Beauty alone is insufficient: female mate choice in the barn swallow


SUZUKI AWARD

Masaru Hasegawa

Beauty alone is insufficient: female mate choice in the barn swallow

Received: 16 September 2017 / Accepted: 27 October 2017 / Published online: 11 November 2017
� The Author(s) 2017. This article is an open access publication

Abstract The barn swallow, Hirundo rustica, is a model
species for studying sexual selection, particularly female
mate choice. Although there have already been several
reviews of female mate choice and its geographic vari-
ation in this species, all of them have focused on sec-
ondary sexual characteristics. Here, for better
understanding of the general pattern of female mate
choice and their influence on male phenotype, I review
all of the female mate choice criteria ever reported in the
barn swallow, emphasizing the importance of relatively
inconspicuous male traits. These include resources de-
fended or provided by males, such as territory and
paternal investment. In addition, females prefer a nest-
ling-like vocalization, enticement call, which is particu-
larly noteworthy because females prefer immature calls.
This pattern contrasts with female choice based on sec-
ondary sexual characteristics, in which more mature,
elaborate male traits are almost always favored. Nest-
ling-like male traits are widespread, and thus female
avoidance of, rather than preference for, mature forms
might be common. In addition to selection on the target
trait itself, these resources and nestling-like male traits
would also matter in understanding the evolution of the
overall male phenotype and its geographic variation, due
to the interrelationships among male target traits and
those among female mate preferences. Female prefer-
ences for inconspicuous traits are highly dependent on
ecological factors such as nest predation pressure, and
thus overall male phenotype including secondary sexual
characteristics might be more predictable than previ-

ously thought. Future studies should focus on not only
conspicuous secondary sexual characteristics but
inconspicuous male traits.

Keywords Female mate preference Æ Hirundo rustica Æ
Nestling-like traits Æ Secondary sexual characteristics Æ
Territory quality

Introduction

Female mate choice is a key issue in evolutionary ecol-
ogy: it affects the evolution of elaborate male traits and
their geographic variation, as well as population growth,
extinction, and speciation, at least in theory (Andersson
1994; Coyne and Orr 2004; Brooks and Griffith 2010). In
empirical studies, however, its understanding is still
insufficient, because most studies have focused solely on
secondary sexual characteristics (i.e., traits that are fully
developed at maturation but are not a direct part of the
reproductive organs; e.g., see Tazzyman et al. 2014 for a
recent review), perhaps in part due to the intuitive
importance of sexual selection (Andersson 1994) or
simply due to its eye-catching nature (Tazzyman et al.
2014). This circumstance potentially biases our under-
standing of female mate choice and its evolutionary
impact on male phenotype. To properly evaluate the
general pattern of female mate choice and its evolu-
tionary causes and consequences, not only secondary
sexual characteristics but also other, relatively incon-
spicuous male sexual or courtship traits should be con-
cerns.

One approach for studying general pattern (and
variation) of female mate choice is to focus on a par-
ticular species and review all of the female mate choice
criteria ever reported. Such an approach is particularly
useful for a model system that has been studied by
many researchers with different interests. The barn
swallow, Hirundo rustica (see frontispiece picture; see
Fig. S1), is such a model system of female mate choice.
After Møller (1988) experimentally demonstrated fe-

Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s11284-017-1527-3) contains supplemen-
tary material, which is available to authorized users.

Masaru Hasegawa is the recipient of the 4th Suzuki Award from
the Ecological Society of Japan.

M. Hasegawa (&)
Department of Evolutionary Studies of Biosystems, Sokendai (The
Graduate University for Advanced Studies), Hayama, Japan
E-mail: perorobomusadiobe@gmail.com
Tel.: (+81)-46-858-1562

Ecol Res (2018) 33: 3–16
DOI 10.1007/s11284-017-1527-3

https://doi.org/10.1007/s11284-017-1527-3
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male mate preference for elongated male tails in this
monogamous bird (also see Bańbura 1986 for a cor-
relational study), many other studies tested and
demonstrated female mate preference for long tail
feathers and other male characteristics (see below).
Also, because this is a cosmopolitan species distributed
across all continents except Antarctica, and exhibits
different phenotypes (e.g., some subspecies have rela-
tively short tails with dark rufous-chestnut underparts;
Turner 2006), the barn swallow is a suitable system for
studying geographic variation as well as speciation
(sensu Scordato and Safran 2014). Until now, several
reviews have been published concerning female mate
choice and its geographic variation in this species (e.g.,
Møller 1994a; Turner 2006; Scordato and Safran 2014;
Romano et al. 2017a). However, all of them are fo-
cused solely on secondary sexual characteristics (and
mostly on plumage ornaments), simply because other
kinds of sexually selected traits are less studied than
secondary sexual characteristics.

Here, I reviewed female mate choice not only on
secondary sexual characteristics (i.e., ‘‘beauty’’ traits)
but also on other sexual or courtship traits. I gathered
studies of female choice at pair formation, at (extra-pair)
copulation, and differential allocation (i.e., increased
maternal investment when paired with attractive males;
Burley 1986, 1988; Møller and Thornhill 1998), which
can be regarded as a form of mate choice (Sheldon 2000;
Brooks and Griffith 2010). I start this review by
describing courtship behavior of male barn swallows,
which provides insights into the function of each male
trait. As in previous studies (see review papers above), I

focused on breeding grounds, because males and females
usually arrive at the breeding ground separately (though
courtship behaviors can be observed even at wintering
grounds; Turner 2006). Second, I listed all the known
criteria of female mate choice with particular attention
to the difference between secondary sexual characteris-
tics and relatively inconspicuous male traits. Finally, I
discuss how female preference for inconspicuous male
traits affects overall male phenotype.

Male courtship displays

Most male barn swallows commence pairing courtship
in the air while some start courting beside perching fe-
males (Fig. 1). Males sing vigorously while courting.
Then, they lead females to an old nest or to a potential
nest site, emitting enticement calls. When the males have
successfully led females to the nest site, they are often
observed to sequentially show females other nests in
their territories. Thus, males can attract females to nest
sites by their plumage characteristics, songs, and
enticement calls, and thereafter show off nest sites in
their territories. These traits would be potentially
important targets of sexual selection via female mate
choice (i.e., mate choice criteria), compared to male
traits that can be assessed only afterwards (e.g., paternal
care behaviors), because sexual selection intensity (or
strictly, effect size in each selection episode) decreases
with the progress of the breeding season (Romano et al.
2017a).

Fig. 1 Courtship sequence of male barn swallows at pair forma-
tion, shown with blue arrows. Detailed behaviors are listed for
each courtship element. The numbers of observations are denoted

in brackets; values in parentheses indicate the numbers of
instances in which males successfully attracted females to their
nests. Redrawn from Hasegawa (2011). Color figure online

4



Female mate choice criteria

In barn swallows, many studies have focused on female
mate choice. I categorized female mate choice criteria into
three groups: secondary sexual characteristics, resources,
and nestling-like traits (Table 1). In this review, I did not
include male arrival date (e.g., Møller et al. 2003), age
(e.g., Lifjeld et al. 2011), kinship (Kleven et al. 2005), or
body or physiological condition (e.g., Møller et al. 2003;
Kojima et al. 2009; Romano et al. 2014). This is not
because these traits are unimportant, but because females
may use other phenotypic traits correlated with these
traits for mate choice (Møller et al. 2003; Romano et al.
2014). In other words, these variables would be infor-
mation (signal) contents rather than mate choice criteria
itself. I also excluded female mate choice in unnatural
environment (e.g., aberrant tail feathers in Chernobyl,
which is virtually absent in other populations; Møller
1993a), although the same characteristics can be found in
normal populations in smaller proportions.

