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Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations


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Spermatozoa vary greatly in size and shape among species across the animal kingdom. Postcopulatory sexual selection is thought to be the major evolutionary force driving this diversity. In contrast, less is known about how sperm size varies among populations of the same species. Here, we investigate geographic variation in sperm size in barn swallows Hirundo rustica, a socially monogamous passerine with a wide Holarctic breeding distribution. We included samples from seven populations and three subspecies: five populations of ssp. rustica in Europe (Czech, Italy, Norway, Spain, and Ukraine), one population of ssp. transitiva in Israel, and one population of ssp. erythrogaster in Canada. All sperm traits (head length, midpiece length, tail length, and total length) varied significantly among populations. The variation among the European rustica populations was much lower than the differences among subspecies, indicating that sperm traits reflect phylogenetic distance. We also performed a test of the relationship between the coefficient of between-male variation in total sperm length and extrapair paternity levels across different populations within a species. Recent studies have found a strong negative relationship between sperm size variation and extrapair paternity among species. Here, we show a similar negative relationship among six barn swallow populations, which suggests that the variance in male sperm length in a population is shaped by the strength of stabilizing postcopulatory sexual selection.
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Variation in sperm morphometry and sperm competition
among barn swallow (Hirundo rustica) populations
Terje Laskemoen &Tomas Albrecht &Andrea Bonisoli-Alquati &
Jaroslav Cepak &Florentino de Lope &Ignacio G. Hermosell &
Lars Erik Johannessen &Oddmund Kleven &Alfonso Marzal &
Timothy A. Mousseau &Anders P. Møller &
Raleigh J. Robertson &Geir Rudolfsen &
Nicola Saino &Yoni Vortman &Jan T. Lifjeld
Received: 7 September 2012 /Revised: 2 November 2012 / Accepted: 7 November 2012 / Published online: 18 November 2012
#Springer-Verlag Berlin Heidelberg 2012
Abstract Spermatozoa vary greatly in size and shape among
species across the animal kingdom. Postcopulatory sexual
selection is thought to be the major evolutionary force driving
this diversity. In contrast, less is known about how sperm size
varies among populations of the same species. Here, we
investigate geographic variation in sperm size in barn swal-
lows Hirundo rustica, a socially monogamous passerine with
a wide Holarctic breeding distribution. We included samples
Communicated by S. Pruett-Jones
Electronic supplementary material The online version of this article
(doi:10.1007/s00265-012-1450-0) contains supplementary material,
which is available to authorized users.
T. Laskemoen (*):L. E. Johannessen :O. Kleven :J. T. Lifjeld
Natural History Museum, University of Oslo,
P.O. Box 1172(Blindern, 0318 Oslo, Norway
T. Albrecht
Institute of Vertebrate Biology, v.v.i., Academy of Sciences of the
Czech Republic, Brno, Czech Republic
T. Albrecht
Department of Zoology, Faculty of Science, Charles University in
Prague, Prague, Czech Republic
A. Bonisoli-Alquati :T. A. Mousseau
Department of Biological Sciences, University of South Carolina,
Columbia, SC, 29208, USA
J. Cepak
Bird-ringing Station, National Museum, Prague,
Czech Republic
F. de Lope :I. G. Hermosell :A. Marzal
Departamento de Anatomia, Biologia Celular y Zoologia,
Universidad de Extremadura, Badajoz, Spain
O. Kleven
Norwegian Institute for Nature Research-NINA,
P. O. Box 5685(Sluppen, 7485 Trondheim, Norway
A. P. Møller
Laboratoire dEcologie, Systématique et Evolution, CNRS UMR
8079, Université Paris-Sud,
Orsay Cedex, France
R. J. Robertson
Department of Biology, Queens University, Kingston,
Ontario, K7L 3N6, Canada
G. Rudolfsen
Department for Environmental Radioactivity, Norwegian
Radiation Protection Authority, Fram Center,
9296 Tromsø, Norway
N. Saino
Dipartimento di Biologia, Universita degli Studi di Milano,
via Celoria 26,
20133 Milano, Italy
Y. Vortman
Department of Zoology, Faculty of Life Sciences,
Tel-Aviv University,
Ramat Aviv, Tel-Aviv, 69978, Israel
Behav Ecol Sociobiol (2013) 67:301309
DOI 10.1007/s00265-012-1450-0
from seven populations and three subspecies: five populations
of ssp. rustica in Europe (Czech, Italy, Norway, Spain, and
Ukraine), one population of ssp. transitiva in Israel, and one
population of ssp. erythrogaster in Canada. All sperm traits
(head length, midpiece length, tail length, and total length)
varied significantly among populations. The variation among
the European rustica populations was much lower than the
differences among subspecies, indicating that sperm traits
reflect phylogenetic distance. We also performed a test of
the relationship between the coefficient of between-male var-
iation in total sperm length and extrapair paternity levels
across different populations within a species. Recent studies
have found a strong negative relationship between sperm size
variation and extrapair paternity among species. Here, we
show a similar negative relationship among six barn swallow
populations, which suggests that the variance in male sperm
length in a population is shaped by the strength of stabilizing
postcopulatory sexual selection.
