examine this potential interaction, we
separated males by age and found a significant effect of male rump PC1
in SY males, where more colourful SY males produced more male-biased
broods (χ 2 = 5.68, p = 0.02); there was no relationship between ASY rump
PC1 and sex ratio (χ 2 = 0.02, p = 0.88; Figure 2B). In contrast to males,
females with lower rump PC1 values produced more male-baised broods
(χ 2 = 4.75, p = 0.03; Figure 3); there was no effect of tail PC1 or female
age (Table 3).
3.3. Parental provisioning rates and brood sex ratio
Finally, we asked whether parents adjusted provisioning rates in response to
offspring sex ratios. We found no effect of sex ratio on provisioning rates by
males or females during either the early or late nestling stage (all p > 0.34;
Table 4).

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Table 3.
Results of generalized linear mixed models examining the influence of plumage colouration
and age on sex ratio.
Variable

Estimate

SE

χ2

p

N

Male plumage colouration
Intercept
Male tail PC1
Male rump PC1
Male age
Male age × male rump PC1

−0.28
−0.30
−0.06
0.38
0.19

0.14
0.11
0.12
0.15
0.10

3.86
7.29
0.23
6.70
3.55

0.05
0.007∗
0.63
0.01∗
0.06

324
324
324
324
324

−0.07
−0.04
0.20
−0.07

0.12
0.10
0.09
0.12

0.38
0.20
4.75
0.28

0.53
0.66
0.03∗
0.59

330
330
330
330

Female plumage colouration
Intercept
Female tail PC1
Female rump PC1
Female age

We used nest ID nested within female identity as a random effect. Non-significant interactions were removed to derive final models.
∗ Significant interaction, p < 0.05.

3.4. Parental provisioning rates and plumage colouration
In most models, neither male nor female provisioning rates (both early and
late) were associated with male tail or rump plumage colouration (only the
relationship between male tail PC1 and late female provisioning approached
significance at p = 0.08; all other relationships p > 0.26). However, for
female provisioning during the early nestling period, there were significant
effects of male tail PC1 and an interaction between male age and tail PC1
(tail PC1: N = 61, F1,56 = 4.86, p = 0.03; tail PC1 × male age: N =
61, F1,56 = 11.75, p = 0.001), but not rump PC1 (N = 61, F1,56 = 0.44,
p = 0.51). After separating by age classes, the relationship between tail
PC1 and early female provisioning was significant for ASY males (N = 46,
r 2 = 0.24, p = 0.0006; Figure 4), but not SY males (N = 15, r 2 = 0.08,
p = 0.31).
4. Discussion
Over four breeding seasons, we observed support for sex allocation in mountain bluebirds: females paired with more colourful males produced more
male-biased broods. Our results were somewhat surprising, however, in that

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Behaviour (2016) DOI:10.1163/1568539X-00003350

Figure 2. (A) Broods contained a greater proportion of male offspring when females paired
to males with bright UV-blue tail plumage (SY and ASY males pooled). (B) SY males (open
circles, grey line) with brighter rump plumage produced more male-biased broods, while
there was no relationship between rump colouration and brood sex ratio in ASY males (closed
circles).

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Figure 3. Females with duller UV-blue tail plumage produced broods with a greater proportion of male offspring.

SY males produced more male-biased broods and a relationship between
rump colouration and male-biased broods was only present in SY males.
Another unexpected finding was that females with less colourful rumps
produced male-biased broods. However, Morrison et al. (2014) also found
perplexing relationships with female colour in the same population of mountain bluebirds, with an observation of negative assortative mating (SY female
tail PC1 was negatively associated with male rump PC1). Despite the relationship between male plumage colouration and offspring sex ratio, which
is consistent with adaptive sex ratio adjustment, we did not observe any
evidence that either females or males adjust their parental investment in response to brood sex ratios.
Relationships between plumage ornamentation and brood sex ratio have
been reported previously in several species. Of the studies investigating male
ornamentation as a driver of sex allocation, those finding significant relationships were generally conducted over three or more breeding seasons (range
1–8, mean ± SD = 3.9 ± 2.6, N = 6) (Ellegren et al., 1996; Sheldon et al.,

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Behaviour (2016) DOI:10.1163/1568539X-00003350

Table 4.
Results of a linear mixed model examining the influence of offspring sex ratio on provisioning
rates of male and female mountain bluebirds. We included nest ID nested within female
identity as a random effect.
Variable

Estimate

SE

t

p

N

1.36
−0.18

0.22
0.40

6.05
−0.47

<0.0001∗
0.64

60
60

0.33
0.29
0.08

0.33
0.30
0.03

0.99
0.97
2.55

0.33
0.34
0.01∗

60
60
60

Late male provisioning
Intercept
Sex ratio

1.81
0.72

0.47
0.84

3.83
0.86

0.0003∗
0.39

54
54

Late female provisioning
Intercept
Sex ratio

2.22
0.21

0.48
0.85

4.63
0.25

<0.0001∗
0.80

54
54

Early male provisioning
Intercept
Sex ratio
Early female provisioning
Intercept
Sex ratio
Nest watch time

∗ Significant value, p < 0.05.