Secondary sexual characteristics

The most well-known target of female mate choice in the
barn swallow, would be the long, sexually dimorphic tail
(reviewed in Møller 1994a; Møller et al. 1998a). Al-
though there are some notions that the aerodynamic
advantages (i.e., maneuverability, here) of deep fork tails
can explain the evolution of this trait (e.g., Thomas
1993; Norberg 1994; Evans 1998; also see e.g., Aparicio
et al. 2012; Pap et al. 2015 for objection to this expla-
nation: reviewed in Hasegawa et al. 2016b; Hasegawa
and Arai 2017a), population mean tail length should be
aerodynamically costly, indicating that female prefer-
ence for long-tailed males should account for the evo-
lution of long tails, at least in part (e.g., Buchanan and
Evans 2000; Rowe et al. 2001). Because only high-
quality (e.g., viable) males can bear the cost of long-tails,
females obtain high-quality mates by preferring long-
tailed males (reviewed in Møller 1994a; Turner 2006;
also see Romano et al. 2017b). Likewise, two other tail
characteristics have been reported to be important cri-

Table 1 Summary of female mate choice criteria reported for the barn swallow

Variables Direction
a

Context
b

Representative studies
c

Secondary sexual characteristics
Plumage ornaments

d

Tail length/asymmetry + Both Møller (1988),
E
(1990),

E
(1992a, b),

E
(1993b),

E
(1994a, b);

E

Møller et al. (2006);
E
Saino et al. (1997b):

E
Smith and

Montgomerie (1991);
A
Vortman et al. (2011, 2013)

M

White tail spots size/shape + Both Kose and Møller (1999);
E
Kose et al. (1999);

E
Møller (2017);

E

Hasegawa (unpub. data)
J
(mentioned in Hasegawa et al. 2012b

J
)

Throat patch coloration/size + Both Ninni (2003);
E
Safran et al. (2005);

A
Hasegawa et al. (2010a);

J

Hasegawa and Arai (2013a, b)
J

Ventral coloration + Both Safran and McGraw (2004);
A
Safran et al. (2005);

E

Vortman et al. (2011, 2013)
M

Dorsal coloration + Social mate choice Garamszegi et al. (2006)
E

Song attributes
Song rate + Sire choice Møller et al. (1998b)

E

Song duration + Social mate choice Garamszegi et al. (2005)
E

Bout rate + Social mate choice Garamszegi et al. (2006)
E

Song length + Social mate choice Garamszegi et al. (2006)
E

Repertoire size + Social mate choice Garamszegi et al. (2006)
E

Versatility + Social mate choice Garamszegi et al. (2006)
E

Peak amplitude frequency + Social mate choice Garamszegi et al. (2006)
E

Rattle impulse tempo + Social mate choice Garamszegi et al. (2006)
E

Song complexity + Sire choice Wilkins et al. (2015)
A

Song tempo + Sire choice Wilkins et al. (2015)
A

Resources defended or provided by males
Territory quality + Social mate choice Hasegawa et al. (2012a)

J

Nest building behavior + Social mate choice Soler et al. (1998)
E
; Møller (2006)

E

Mate guarding + Sire choice Møller (1987)
E

(Inter-territory distance)
e

+ Sire choice Hasegawa et al. (2010b)
J
; Møller and Ninni (1998)

E
;

but see Saino et al. (1999)
E

Nestling-like traits
Enticement call – Social mate choice Hasegawa et al. (2013)

J
; Hasegawa and Arai (2016)

J

a
Direction indicates positive (exaggeration) or negative (reduced form). The direction of female mate preference is often difficult to judge,
and thus I considered the direction as positive or negative when females preferred more or less adult male-like characteristics, respectively.
Full song is emitted solely by adult males (Turner 2006), and so I considered the direction positive for the characteristics of full song
bFemale mate preference can be divided into social mate choice (e.g., pair formation, pre-mating period, breeding date, brood numbers)
and choosing sires (i.e., paternity allocation)
cFor reference, I included study region information (E Europe, A North America, M Middle east, J Japan; see Romano et al. 2017a for the
formal analysis of geographic variation in the intensity of sexual selection on plumage ornaments)
dSee Romano et al. (2017a) for effect size and its population divergence
e
See text for explanation

5



teria of female mate choice: fluctuating tail asymmetry
(e.g., Møller 1992a, 1993b) and white tail spots (e.g.,
Kose and Møller 1999; Kose et al. 1999). These char-
acteristics can evolve as byproducts of long tails (e.g.,
Johnstone 1994), as amplifiers (Fitzpatrick 1998; also see
Møller 2017 for potential illusion effects of white tail
spots), or as quality indicators, because these traits also
indicate male quality (e.g., condition at molt; Møller
1994a, b; Saino et al. 2015).

In addition to these tail characteristics, plumage
coloration would be important. A red throat patch
(color: Ninni 2003; size: Møller 1994a; Hasegawa and
Arai 2013a), and other ventral plumage feathers (e.g.,
breast and vent coloration; Safran and McGraw 2004;
Safran et al. 2005) are related to several indices of female
choice (e.g., mating success, paternity; reviewed in Ro-
mano et al. 2017a). Because all of these ornaments are
sexually dimorphic, one may argue that female prefer-
ence for these traits are as expected (Andersson 1994).
However, this might not always be the case, as sexual
dimorphism evolved in the past and might be main-
tained to achieve threshold levels of stimulation or for
other reasons (Candolin 2003; van Doorn and Weissing
2004). For example, the blue-black coloration of dorsal
feathers is highly sexually dimorphic in this species, but
female preference for this coloration would be at best
weak (Perrier et al. 2002; Galván and Møller 2009; also
see Garamszegi et al. 2006; Table 1). Because ventral,
but not dorsal, plumage is pheomelanin-based col-
oration, honest signaling via pleiotropy of pheome-
lanogenesis genes and resource tradeoff between
pheomelanin production and somatic maintenance may
facilitate female preference on the ventral coloration
(reviewed in Ducrest et al. 2008; Roulin 2016). Consis-
tent with this perspective, in the barn swallow, throat
and ventral plumage coloration (and its pigmentation) is
linked to several physiological traits (e.g., testosterone
levels), age, body condition, and viability across the
range of the species (e.g., Safran et al. 2008; Galván and
Møller 2009, 2013; Hasegawa et al. 2014; Vitousek et al.
2016; but see Saino et al. 2013).

Song is another well-known secondary sexual char-
acteristic in passerines including the barn swallow (re-
viewed in Turner 2006). There are several studies
indicating that characteristics of song are related to male
quality (e.g., parasite infection, hormone levels, immu-
nity, and so on; Møller 1991a; Galeotti et al. 1997; Saino
et al. 1997a; Garamszegi et al. 2005, 2006; Dreiss et al.
2008), which may facilitate female mate choice based on
male traits. For example, Møller et al. (1998b) found
that song rate is related to extra-pair paternity together
with tail length, indicating female preference for a high
song rate. Wilkins et al. (2015) found that song com-
plexity together with feather length (including tail
length) affects paternity success. A similar, but weaker,
relationship has been found for song tempo (Table 1;
also see Wilkins et al. 2015 for other non-significant
song characteristics). Likewise, Garamszegi and his
colleagues have reported relationships between the pre-

mating period, a measure of female preference, and song
characteristics (e.g., song length; Garamszegi et al. 2005,
2006; Table 1; also see Garamszegi and Møller 2004 for
unpublished non-significant data). Other characteristics
of song (e.g., rattle duration) have not yet been
demonstrated to be targets of female choice, although
they might be used in male–male contests rather than for
attracting females (Galeotti et al. 1997; Scordato and
Safran 2014; Wilkins et al. 2015; also see Galeotti et al.
1997 for a strong positive correlation between testos-
terone level and rattle duration).

In summary, many secondary sexual characteristics
would be used in female mate choice in this species
(Table 1). The target, direction, and intensity of prefer-
ence varies among populations at least for plumage
ornaments (e.g., Safran et al. 2016; Wilkins et al. 2016;
reviewed in Scordato and Safran 2014; Romano et al.
2017a), affecting the geographic variation in male trait
expression, although most studies have found positive
female preference (i.e., toward exaggerated traits; Ro-
mano et al. 2017a). Well-ornamented males provide less,
rather than more, paternal care compared to less-orna-
mented males in barn swallows (e.g., de Lope and
Møller 1993; Saino and Møller 1995; Maguire and Sa-
fran 2010; Hasegawa et al. 2014; Hasegawa and Arai
2015a), which may be costly for females even if well-
ornamented males have fewer ectoparasites and thus
lower risk of contagion (Møller 1994a). Females would
rather obtain indirect benefits (i.e., genes for attractive-
ness and viability) by preferring well-ornamented males
(Møller 1994a; also see Møller and Jennions 2001 for
unpublished data on song in relation to direct benefits).
Still, even in this model species of female mate choice,
direct evidence of female mate choice is scarce (but see
Møller 1988, 2001 for female extra-pair copulation
behavior), and most of them rely on indirect evidence
such as mating pattern or extra-pair paternity, both of
which can be affected by male–male contests, male
strategy, or ecological factors such as inter-nest distance,
which cannot easily be teased apart by experimental
manipulation (e.g., Hasegawa et al. 2010b; Lifjeld et al.
2011; reviewed in Westneat and Stewart 2003; also see
Møller 1991b; Møller and Ninni 1998; Saino et al. 1999
for relationship between inter-nest distance and extra-
pair copulation or paternity). Thus, these observations
and even experiments should be interpreted carefully,
though careful interpretation is required for other works
as well (e.g., for those with small sample size; see below).