Keywords Barn swallow .Extrapair paternity .Hirundo
rustica .Sperm competition .Sperm size
Spermatozoa show enormous variation in size and shape
across animal taxa (e.g., Cohen 1977). The evolutionary
forces shaping this variation have received increasing atten-
tion but are not fully understood (Birkhead et al. 2009).
Polyandry, i.e., females mating with more than one male,
is common across the animal kingdom, and this constitutes a
potentially powerful source of postcopulatory sexual selec-
tion on sperm traits, either through sperm competition
(Parker 1970) or cryptic female choice (Eberhard 1996).
It is well documented that spermatozoa vary considerably
in size both within (e.g., Ward 1998; Morrow and Gage
2001b; Laskemoen et al. 2007) and among species (e.g.,
Gage 1998; Calhim et al. 2007; Kleven et al. 2008; Lüpold
et al. 2009). Although geographical variation in sperm size
within species has been studied in a range of species, the
patterns are complex and not clear. For example, in guppies
(Poecilia reticulata), Elgee et al. (2010) found that males
from populations with high risk of predation had faster
swimming sperm and sperm with longer midpieces than
males from populations with lower risk of predation.
However, total sperm length did not differ between guppy
populations (Elgee et al. 2010). Studies of several droso-
philid flies have found significant variation in sperm size
among populations (Snook 2001; Pitnick et al. 2003; Joly et
al. 2004). Yellow dung flies (Scatophaga stercoraria) have
been shown to have longer sperm at high temperature when
raised experimentally in laboratory conditions (Blanckenhorn
and Hellriegel 2002). However, another study of the same
species did not find differences in sperm length in three natural
populations (Hosken et al. 2003). A comparative study of
sperm morphology of rhacophorid frogs included samples of
the species (Chirixalus eiffingeri) from both Japan and Taiwan
and documented significant differences in sperm size between
these two populations (Kuramoto 1996). A study of quacking
frogs (Crinia georgiana) documented significant variation in
sperm size and relative number of sperm among four popula-
tions (Hettyey and Roberts 2006). The sea urchin
(Strongylocentrotus droebachiensis) was found to have high
diversity in sperm traits, except total sperm length, among
three different populations (Manier and Palumbi 2008).
Minoretti and Baur (2006) documented significant differences
in sperm size among four populations of the land snail
(Arianta arbustorum). In birds, two recent studies have inves-
tigated geographic variation in sperm size, both documenting
significant differences among populations (Lüpold et al. 2011;
Schmoll and Kleven 2011 ). In red-winged blackbirds
(Agelaius phoeniceus), sperm morphology varied significant-
ly among the 17 study sites in continental United States
(Lüpold et al. 2011). Lüpold et al. (2011) also found a gradual
increase in sperm size from southwest to northeast of the
breeding range, and further, a negative relationship between
sperm length and body size. Schmoll and Kleven (2011)
investigated variation in sperm size within and between two
populations of coal tits (Periparus ater) and documented
significant variation in total sperm length and sperm head
length between the two populations. These two species are
characterized by little or moderate gene flow, which could
help explain geographical differences in sperm traits with high
heritability. A call is thus made for investigation of variation in
sperm size among populations in species with a higher degree
of gene flow among populations.