1999; Griffith et al., 2003; Delhey et al., 2007; Mitrus et al., 2015; Romano
et al., 2015), while those finding no evidence for such a relationship were
conducted over three or fewer breeding seasons (range 1–3, mean ± SD =
2.0 ± 0.8, N = 4) (Saino et al., 1999; Rosivall et al., 2004; Korsten et al.,
2006; Czyź et al., 2012). A comparison between studies on the same species
illustrates the importance of the inclusion of multiple breeding seasons: in
barn swallows, Romano et al. (2015) found evidence to support sex allocation in relation to male ornamentation over eight breeding seasons, while
Saino et al. (1999) found no such evidence over three breeding seasons. Here,
we observed support for sex allocation in response to male mountain bluebird
plumage colouration over four breeding seasons. This relationship was either
significant or approached significance in all but one of our study years. Thus,
data spanning multiple breeding seasons may be necessary to reveal overall
trends of sex allocation both within species and populations.
Contrary to our expectations, we found that females paired to SY males
produced more male offspring. This is counterintuitive, as females may receive indirect genetic benefits by mating with older males (Brooks & Kemp,
2001) and, thus, often prefer older males as both social and extra-pair part-

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Figure 4. When paired to ASY males with bright tail plumage, females provisioned more
frequently during the early nestling phase.

ners (Kempenaers et al., 1997; Brooks & Kemp, 2001; Freeman-Gallant et
al., 2011). As a result, females paired to older males would be predicted
to produce male-biased broods. In addition, the relationship between rump
colouration and offspring sex ratio was only present in SY males, which is
somewhat surprising. However, Taff et al. (2011) found a similar relationship
between male age, plumage ornamentation and brood sex ratio in common
yellowthroats. One possible explanation is because first-year males moult
rump feathers shortly after fledging, there was greater variability in condition
amongst first-year males, making rump colouration a more reliable signal of
quality in SY males than ASY males. However, this fails to account for the
lack of an age effect in tails, which are grown under different conditions in
SY and ASY males (in the nest vs. free-living, respectively).
The negative relationship observed between female rump colour and
brood sex ratios is perplexing. Trivers & Willard’s (1973) seminal hypotheses regarding sex allocation stated that females in good condition should
produce male-biased broods, assuming offspring condition and survival is

16

Behaviour (2016) DOI:10.1163/1568539X-00003350

correlated with maternal condition (Trivers & Willard, 1973). This relationship between maternal condition and brood sex ratio has been well studied
and validated in several species (Nager et al., 1999; Whittingham & Dunn,
2000; Alonso-Alvarez & Velando, 2003; Pike & Petrie, 2005). Thus, based
on sex allocation theory, more colourful females (presumably in better nutritional condition during the time of moult) should produce male-biased
broods. The fact that we observed the opposite clearly indicates the need
for more research into the signalling system of mountain bluebirds.
Female provisioning behaviour was positively associated with mate attractiveness. During the early stages of nestling development, females paired
to older, ASY males with brighter tail plumage colouration provisioned their
offspring at a higher rate. This result is somewhat surprising, as previous
work by Morrison et al. (2014) in our study population, and by Balenger et
al. (2007) in a population of mountain bluebirds from Wyoming, USA, failed
to find a relationship between male or female plumage colouration and provisioning rates.
One potential explanation for the relationship between female provisioning and male colouration is differential resource allocation. Under the Differential Allocation Hypothesis, individuals maximize fitness through strategic
partitioning of parental investment (Burley, 1986). Females paired to highly
attractive males may increase parental investment and, in return, attractive
males may be able to decrease parental investment (Linville et al., 1998; Jawor et al., 2004; Siefferman & Hill, 2005). Though plausible, we did not
observe any evidence of differential allocation of parental investment driving increased maternal investment (as measured by provisioning rate). These
results are consistent with the findings of Balenger et al. (2007) and Morrison et al. (2014); they similarly found no direct association between male
and female plumage colouration and provisioning rates.
An alternative explanation for the relationship between female provisioning and male colouration is that provisioning rates may be related to territory
quality. In blue grosbeaks (Passerina caerulea), the quality of the territory a
male is able to establish is associated with individual condition and UV-blue
plumage colouration (Keyser & Hill, 2000). In addition, males on high quality territories with abundant prey provision at increased rates (Keyser & Hill,
2000). As mountain bluebirds also display UV-blue plumage colouration, it
is plausible that male colouration may be associated with quality of the territory a male is able to obtain. Thus, one possibility is that females paired

E.S. Bonderud et al. / Behaviour (2016)

17

with colourful males are rearing young on high quality territories with easily accessible prey and as a result, are able to provision at a higher rate. At
present, no measures of territory quality have been taken in our study population. An important next step in deciphering the underlying cause(s) of
this relationship would be to assess food availability and other indicators of
habitat quality in each male bluebird’s territory.
Sex allocation theory predicts that females should increase investment and
adjust the sex ratio of their broods in response to the differential reproductive
value of sons and daughters. As predicted, we found that female mountain
bluebirds produced more male-biased broods when paired with attractive
males (i.e., higher tail UV-blue plumage colouration). In addition, we found
females paired with more colourful males provisioned their offspring more
frequently. However, there was no evidence that either males or females
adjusted provisioning rates in response to brood sex ratios. Together, these
results provide support for sex allocation in mountain bluebirds, and suggest
male attractiveness may influence female reproductive decisions. However,
more work is clearly needed to understand the role of male age and female
plumage colouration in the signalling system of mountain bluebirds.
Acknowledgements
We thank the Kamloops Naturalist Club, in particular G. Dreger and
P. and J. Gray, for use of their bluebird boxes for this study. We also thank
N. Cheeptham, J. Bailey, T. Rodrigues, A. Morrison, and S. McArthur for
assistance in the field and lab. We thank S. LaZerte, K. Otter and two anonymous reviewers for helpful comments that improved the manuscript. Funding
was provided by a Natural Sciences and Engineering Research Council of
Canada (NSERC) Discovery Grant to M.W.R. and a Thompson Rivers University undergraduate research award to E.S.B.
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