Resources defended or provided by males

Together with male plumage and song characteristics,
territory quality is one of the most well-known female
mate choice criteria in passerine birds (e.g., Alatalo et al.
1986; Slagsvold 1986). Because barn swallows defend
only a small territory (< 20 m2) with few resources (i.e.,
nest and perch sites; Turner 2006), and because repro-
ductive success does not depend on territory quality but

6



on male quality (Møller 1994a), territory is thought to
be unimportant in this species (Møller 1990, p. 463). In
the same colonial population, territory did not predict
male settlement patterns, which was inconsistent with
the hypothesis that territory quality is important in fe-
male mate choice (Møller 1990, 1994c). However, this
might not be the universal pattern in the barn swallow.
Although these studies focused on colonial breeders in
livestock stalls where nest predation is virtually absent
(Møller 1994a; Turner 2006), outdoor populations
experience high nest predation rates (see Fig. 2 for nest
predation attempt by the carrion crow). In Japan,

approximately 50% experience nest failure (Fujita 1993;
Hasegawa et al. 2012a, 2017; also see Turner 2006 for
the potential importance of crows as nest predators in
this region: also see Liang et al. 2013; Su et al. 2017 for
the potential importance of interspecific brood para-
sitism), though actual predation rates depend on popu-
lation (e.g., see Møller 2010 for subtle differences
between colony and outdoor populations in European
subspecies). In Japan, territory quality, measured by the
quality and quantity of old nests, predicts seasonal
reproductive success (Hasegawa et al. 2012a), and males
did settle in better territories than their previous terri-

(a) (b)

Fig. 2 A nest predation attempt by a carrion crow. Color figure online

7



tories when they changed territories across years in
outdoor breeding sites (Fig. 3). As expected, males with
high-quality territories paired earlier, indicating female
mate choice based on territory quality (Hasegawa et al.
2012a; though there may still be some population dif-
ferences in the relationship between territory quality and
reproductive parameters; see above). Although territory
quality is often related to male morphological traits
(e.g., throat coloration in this species; Hasegawa et al.
2014; Wilkins et al. 2015), multivariable analysis indi-
cates that territory quality is an important mate choice
criteria than male morphology (in fact, effect size,
Zr = 0.60, 95% CI = 0.14–1.06 for laying date and
0.62, 95% CI = 0.11–1.12 for pairing date, computed
from R

2
value, is quite high for female preference for

territory quality, though sample sizes were small
(n = 21, 18, respectively); note that mean overall effect
size for plumage ornaments was 0.21; Romano et al.
2017a). As swallows choose high-quality (i.e., intact)
nests within their territories (Hasegawa et al. 2012a) or
choose colonies/breeding sites with many high-quality
nests (Safran 2004, 2007; also see Ringhofer and Hase-
gawa 2014), it is not surprising that females choose
territories with high-quality nests, though experimental
validation remains to be carried out.

Because territory is not the sole resource provided by
males in this biparental care species, it is natural to
suppose that other types of resources may also be the
targets of female preference. For example, Soler et al.
(1998) argued that female swallows should invest more
when breeding with males of high parental quality, and
found that females provide larger amounts of repro-
ductive investments, measured as total numbers of eggs
laid during the breeding season, when paired with
superior nest builders. Because male contribution to nest
building reflects his willingness to invest in reproduction
(i.e., feeding rate: Møller 1994a, 2006), female preference

for these males accompanies direct benefits (also see
Soler et al. 2007 for additional indirect benefits). Al-
though males provide several types of paternal cares
(e.g., provisioning to nestlings and fledglings, and incu-
bation in some subspecies; Turner 2006), whether fe-
males pay particular attention to specific paternal care
behaviors is unknown. In addition to direct parental
care, males may provide females with time and energy by
mate guarding, which can improve female foraging
efficiency (i.e., indirect parental care; sensu Fedy and
Martin 2009). Møller (1987) showed that female extra-
pair copulation decreased with increasing male mate
guarding, which can be regarded as female preference
for males who have high fertilization ability. Likewise,
males that prevent other males from settling nearby
suffer less paternity loss (e.g., Møller and Ninni 1998;
Hasegawa et al. 2010b; but see Saino et al. 1999) and
thus this might also be female preference for indirect
parental care (Table 1).

In sum, resources defended or provided by males can
directly affect reproductive success and thus facilitate
female preference at least in some circumstances (Ta-
ble 1). By preferring such males, females can obtain di-
rect benefits, increasing the number and quality of
offspring (note that indirect benefits should automati-
cally arise whenever male target traits are heritable;
Kokko et al. 2003). Apart from secondary sexual char-
acteristics, some resources (e.g., territory) are not
inherent characteristics of males, and thus promote
male–male contest for resources. Therefore, female
preference for resource holders results in indirect mate
choice (sensu Wiley and Poston 1996) on the male traits
used in male–male contests, confounding with direct
mate choice for the male traits (note that direct mate
choice for the male traits should also be enhanced if it
increases female fitness; Wong and Candolin 2005).
Unfortunately, unlike the plumage characteristics I no-
ted in the previous subsection, resources defended or
provided by males are difficult to experimentally
manipulate and, thus, it is much more difficult to exclude
confounding effects from unmeasured traits than when
studying plumage characteristics (though not impossible
as it has been done in the pied flycatcher: Alatalo et al.
1986). To understand how male traits (and female
preference on the traits) evolved, researchers should take
resources (e.g., territory) into account, possibly with
experimental manipulation of resources.

Nestling-like traits

Although secondary sexual characteristics and territory
quality are well-known criteria of female mate choice,
there are several other criteria. In the barn swallow,
enticement calls (Turner 2006, p. 64) are noticeable
vocalizations emitted during pairing courtship (Fig. 1;
also see supplementary sounds in Hasegawa and Arai
2016 for some examples). Given the resemblance to
nestling food-begging calls, male enticement calls may

Fig. 3 Territory quality of males that moved into a new territory
without their previous territories being occupied and males that
settled in the same territories they held in the previous season in
Joetsu population in Japan. White and black bars indicate the
mean (± SE) quality of the previous and current territory,
respectively. Statistics are based on t tests and paired t tests.
Redrawn from Hasegawa (2011)

8



attract females by exploiting female parental care for
nestlings (i.e., attraction to nestlings; sensu Christy
1995). As predicted, Hasegawa et al. (2013) showed that
male enticement calls and nestling food-begging calls
structurally resemble each other, as compared to other
male vocalizations (Fig. 1 in Hasegawa et al. 2013) and
unpaired females are similarly attracted to the playback
of nestlings’ food-begging calls and male enticement
calls. Hasegawa and Arai (2016) further demonstrated
that unpaired females were more attracted to height-
ened-pitch (i.e., more nestling-like) calls than to control
enticement calls (though female swallows prefer lower,
rather than higher, pitched songs; Garamszegi et al.
2005, 2006). Because male enticement calls pitched lower
than typical nestling food-begging calls, the similarity to
nestlings decreases with maturation at least in pitch
height.

The most intriguing point of female preference for
male enticement calls is that females are attracted to
males with immature forms (Table 1), which contrasts
with female mate choice based on secondary sexual
characteristics that almost always favors more ma-
tured, elaborate traits (Table 1; also see Tazzyman
et al. 2014 for other species). Although I focus here on
nestling-like vocalizations, this may not be the sole
nestling-like traits. Many adult birds including male
barn swallows possess characteristics that resemble
those of nestlings (or informally, ‘‘cute’’ traits; sensu
Jones 1995), such as courtship begging, colorful gape,
and so on (reviewed in Bradbury and Vehrencamp
1998), though it is premature to argue about their
evolutionary relationship. Thus, the directionality of
female mate preference, deduced from those for sec-
ondary sexual characteristics (i.e., toward exaggera-
tion; reviewed in Tazzyman et al. 2014) might not be
generalized into all courtship traits until female choice
on these traits is tested. Unfortunately, except for
enticement calls, experimental manipulation of nest-
ling-like traits (e.g., courtship begging) is difficult to
accomplish, which remains to be tested in the future
with advanced statistical and manipulation techniques
(e.g., use of robotic models: Patricelli et al. 2006).
Female mate preference for mimetic male signal
(nestling-like traits, here) is expected even if the
preference is costly, given that female attraction to
certain stimuli (nestlings, here) is adaptive (Christy
1995; Arnqvist 2006).