Recently, comparative studies of passerine birds have
shown that the intraspecific variation in total sperm length
and other sperm components are negatively associated with
the risk of sperm competition (Calhim et al. 2007; Immler et
al. 2008; Kleven et al. 2008; Lifjeld et al. 2010). This can be
interpreted as evidence of stronger stabilizing selection on
males producing an optimal sperm type when the risk of
sperm competition increases. However, this relationship has
not been investigated among populations of the same spe-
cies. It is well known that levels of extrapair paternity vary
among populations (Petrie and Kempenaers 1998), and in
this study, we ask if this variation amongst populations in
sperm competition could also be reflected in between-male
variation in sperm size.
The barn swallow (Hirundo rustica) is a socially monog-
amous passerine with a broad Holarctic breeding distribu-
tion (Møller 1994b; Turner 2006). The barn swallow has
been thoroughly studied over the last decades and is con-
sidered a model species for studies on sexual selection, mate
choice, and sperm competition (e.g., Møller 1988; Møller
302 Behav Ecol Sociobiol (2013) 67:301309
1994a; Møller 1994b; Saino et al. 1997; Safran et al. 2005;
Kleven et al. 2006; Lifjeld et al. 2011). Currently, six dif-
ferent subspecies of barn swallows are recognized (Turner
2006; Dor et al. 2010). However, some of these subspecies
are geographically isolated, preventing gene flow (Turner
2006). A recent phylogeny of barn swallows and other
Hirundo species found that the European H. rustica rustica
and East-Mediterranean barn swallows H.rustica transitiva
cluster together, as do the Asian and American barn swal-
lows (Dor et al. 2010). Dor et al. (2010) also reported
pairwise molecular distances within and between these
clades, showing low distance within the European-
Mediterranean clade and substantially greater distance be-
tween the Asian-American and the European-Mediterranean
clades. Furthermore, there is evidence from barcoding of the
mitochondrial cytochrome c oxidase I (CO1) gene showing
that the North American barn swallow H. rustica eryth-
rogaster differs almost 2 % in genetic distance from the
European barn swallow (Johnsen et al. 2010).
Here, we investigate geographic variation in sperm mor-
phometry in barn swallows. We examined sperm morphome-
try in seven different barn swallow populations representing
three subspecies: five populations of European (Czech, Italy,
Norway, Spain and Ukraine), one population of East-
Mediterranean (Israel), and one North American population
(Canada). Based on the prior knowledge of genetic variation
(Dor et al. 2010; Johnsen et al. 2010), we predicted that
European and Mediterranean barn swallows would exhibit
more similar sperm morphometry when compared to North
American barn swallows. We also tested the hypothesis that
sperm size variation is negatively related to the risk of sperm
competition across populations.
Field procedures
We captured and sampled male barn swallows from seven
different populations; Czech Republic (2009), Italy (2011),
Norway (2008 and 2009), Spain (2010 and 2011), Ukraine
(2010), Israel (2010 and 2011), and Canada (2006). See
supplementary Table S1 for detailed sampling location infor-
mation. Notably, European barnswallows migrate through the
breeding areas of East-Mediterranean barn swallows in Israel,
which could potentially cause sampling errors in this area.
However, all birds sampled in Israel were earlier banded and
belonged to a monitored population of East-Mediterranean
barn swallows. To prevent pseudo-replication of already sam-
pled birds, all unbanded birds were banded with unique alu-
minium bands.We obtained ejaculate samples either by gently
massaging the males' cloacal protuberance following a mod-
ified method from Wolfson (1952) or from fecal samples
following Immler and Birkhead (2005). The ejaculate or fecal
sample was immediately fixed in a 5 % formalin solution and
stored until slide preparation. After sampling, all birds were
released in the immediate vicinity of their respective colonies.
Sperm morphometry
For each sperm sample, a small aliquot of approximately
15 μl was applied on a microscope slide, allowed to air-dry,
and subsequently gently rinsed with distilled water and air-
dried again. We measured the head, midpiece, and tail
(±0.1 μm) of ten intact spermatozoa per male. Measuring
ten sperms per male has been shown to give representative
estimations of an individual's mean sperm length
(Laskemoen et al. 2007). Total length is the sum of all three
separate sperm traits. For one individual, we measured the
same ten sperms twice to establish the repeatability of our
measurements, following Lessells and Boag (1987). The
measurements were highly repeatable (head: F
P00.003, r00.74; midpiece: F
0114.0, P<0.001, r0
0.98; tail: F
0105.8, P<0.001, r00.98). For the samples
of North American barn swallows, we used a Zeiss
AxioCam HRc camera mounted on a Zeiss Axioplan 2 light
microscope to obtain digital images of spermatozoa at a
magnification of 200×. Further, the morphometric measure-
ments were conducted using the software Zeiss AxioVision
4.1 (© Carl Zeiss Vision GmbH, Germany). For all other
samples, we used a Leica DFC420 camera mounted on a
Leica DM6000 B digital light microscope to obtain digital
images at magnifications of 200×. The morphometric meas-
urements were conducted using Leica Application Suite
(version 2.6.0 R1). The use of two different microscope
setups could potentially cause artificial differences. In order
to establish whether the different microscope systems gave
different results, we measured ten randomly chosen individ-
uals of the North American barn swallows on the Leica
microscope system as well. No significant differences were
observed (average head length, 14.3 vs. 14.3 μm; average
midpiece length, 59.8 vs. 59.9 μm; average tail length, 14.4
vs. 14.2 μm, Zeiss vs. Leica systems, respectively; paired t
tests: all t<0.57, all P>0.58). To avoid observer effects, one
person (TL) conducted all morphometric measurements. In
an earlier study of sperm characteristics of Ukrainian barn
swallows, Møller et al. (2008) found differences in both sperm
size and proportion of abnormal sperm between birds sampled
near the Chernobyl area and those sampled at control areas
southwest of Chernobyl. Therefore, we tested for differences
in sperm traits between the four Ukrainian localities in the
present dataset. We found no significant differences in any of
the measured sperm traits (ANOVA, all F
<1.46, all P>
0.25). Hence, we pooled all individuals from Ukraine as one
population. Notably, the Ukrainian samples included in the
present study are not the same as in Møller et al. (2008).
Behav Ecol Sociobiol (2013) 67:301309 303
Extrapair paternity data
We extracted data on extrapair paternity from five populations
from the literature (Canada, Italy, Israel, Spain, and Ukraine).
In addition, we obtained unpublished data on extrapair pater-
nity from the Czech population (T. Albrecht, J. Kreisinger, and
R. Michalkova unpublished data). Notably, all extrapair pa-
ternity data originate from the same populations from which
we obtained sperm samples. A summary of paternity data and
sample sizes are presented in Table 1.
Statistical analyses
We included all sperm measurements, i.e., ten sperms per
male, and used General Linear Mixed Models (GLMM) with
population as fixed factor and individual as random factor in
our tests for differences in sperm traits among populations.
For the traits that showed significant variation among popu-
lations, we estimated marginal means and conducted all pos-
sible pairwise comparisons, Bonferroni-adjusted for multiple
comparisons. We calculated the coefficient of variation in
sperm length between males (CV
) for all populations using
the formula: CV
0SD/mean×100. Furthermore, as the co-
efficient of variation for small sample sizes tends to be under-
estimated, weapplied the formula recommended by Sokal and
Rohlf (1995): CV
0CV×(1 + (1/4n)). Hence, all CV
ues reported here are adjusted for sample size. Statistical tests
were conducted using Statistica v7.1 (StatSoft Inc), SPSS
v19.0.0 (SPSS Inc.), and figures were drawn using Origin
v7.0300 (OriginLab Corporation).
Sperm morphometry
Sperm head length, midpiece length, and total length dif-
fered significantly among populations (GLMMs: head
length: F
6, 183
017.4, P<0.001; midpiece length: F
6, 183
15.9, P<0.001; total length: F
6, 183
010.3, P<0.001). Thus,
for these traits, we estimated marginal means and pair-
wise comparisons to reveal which populations differed
(Table S2S4). Descriptive statistics of sperm morphom-
etry from all seven populations are presented in Table 2.
Sperm tail length did not differ significantly among
populations (F
6, 183
02.0, P00.07 ). Generally, the
North American barn swallows differed most from the
other populations in sperm morphometry, with longer
sperm heads than individuals from all the other popula-
tions and shorter midpieces than all but the Italian and
East-Mediterranean populations (Fig. 1a, b;TableS2,
S3). Considering total sperm length, North American barn
swallows generally had shorter sperm than the European
populations but did not differ from the population of East-
Mediterranean barn swallows (Fig. 1c; Table S4).