Differences among the three categories

It is interesting that three categories of female mate
choice criteria listed here would have different sexual
selection mechanisms (Fig. 4). Secondary sexual
characteristics provide females with indirect benefits,
while resources provide females with direct benefits
(but note that males who provide resources can also
provide indirect benefits; also see below). Nestling-like
traits attract females via a sensory trap to exploit fe-

male parental care for nestlings, and thus exploit the
sensory bias of females. These traits correspond to the
three main mechanisms proposed to explain how
mating preferences arise and select for male traits
(Candolin 2003; also see Safran et al. 2013 for a
variant). It should be noted that these three mecha-
nisms are not mutually exclusive. For example, as
noted above, indirect benefits should automatically
arise whenever male target traits are heritable (Kokko
et al. 2003), and direct benefits can affect female
preference for secondary sexual characteristics to
some extent (e.g., ectoparasites; Møller 1994a). Sen-
sory bias may also exist in female preference for re-
sources or secondary sexual characteristics (see
above), which can promote subsequent coevolution
between male traits and female preference (e.g., sex-
ually antagonistic coevolution; Arnqvist 2006). Still,
differences in the main mechanisms provide an excel-
lent opportunity of simultaneous evaluation and pre-
diction of the evolution of each focal trait and its
correlates (see below).

Importance of inconspicuous male traits on overall phe-
notype

Given that females prefer relatively inconspicuous male
traits as well as conspicuous secondary sexual charac-
teristics, how can they influence overall male phenotype?
Of course, female preference for each male trait would
select for each target trait (Andersson 1994), as noted in
the previous section. However, the evolution of one trait
is rarely independent of other traits because of the
interrelationships among male traits and among female
preferences, as is often discussed in the context of mul-
tiple cues in mate choice (reviewed in Møller and
Pomiankowski 1993; Candolin 2003; Bro-Jørgensen
2010). Here, I briefly discuss each topic, to facilitate
understanding of the evolutionary consequences of fe-
male mate choice. Then, I present how consideration (or
ignorance) of inconspicuous male traits affects our
understanding of evolution of overall male phenotype
with a simple hypothetical scenario.

Fig. 4 Schematic illustration of the three categories of female mate
preference criteria in relation to the most likely causes of the
preference in the barn swallow. Thick lines represent main linkages,
while thin lines are also likely involved in the evolution of female
preferences and corresponding male target traits (see text)

9



Interrelationships among male traits

Several studies have demonstrated positive intercorre-
lations among male secondary sexual characteristics in
barn swallows (e.g., Møller et al. 1998a; Kose and
Møller 1999; Kose et al. 1999; Saino et al. 2003; Hase-
gawa et al. 2010a; but see Vortman et al. 2011; Safran
et al. 2016 for no detectable relationships). Still, it is
often unclear whether these patterns reflect evolutionary
covariation without a well-designed experiment (e.g.,
Wagner et al. 2012; van Noordwijk and de Jong 1986;
Stearns 1992; Andersson et al. 2002; Saino et al. 2003),
due to individual variation in resource availability (e.g.,
when the allocation between the traits varies less than
the total investment, a positive correlation can be pre-
dicted even if there is a trade-off between two orna-
ments). For example, colorful ventral plumage and tail
ornaments vary inversely across regions, subspecies, and
even species within the genus Hirundo (Turner 2006;
Hasegawa and Arai 2013b; Hasegawa et al. 2016b),
indicating that within-population patterns do not always
predict evolutionary relationships in swallows (also see
Vortman et al. 2015 for heritable variation in the relative
investment of the two ornaments). An exception is the
case in which traits are developmentally and functionally
(or genetically) integrated (Andersson et al. 2002), in
which case the evolution of one trait accompanies those
of others (e.g., long, symmetrical tails; Møller 1990,
1993b, Balmford and Thomas 1992). A positive corre-
lation between territory quality and male plumage col-
orfulness might be one such case, because melanin
pigmentation is often pleiotropically interrelated to
several other traits such as aggressiveness (see above;
Hasegawa et al. 2014; Wilkins et al. 2015; also see
Møller 2002 for decreased aggressiveness in colonial
populations where territory quality is negligible). Such
an interrelationship might be reinforced by hormonal
feedback perhaps via social interactions, because plu-
mage coloration affects testosterone levels, which is
linked to aggressive behavior (Safran et al. 2008). Other
interrelationships (e.g., territory and song: Wilkins et al.
2015) might also be reinforced by hormonal feedback,
which remains to be clarified. In addition, nestling-like
traits should be related to male secondary sexual char-
acteristics, although a negative relationship can be pre-
dicted in this case, because nestling-similarity decreases
with maturation, which contrasts with secondary sexual
characteristics that increase with maturation (see above;
Table 1). Hasegawa and Arai (2016) found that males
with less-colorful throat patches emitted more nestling-
like calls. This can also be interpreted as less-orna-
mented males can still attract females with more nest-
ling-like vocalizations (i.e., they are alternative female
attractants; Candolin 2003), maintaining the variation in
these traits or even predicting a negative evolutionary
relationship between them. In another negatively cor-
related pair of female mate choice criteria, tail length
and nest-building behavior, Møller (2006) found that a
longitudinal decrease in nest size (and thus male

investment in nesting) could be accounted for by indirect
selection on long tails, which have elongated over the
past 25 years. Selection on one trait would affect the
expression of correlated traits as well, and thus the
evolution of one trait cannot be understood without
considering the others.

Interrelationship among female mate preferences

The evolution of female mate preference for a specific
male trait would not be independent of the evolution of
a preference for another trait, because the benefits and
costs of one female preference depend on those of other
preferences. As noted in Candolin (2003), theoretical
models generally assume an increased cost of assessment
when females use multiple cues in mate choice (which
inhibits the evolution of multiple cues in mate choice;
e.g., Schluter and Price 1993; van Doorn and Weissing
2004); however, in reality, costs as well as benefits of
choice depend on focal traits (e.g., cost of assessment for
adjacent traits should be low; Kose and Møller 1999;
Arai et al. 2017). Thus, when females obtain higher net
benefits by preferring specific combinations of male
traits, preference for the combination is expected.
Vortman et al.’s study may represent one such case:
males with two experimentally enhanced ornaments (tail
length and plumage coloration), but not males with ei-
ther experimentally enhanced one ornament, had in-
creased within-pair paternity, indicating female
preference for the combination (Vortman et al. 2013).
This preference would be adaptive for females to avoid
interbreeding with other adjacent subspecies in this East-
Mediterranean subspecies (where an adjacent subspecies
has more colorful plumage with shorter tails and an-
other has less colorful plumage with longer tails than the
focal subspecies). Because the same treatment rather
decreases paternity in the North American subspecies
(Safran et al. 2016), female preference for each ornament
(and combinations of ornaments) may be population-
dependent (see Romano et al. 2017a for meta-analysis).
Although these studies focused solely on plumage
ornaments, interacting female preferences for plumage
ornaments and song have also been reported. Møller
et al. (1998b) found that female preference for song rate,
measured by paternity allocation, increased with the
sire’s tail length, perhaps because females placed more
weight on song (which indicates superior current con-
dition) when males had longer tails (which indicate high
long-term quality). These studies focused on paternity
allocation, but some interrelationship among male
ornaments at pair formation should also be expected,
because females receive territory and paternal care in
addition to sperm from social mates, which is further
complicated by female–female competition for limited
resources (e.g., territory). In a correlational study, the
probability of pair formation was predicted by the
negative interplay between tail length and plumage col-
oration (Hasegawa and Arai 2017b), though the relative

10



importance of female mate preference and male–male
competition for resources remains to be clarified. Inter-
relationships between female preference for secondary
sexual characteristics and other male traits have,
unfortunately, not yet been reported but may also be
interdependent. For example, it is unlikely that indi-
vidual preference for male enticement calls has no
influence on preference for male song (even if females,
on average, prefer higher-pitched enticement calls and
lower-pitched song; Hasegawa and Arai 2016; Garam-
szegi et al. 2005, 2006). In addition, it is likely that the
benefits and costs of choosing well-ornamented males
depend on whether they hold high-quality territories
(i.e., whether they can avoid nest predation or para-
sitism), as explained in the next subsection. Ignoring
some important female choice criteria may prevent to
explain the evolution of the focal traits.

Divergence between colonial and sparse populations

As discussed above, male traits and female mate choice
are highly complicated, which makes it difficult to pre-
dict the causes and consequences of given female mate
choice. Still, female preferences, particularly those for
direct benefits, depend on environmental conditions (or,
ecological factors: Safran et al. 2013), and thus a simple
testable prediction can be made as follows.

Among others, breeding habitat should affect female
choice in the barn swallow, particularly between colonial
and sparse populations (Fig. 5). In sparse, outdoor
populations where territory quality affects seasonal
reproductive success, female preference for territory
quality should be much more intense than in colonial
populations in livestock stalls in which nest predation
and interspecific brood parasitism are virtually absent
(see above: note that conspecific brood parasitism can
also be found in some populations which may select for
intense nest guarding: Turner 2006). In the former
populations, choosing attractive mates provides nothing
when they have low-quality territories (in which off-
spring will be predated), reducing female preference for
male attractiveness. By contrast, in colonial populations
in which nest predation is virtually absent, choosing
attractive mates produces high-quality offspring. Such
benefits of choosing attractive males should increase
with female preference for the trait through a runaway
process, particularly in dense colonial populations due
to the high frequency of extra-pair young (> 15% of
nestlings: reviewed in Table 5.1 in Turner 2006; see
Hasegawa et al. 2010a for sparse populations where
extra-pair paternity is virtually absent: < 3%), which
boosts sexual selection (e.g., eightfold compared to no
extra-pair paternity: Kleven et al. 2006). At the same
time, because courtship display at breeding sites is not
necessary for extrapair paternity (e.g., Hasegawa et al.
2016a; also see Turner 2006), total female preference
(and selection) for the traits displayed during courtship

(e.g., territory, enticement calls; see Fig. 1) should be
relatively weak in colonies.

Such a population difference in breeding environment
alone could explain the geographic variation in female
preferences and male phenotypes, because territory
quality, which is important in sparse populations but not
in colonies, is positively linked to male plumage col-
oration, but not to tail ornaments (Hasegawa et al. 2014;
Wilkins et al. 2015; note that nest predation pressure
also depends on local fauna; see above). In support of
this, Asian and North American subspecies, which are
less colonial than European subspecies (e.g., only 1%
breed in colonies in Japan; Ministry of Environment
1997; reviewed in Turner 2006, p. 101; though large
colonies can also be found in the former subspecies; e.g.,
Brown and Brown 1999), have intense selection for
colorful plumage rather than long tails (reviewed in
Romano et al. 2017a). These subspecies have shorter
tails and larger throat patches, which would be devel-
opmentally and functionally integrated to throat col-
oration, than European subspecies (where 47% breed in
colonies with 7–22 pairs; Turner 2006; Hasegawa et al.
2010a; Hasegawa and Arai 2013a). Such a pattern is also
found even within subspecies, because throat patch size
decreases and tail ornaments increase with latitude (i.e.,
a correlate of coloniality; Hasegawa and Arai 2013b). Of
course, colonial populations and outdoor populations
differ in many other ecological factors (Table 2) and
these additional factors may also contribute to the
population differences in female preferences and thus
male phenotype as well. For example, outdoor popula-
tions experience greater temperature cooling and fluc-
tuation relative to those nesting in warm livestock stalls
(Turner 2006; also see Löhrl and Gutscher 1973 for
subtle differences in reproductive performance between
warm and cold sites in European subspecies). Male
contribution to incubation (and thus males that incubate
more than others; e.g., short-tailed males: see Smith and
Montgomerie 1992; Møller 1994a, p. 247) might be more
important in outdoor populations than in colonial
populations, even if male incubation is inefficient (Voss
et al. 2008). In consistent with this perspective, male
share of incubation is higher in less-colonial subspecies
(Turner 2006) and outdoor populations than in colonial
populations within subspecies (Kojima et al. 2009; Ha-
segawa et al. 2012b), though there is no direct evidence
for now. Because coloniality varies widely even within
each region and is genetically determined at least in part
(e.g., see Møller 2002 for European subspecies), it might
be relevant to study how female preference changes with
population density (as Møller 2002 found decreased
aggressiveness with increasing population density; see
above).

This apparent match between the hypothetical sce-
nario and actual geographic variation does not deny the
importance of geographic variation in female preference
for each secondary sexual characteristic (e.g., plumage
coloration and tail length; Safran et al. 2016). Because
each ornament has its own information content, some of

11



which seems to be population-dependent (e.g., Vitousek
et al. 2016; also see above), female choice for each
ornament should itself depend on population. Never-
theless, consideration of female preference for male
traits other than secondary sexual characteristics would
advance our understanding of geographic variation in
female preference in a predictable manner (e.g., the
exaggeration of plumage coloration might have evolved
due to selection for males holding high-quality territory

in low-density sites; see above). Without considering it,
researchers may fail to detect or misunderstand the link
between ecological factors and sexual selection.

Concluding remarks and future directions

Although recent studies have reported geographic vari-
ation in female preference for male secondary sexual

(a)

(b)

Fig. 5 Hypothetical scenario of the relative importance of each
category of male traits (blue) and the female preference (pink),
denoted by the size of each node, in a sparse outdoor populations
and b dense colonial populations of barn swallows. Arrows
indicate (potential) mutual influences of nodes within each sex.
High breeding density, which increases extra-pair paternity, and
low nest predation favor female mate preference for traits

conferring indirect benefits in colonial populations, while low
breeding density and high nest predation favor female mate
preferences for traits conferring direct benefits (e.g., high-quality
territory). Note that female mate preference for resources results in
male–male contests favoring the exaggeration of some (but not all)
secondary sexual characteristics. Color figure online

12



characteristics, it remains unclear how such patterns
arose (Scordato and Safran 2014). Because female mate
preference covaries with ecological factors (e.g., nest
predation), future studies should consider ecological
factors causing such variation, rather than simply
detecting female mate choice and its geographic varia-
tion. In this sense, female mate preference for incon-
spicuous male characteristics such as territory quality
should be particularly important, because these charac-
teristics are highly dependent on ecological factors (Sa-
fran et al. 2013) and may be interrelated with female
mate preference for other traits such as secondary sexual
characteristics. In other words, the local environment
directly affects female preference for inconspicuous
traits, which may then affect male phenotype, including
secondary sexual characteristics, via intercorrelation of
male traits or those of female preference. Rather than
controlling habitat variability by using ideal study sys-
tems for efficient data collection (e.g., colonial breeders),
researchers need to take into account ecological factors
and its geographic variation to evaluate female mate
choice (and male–male contests; Hunt et al. 2009) and its
influence on overall male phenotype and other ecologi-
cal events (e.g., speciation) in this model species of fe-
male mate choice and in other species as well.

Acknowledgements This review is based on a presentation delivered
at the fourth Suzuki Award at the 63st Annual Meeting of the Eco-
logical Society of Japan, March 2016. I thank Dr Nobuyuki Kut-
sukake and his lab members at Sokendai (The Graduate University
for Advanced Studies) for their kindest advices. Particularly, Dr Emi
Arai gave me critical comments. MH was supported by the Research
Fellowship of the Japan Society for the Promotion of Science (JSPS,
15J10000). I thank Drs Yuichi Yamamura, Zhijun Ma, Atsushi
Kume, and the anonymous reviewers for their comments, which
helped to improve this manuscript. Open access funding provided by
the Ecological Society of Japan.

Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License
(http://creativecommons.org/licenses/by/4.0/), which permits un-
restricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original author(s) and
the source, provide a link to the Creative Commons license, and
indicate if changes were made.

References

Alatalo RV, Lundberg A, Glynn C (1986) Female pied flycatchers
choose territory quality and not male characteristics. Nature
323:152–153

Andersson M (1994) Sexual selection. Princeton Univ Press,
Princeton

Andersson S, Pryke SR, Ornborg J, Lawes MJ, Andersson M
(2002) Multiple receivers, multiple ornaments, and a trade-off
between agonistic and epigamic signaling in a widowbird. Am
Nat 160:683–691

Aparicio JM, Muñoz A, Bonal R, Møller AP (2012) Population
differences in density and resource allocation of ornamental tail
feathers in the barn swallow. Biol J Linn Soc 105:925–936

Arai E, Hasegawa M, Makino T, Hagino A, Sakai Y, Ohtsuki H,
Wakamatsu K, Kawata M (2017) Physiological conditions and
genetic controls of phaeomelanin pigmentation in nestling barn
swallows. Behav Ecol 28:706–716

Arnqvist G (2006) Sensory exploitation and sexual conflict. Phil
Trans R Soc Lond B 361:375–386

Balmford A, Thomas A (1992) Swallowing ornamental asymmetry.
Nature 359:487

Bańbura J (1986) Sexual dimorphism in wing and tail length as
shown by the swallow, Hirundo rustica. J Zool 210:131–136

Bradbury JW, Vehrencamp SL (1998) The principles of animal
communication. Sinauer, Sunderland

Bro-Jørgensen J (2010) Dynamics of multiple signaling systems:
animal communication in a world in flux. Trends Ecol Evol
25:292–300

Brooks RC, Griffith SC (2010) Mate choice. In: Westneat DF, Fox
CW (eds) Evolutionary behavioral ecology. Oxford Univ Press,
Oxford, pp 416–433

Brown CR, Brown MB (1999) Barn swallow (Hirundo rustica). In:
Rodewald PG (ed) The birds of North America. Cornell Lab of
Ornithology, Ithaca. https://birdsna.org/Species-Account/bna/
species/barswa. 10.2173/bna.452. Accessed 4 Nov 2017

Buchanan KL, Evans MR (2000) The effect of tail streamer length
on aerodynamic performance in the barn swallow. Behav Ecol
11:228–238

Burley N (1986) Sexual selection for aesthetic traits in species with
biparental care. Am Nat 127:415–445

Burley N (1988) The differential-allocation hypothesis: an experi-
mental test. Am Nat 132:611–628

Candolin U (2003) The use of multiple cues in mate choice. Biol
Rev 78:575–595

Christy JH (1995) Mimicry, mate choice, and the sensory trap
hypothesis. Am Nat 146:171–181

Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland
de Lope F, Møller AP (1993) Female reproductive effort depends

on the degree of ornamentation of their mates. Evolution
47:1152–1160

Dreiss AN, Navarro C, De Lope F, Møller AP (2008) Effects of an
immune challenge on multiple components of song display in
barn swallows Hirundo rustica: implications for sexual selection.
Ethology 114:955–964

Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melano-
cortin system, coloration and behavioural syndromes. Trends
Ecol Evol 23:502–510

Evans MR (1998) Selection on swallow tail streamers. Nature
394:233–234

Fedy BC, Martin TE (2009) Male songbirds provide indirect par-
ental care by guarding females during incubation. Behav Ecol
20:1034–1038

Fitzpatrick S (1998) Birds’ tails as signaling devices: markings,
shape, length, and feather quality. Am Nat 151:157–173

Table 2 Notable differences in ecological factors between colonial populations in livestock stalls and sparse outdoor populations

Colony Sparse Representative studies

Density High Low Turner (2006); Hasegawa et al. (2010b)
Extra-pair paternity High Low Turner (2006); Hasegawa et al. (2010b)
Nest predation Negligible Important Fujita (1993); Hasegawa et al. (2012a)
Territory quality Negligible Important Møller (1990); Hasegawa et al. (2012a)
Infanticide Young Young and Grown Turner (2006); Hasegawa and Arai (2015b)
Air temperature High Low Turner (2006)

13

http://creativecommons.org/licenses/by/4.0/
https://birdsna.org/Species-Account/bna/species/barswa
https://birdsna.org/Species-Account/bna/species/barswa


Fujita G (1993) Nest site selection and reproductive success in barn
swallows—preliminary report. Strix 12:35–39 (Japanese with
English summary)

Galeotti P, Saino N, Sacchi R, Møller AP (1997) Song correlates
with social context, testosterone and body condition in male
barn swallows. Anim Behav 53:687–700

Galván I, Møller AP (2009) Different roles of natural and sexual
selection on senescence of plumage colour in the Barn Swallow.
Funct Ecol 23:302–309

Galván I, Møller AP (2013) Pheomelanin-based plumage col-
oration predicts survival rates in birds. Physiol Biochem Zool
86:184–192

Garamszegi LZ, Møller AP (2004) Extrapair paternity and the
evolution of bird song. Behav Ecol 15:508–519

Garamszegi LZ, Heylen D, Møller AP, Eens M, de Lope F (2005)
Age-dependent health status and song characteristics in the
barn swallow. Behav Ecol 16:580–591

Garamszegi LZ, Hegyi G, Heylen D, Ninni P, de Lope F, Eens M,
Møller AP (2006) The design of complex sexual traits in male
barn swallows: associations between signal attributes. J Evol
Biol 19:2052–2066

Hasegawa M (2011) Sexual selection on multiple ornaments in barn
swallows. PhD Dissertation, University of Tsukuba

Hasegawa M, Arai E (2013a) Differential female access to males
with large throat patches in the Asian barn swallow Hirundo
rustica gutturalis. Zool Sci 30:913–918

Hasegawa M, Arai E (2013b) Divergent tail and throat ornamen-
tation in the barn swallow across the Japanese islands. J Ethol
31:79–83

Hasegawa M, Arai E (2015a) Experimentally reduced male orna-
mentation increased paternal care in the barn swallow. J Or-
nithol 156:795–804

Hasegawa M, Arai E (2015b) Infanticide on a grown nestling in a
sparse population of Japanese barn swallows Hirundo rustica
gutturalis. Wilson J Ornithol 127:524–528

Hasegawa M, Arai E (2016) Female attraction to higher-pitched
male enticement calls in barn swallows. Ethology 122:430–441

Hasegawa M, AraiE (2017a)Egg sizedecreaseswithincreasingfemale
tail fork depth in family Hirundinidae. Evol Ecol 31:559–569

Hasegawa M, Arai E (2017b) Negatively interplay of tail and throat
ornamentation in male barn swallows. Behaviour 154:835–851

Hasegawa M, Arai E, Watanabe M, Nakamura M (2010a) Mating
advantage of multiple male ornaments in the barn swallow
Hirundo rustica gutturalis. Ornithol Sci 9:141–148

Hasegawa M, Arai E, Kojima W, Kitamura W, Fujita G, Higuchi
H, Watanabe M, Nakamura M (2010b) Low level of extra-pair
paternity in a population of the barn swallow Hirundo rustica
gutturalis. Ornithol Sci 9:161–164

Hasegawa M, Arai E, Watanabe M, Nakamura M (2012a) Female
mate choice based on territory quality in barn swallows. J Ethol
30:143–150

Hasegawa M, Arai E, Watanabe M, Nakamura M (2012b) High
incubation investment of females paired to attractive males in
barn swallows. Ornithol Sci 11:1–8

Hasegawa M, Arai E, Watanabe M, Nakamura M (2013) Male
nestling-like courtship calls attract female barn swallows Hir-
undo rustica gutturalis. Anim Behav 86:949–953

Hasegawa M, Arai E, Watanabe M, Nakamura M (2014)
Colourful males hold high quality territories but exhibit re-
duced paternal care in barn swallows. Behaviour 151:591–612

Hasegawa M, Watanabe M, Nakamura M (2016a) Promiscuous
copulation attempts and discriminate pairing displays in male
barn swallows as revealed by model presentation. Ethol Ecol
Evol 28:163–174

Hasegawa M, Arai E, Kutsukake N (2016b) Evolution of tail fork
depth in genus Hirundo. Ecol Evol 6:851–858

Hasegawa M, Arai E, Watanabe M, Nakamura M (2017) Repro-
ductive advantage of multiple female ornaments in the Asian
barn swallow Hirundo rustica gutturalis. J Ornithol 158:517–532

Hunt J, Breuker CJ, Sadowski JA, Moore AJ (2009) Male–male
competition, female mate choice and their interaction: deter-
mining total sexual selection. J Evol Biol 22:13–26

Johnstone RA (1994) Female preference for symmetrical males as a
by-product of selection for mate recognition. Nature
372:172–175

Jones D (1995) Sexual selection, physical attractiveness, and facial
neoteny: cross-cultural evidence and implications. Curr
Anthropol 36:723–748

Kleven O, Jacobsen F, Robertson RJ, Lifield JT (2005) Extrapair
mating between relatives in the barn swallow: a role for kin
selection? Biol Lett 1:389–392

Kleven O, Jacobsen F, Izadnegahdar R, Robertson RJ, Lifjeld JT
(2006) Male tail streamer length predicts fertilization success in
the North American barn swallow (Hirundo rustica erythro-
gaster). Behav Ecol Sociobiol 59:412–418

Kojima W, Kitamura W, Kitajima S, Ito Y, Ueda K, Fujita G, Hi-
guchi H (2009) Female barn swallows gain indirect but not direct
benefits through social mate choice. Ethology 115:939–947

Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution
of mate choice and mating biases. Proc R Soc Lond B
270:653–664

Kose M, Møller AP (1999) Sexual selection, feather breakage and
parasites: the importance of white spots in the tail of the barn
swallow. Behav Ecol Sociobiol 45:430–436

Kose M, Mänd R, Møller AP (1999) Sexual selection for white tail
spots in the barn swallow in relation to habitat choice by feather
lice. Anim Behav 58:1201–1205

Liang W, Yang C, Wang L, Møller AP (2013) Avoiding parasitism
by breeding indoors: cuckoo parasitism of hirundines and
rejection of eggs. Behav Ecol Sociobiol 67:913–918

Lifjeld JT, Kleven O, Jacobesen F, McGraw KJ, Safran RJ,
Robertson RJ (2011) Age before beauty? Relationships between
fertilization success and age-dependent ornaments in barn
swallows. Behav Ecol Sociobiol 65:1687–1697

Löhrl VH, Gutscher H (1973) Zur Brutökologie der Rauch-
schwalbe (Hirundo rustica) in einem südwestdeutschen Dorf.
J Ornithol 114:399–416 (In Germany with English summary)

Maguire SE, Safran RJ (2010) Morphological and genetic predic-
tors of parental care in the North American barn swallow
Hirundo rustica erythrogaster. J Avian Biol 41:74–82

Ministry of Environment (1997) http://www.biodic.go.jp/reports/
5-4/p000.html. Accessed 4 Nov 2017

Møller AP (1987) Extent and duration of mate guarding in swal-
lows Hirundo rustica. Ornis Scand 18:95–100

Møller AP (1988) Female choice selects for male sexual tail orna-
ments in the monogamous swallow. Nature 332:640–642

Møller AP (1990) Male tail length and female mate choice in the
monogamous swallow Hirundo rustica. Anim Behav 39:458–465

Møller AP (1991a) Parasite load reduces song output in a passerine
bird. Anim Behav 41:723–730

Møller AP (1991b) Density-dependent extra-pair copulations in the
swallow Hirundo rustica. Ethology 87:316–329

Møller AP (1992a) Female swallow preference for symmetrical
male sex ornaments. Nature 357:238–240

Møller AP (1992b) Sexual selection in the monogamous barn
swallow (Hirundo rustica) II. Mechanisms of sexual selection.
J Evol Biol 5:603–624

Møller AP (1993a) Morphology and sexual selection in the barn
swallow Hirundo rustica in Chernobyl, Ukraine. Proc R Soc
Lond B 252:51–57

Møller AP (1993b) Female preference for apparently symmetrical
male sexual ornaments in the barn swallow Hirundo rustica.
Behav Ecol Sociobiol 32:371–376

Møller AP (1994a) Sexual selection and the barn swallow. Oxford
Univ Press, Oxford

Møller AP (1994b) Sexual selection in the barn swallow (Hirundo
rustica). IV. Patterns of fluctuating asymmetry and selection
against asymmetry. Evolution 48:658–670

Møller AP (1994c) Phenotype-dependent arrival time and its con-
sequences in a migratory bird. Behav Ecol Sociobiol 35:115–122

Møller AP (2001) Sexual selection in the barn swallow. In: Dugakin
LA (ed) Model systems in behavioral ecology: integrating
conceptual, theoretical, and empirical approaches. Princeton
Univ Press, Princeton, pp 359–377

14

http://www.biodic.go.jp/reports/5-4/p000.html
http://www.biodic.go.jp/reports/5-4/p000.html


Møller AP (2002) Parent–offspring resemblance in degree of
sociality in a passerine bird. Behav Ecol Sociobiol 51:276–281

Møller AP (2006) Rapid change in nest size of a bird related to
change in a secondary sexual character. Behav Ecol 17:108–116

Møller AP (2010) The fitness benefit of association with humans:
elevated success of bird breeding indoors. Behav Ecol
21:913–918

Møller AP (2017) Experimental manipulation of size and shape of
tail spots and sexual selection in barn swallows. Curr Zool
63:569–572

Møller AP, Jennions MD (2001) How important are direct fitness
benefits of sexual selection? Naturwissenschaften 88:401–415

Møller AP, Ninni P (1998) Sperm competition and sexual selection:
a meta-analysis of paternity studies of birds. Behav Ecol
Sociobiol 43:345–358

Møller AP, Pomiankowski A (1993) Why have birds got multiple
sexual ornaments? Behav Ecol Sociobiol 32:167–176

Møller AP, Thornhill R (1998) Male parental care, differential
parental investment by females and sexual selection. Anim
Behav 55:1507–1515

Møller AP, Barbosa A, Cuervo JJ, de Lope F, Merino S, Saino N
(1998a) Sexual selection and tail streamers in the barn swallow.
Proc R Soc Lond B 264:409–414

Møller AP, Saino N, Taramino G, Galeotti P, Ferrario S (1998b)
Paternity and multiple signaling: effects of a secondary sexual
character and song on paternity in the barn swallow. Am Nat
151:236–242

Møller AP, Brohede J, Cuervo JJ, de Lope F, Primmer C (2003)
Extrapair paternity in relation to sexual ornamentation, arrival
date and condition in a migratory bird. Behav Ecol 14:707–712

Møller AP, Chabi Y, Cuervo JJ, De Lope F, Kilpimaa J, Kose M,
Matyjasiak P, Pap PL, Saino N, Sakraoui R, Schifferli L, von
Hirschheydt J (2006) An analysis of continent-wide patterns of
sexual selection in a passerine bird. Evolution 60:856–868

Ninni P (2003) Carotenoid Signals in Barn Swallows. PhD thesis,
Université Pierre et Marie Curie, Paris, France

Norberg RA (1994) Swallow tail streamer is a mechanical device
for self deflection of tail leading edge, enhancing aerodynamic
efficiency and flight manoeuvrability. Proc R Soc Lond B
257:227–233

Pap PL, Osváth G, Aparicio JM, Bărbos L, Matyjasiak P, Rubolini
D, Saino N, Vágási CI, Vincze O, Møller AP (2015) Sexual
dimorphism and population differences in structural properties
of barn swallow (Hirundo rustica) wing and tail feathers. PLoS
ONE 10:e0130844

Patricelli GL, Coleman SW, Borgia G (2006) Male satin bower-
birds, Ptilonorhynchus violaceus, adjust their display intensity in
response to female startling: an experiment with robotic fe-
males. Anim Behav 71:49–59

Perrier G, de Lope F, Møller AP, Ninni P (2002) Structural col-
oration and sexual selection in the barn swallow Hirundo rus-
tica. Behav Ecol 13:728–736

Ringhofer M, Hasegawa T (2014) Social cues are preferred over
resource cues for breeding-site selection in barn swallows.
J Ornithol 155:531–538

Romano A, Rubolini D, Ambrosini R, Saino N (2014) Early
exposure to a bacterial endotoxin may cause breeding failure in
a migratory bird. Ethol Ecol Evol 26:80–85

Romano A, Constanzo A, Rubolini D, Saino N, Møller AP
(2017a) Geographical and seasonal variation in the intensity of
sexual selection in the barn swallow Hirundo rustica: a meta-
analysis. Biol Rev 92:1582–1600

Romano A, Saino N, Møller AP (2017b) Viability and expression
of sexual ornaments in the barn swallow Hirundo rustica: a
meta-analysis. J Evol Biol. https://doi.org/10.1111/jeb.13151 (in
press)

Roulin A (2016) Condition-dependence, pleiotropy and the hand-
icap principle of sexual selection in melanin-based colouration.
Biol Rev 91:328–348

Rowe LV, Evans MR, Buchanan KL (2001) The function and
evolution of the tail streamer in hirundines. Behav Ecol
12:157–163

Safran RJ (2004) Adaptive site selection rules and variation in
group size of barn swallows: individual decisions predict pop-
ulation patterns. Am Nat 164:121–131

Safran RJ (2007) Settlement patterns of female barn swallows
Hirundo rustica across different group sizes: access to colorful
males or favored nests? Behav Ecol Sociobiol 61:1359–1368

Safran RJ, McGraw KJ (2004) Plumage coloration, not length or
symmetry of tail-streamers, is a sexually selected trait in North
American barn swallows. Behav Ecol 15:455–461

Safran RJ, Neuman CR, McGraw KJ, Lovette IJ (2005) Dynamic
paternity allocation as a function of male plumage color in barn
swallows. Science 309:2210–2212

Safran RJ, Adelman JS, McGraw KJ, Hau M (2008) Sexual signal
exaggeration affects physiological state in male barn swallows.
Curr Biol 18:R461–R462

Safran RJ, Scordato ESC, Symes LB, Rodrı́guez RL, Mendelson
TC (2013) Contributions of natural and sexual selection to the
evolution of premating reproductive isolation: a research
agenda. Trends Ecol Evol 28:643–650

Safran RJ, Vortman Y, Jenkins BR, Hubbard JK, Wilkins MR,
Bradley RJ, Lotem A (2016) The maintenance of phenotypic
divergence through sexual selection: an experimental study in
barn swallows Hirundo rustica. Evolution 70:2074–2084

Saino N, Møller AP (1995) Testosterone-induced depression of
male parental behavior in the barn swallow: female compen-
sation and effects on seasonal fitness. Behav Ecol Sociobiol
36:151–157

Saino N, Galeotti P, Sacchi R, Møller AP (1997a) Song and
immunological condition in male barn swallows (Hirundo rus-
tica). Behav Ecol 8:364–371

Saino N, Primmer CR, Ellegren H, Møller AP (1997b) An exper-
imental study of paternity and tail ornamentation in the barn
swallow (Hirundo rustica). Evolution 51:562–570

Saino N, Primmer CR, Ellegren H, Møller AP (1999) Breeding
synchrony and paternity in the barn swallow (Hirundo rustica).
Behav Ecol Sociobiol 45:211–218

Saino N, Romano M, Sacchi R, Ninni P, Galeotti P, Møller AP
(2003) Do male barn swallows (Hirundo rustica) experience a
trade-off between the expression of multiple sexual signals?
Behav Ecol Sociobiol 54:465–471

Saino N, Romano M, Rubolini D, Ambrosini R, Caprioli M,
Milzani A, Costanzo A, Colombo G, Canova L, Wakamatsu K
(2013) Viability is associated with melanin-based coloration in
the barn swallow (Hirundo rustica). PLoS ONE 8:e60426.
https://doi.org/10.1371/journal.pone.0060426

Saino N, Romano M, Romano A, Rubolini D, Ambrosini R,
Caprioli M, Parolini M, Scandolara C, Bazzi G, Costanzo A
(2015) White tail spots in breeding barn swallows Hirundo rustica
signal body condition during winter moult. Ibis 157:722–730

Schluter D, Price T (1993) Honesty, perception and population
divergence in sexually selected traits. Proc R Soc Lond B
253:117–122

Scordato ES, Safran RJ (2014) Geographic variation in sexual
selection and implications for speciation in the Barn Swallow.
Avian Res 5:1–13

Sheldon BC (2000) Differential allocation: tests, mechanisms and
implications. Trends Ecol Evol 15:397–402

Slagsvold T (1986) Nest site settlement by the pied flycatcher: does
the female choose her mate for the quality of his house or
himself? Ornis Scand 17:210–220

Smith HG, Montgomerie R (1991) Sexual selection and the tail
ornaments of North American barn swallows. Behav Ecol
Sociobiol 28:195–201

Smith HG, Montgomerie R (1992) Male incubation in barn swal-
lows: the influence of nest temperature and sexual selection.
Condor 94:750–759

Soler JJ, Cuervo JJ, Møller AP, De Lope F (1998) Nest building is
a sexually selected behaviour in the barn swallow. Anim Behav
56:1435–1442

Soler JJ, Martı́n-Vivaldi M, Haussy C, Møller AP (2007) Intra- and
interspecific relationships between nest size and immunity. Be-
hav Ecol 18:781–791

15

https://doi.org/10.1111/jeb.13151
https://doi.org/10.1371/journal.pone.0060426


Stearns SC (1992) The evolution of life-histories. Oxford Univ
Press, Oxford

Su T, Huo J, Yang C, Liang W (2017) Brood parasitism on barn
swallow (Hirundo rustica) populations in China by common
cuckoo (Cuculus canorus). Chin J Zool 52:338–341 (In Chinese
with English summary)

Tazzyman SJ, Iwasa Y, Pomiankowski A (2014) Signaling efficacy
drives the evolution of larger sexual ornaments by sexual
selection. Evolution 68:216–229

Thomas ALR (1993) On the aerodynamics of birds’ tails. Phil
Trans R Soc Lond B 340:361–380

Turner AK (2006) The barn swallow. T & AD Poyser, London
van Doorn GS, Weissing FJ (2004) The evolution of female pref-

erences for multiple indicators of quality. Am Nat 164:173–186
van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of

resources: their influence on variation in life history tactics. Am
Nat 128:137–142

Vitousek MN, Tomášek O, Albrecht T, Wilkins MR, Safran RJ
(2016) Signal traits and oxidative stress: a comparative study
across populations with divergent signals. Front Ecol Evol 4:56

Vortman Y, Lottem A, Dor R, Lovette IJ, Safran RJ (2011) The
sexual signals of the East-Mediterranean barn swallow: a dif-
ferent swallow tale. Behav Ecol 22:1344–1352

Vortman Y, Lotem A, Dor R, Lovette I, Safran RJ (2013) Multiple
sexual signals and behavioral reproductive isolation in a
diverging population. Am Nat 182:514–523

Vortman Y, Safran RJ, Brodetzki TR, Dor R, Lotem A (2015)
Expression of multiple sexual signals by fathers and sons in the
East-Mediterranean barn swallow: are advertising strategies
heritable? PLoS ONE 10:e0118054

Voss MA, Rutter MA, Zimmerman NG, Moll KM (2008) Adap-
tive value of thermally inefficient male incubation in barn
swallows (Hirundo rustica). Auk 125:637–642

Wagner WE Jr, Beckers OM, Tolle AE, Basolo AL (2012) Trade-
offs limit the evolution of male traits that are attractive to fe-
males. Proc R Soc Lond B 279:2899–2906

Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds:
causes, correlates, and conflict. Annu Rev Ecol Evol Syst
34:265–396

Wiley RH, Poston J (1996) Indirect mate choice, competition for
mates, and coevolution of the sexes. Evolution 50:1371–1381

Wilkins MR, Shizuka D, Joseph MB, Hubbard HK, Safran RJ
(2015) Multimodal signalling in the North American barn
swallow: a phenotype network approach. Proc R Soc Lond B
282:20151574

Wilkins MR, Karaardiç H, Vortman Y, Parchman TL, Albrecht T,
Petrželková A, Özkan L, Pap PL, Hubbard JK, Hund AK,
Safran RJ (2016) Phenotypic differentiation is associated with
divergent sexual selection among closely related barn swallow
populations. J Evol Biol 29:2410–2421

Wong BBM, Candolin U (2005) How is female mate choice af-
fected by male competition? Biol Rev 80:559–571

16


	Beauty alone is insufficient: female mate choice in the barn swallow
	Abstract
	Introduction
	Male courtship displays
	Female mate choice criteria
	Secondary sexual characteristics
	Resources defended or provided by males
	Nestling-like traits
	Differences among the three categories

	Importance of inconspicuous male traits on overall phenotype
	Interrelationships among male traits
	Interrelationship among female mate preferences
	Divergence between colonial and sparse populations

	Concluding remarks and future directions
	Acknowledgements
	References