Two of our populations (Norway and Spain) included
samples from two different seasons, and thus we tested for
potential year-effects on sperm size. However, we found no
significant effect of sample year on any of the sperm traits
measured (Norway: all F
<0.69, P>0.42; Spain: all F
<2.48, all P>0.14).
Among-male variation in sperm size and extrapair paternity
The populations showed somewhat different values of
among male variation in sperm size (CV
When examining the relationship between CV
percentage broods containing one or more extrapair
young (EPB), we found a significant negative relation-
ship (Pearson's: r00.96, N06, P00.003) (Fig. 2a). The
relationship between CV
and percentage extrapair
young (EPY) also went in the predicted negative direc-
tion, although this was not statistically significant
(Pearson's: r00.62, N06, P00.19) (Fig. 2b). Hence, both
tests were in the predicted direction with decreasing CV
Table 1 Summary of extrapair paternity data from six populations of barn swallows Hirundo rustica used in the present study
Country EPY (95 % CI)
Nyoung/Nbroods Source
Czech 23.1 (15.231.1) 60.0 108/25 (T. Albrecht, J. Kreisinger
and R. Michalkova
unpublished data)
Italy 29.0 (22.935.1) 52.0 214/52 (Saino et al. 1999)
Spain 17.8 (14.920.7) 32.4 674/170 (Møller et al. 2003)
Ukraine 30.0 (20.040.0) 50.0 80/18 (Ellegren et al. 1997)
Israel 15.3 (9.720.9) 43.9 161/41 (Vortman et al. 2011)
Canada 28.8 (25.931.7) 48.1 917/210 (Kleven et al. 2005)
Percentage extrapair young with the 95 % lower and upper confidence limits of the estimate indicated
Percentage broods containing one or more extrapair young
304 Behav Ecol Sociobiol (2013) 67:301309
being associated with increasing level of extrapair paternity
(Lifjeld et al. 2010).
Our analysis revealed significant differences in sperm mor-
phometry among barn swallow populations and subspecies.
North American barn swallows from Canada had signifi-
cantly shorter sperm than European barn swallows from
Czech, Norway, Spain, and Ukraine but did not differ sig-
nificantly from European barn swallows from Italy and
East-Mediterranean barn swallows from Israel. When exam-
ining the three different sperm traits included in our analyses
(head length, midpiece length, and tail length), North
American barn swallows were characterized by longer
sperm heads than all other populations and shorter midpie-
ces than all other populations except the East-Mediterranean
one. Further, we found that between male variation in sperm
length (CV
) was negatively related to levels of extrapair
paternity, both expressed as percentage broods contain-
ing extrapair young (EPB) and percentage extrapair
young (EPY).
Based on the phylogenetic relationships between the
three subspecies of barn swallows included in our analyses
(Dor et al. 2010), we predicted that European and East-
Mediterranean barn swallows should be more similar to
each other in sperm morphometry compared to North
American barn swallows. Although our findings were not
clear, some of the sperm traits coincided with this predic-
tion, e.g., spermatozoa of North American barn swallows
had longer heads and shorter midpieces than all other pop-
ulations. Total sperm length showed a different pattern, with
European barn swallows having significantly longer sperm
than both East-Mediterranean and North American barn
swallows, whereas the two latter did not differ significantly
for this trait. Interestingly, sperm head size seems to be a
trait that often differs among populations. It was the most
variable sperm trait in the coal tit study (Schmoll and
Kleven 2011). Also, in a recent comparison of wild and
domesticated zebra finches (Taeniopygia guttata), sperm
head length showed the greatest difference between the
two groups (Immler et al. 2012). We do not know if genetic
drift or selection is causing the differentiation in sperm
morphometry among populations. Both factors can however
be important for differentiation in sperm morphometry and
are not mutually exclusive. Whereas the studies of coal tits
and red-winged blackbirds documented significant differen-
tiation in sperm size between relatively close populations
(Lüpold et al. 2011; Schmoll and Kleven 2011), this study
documented little differentiation in sperm size across the
five European barn swallow populations. Another study on
pied flycatchers (Ficedula hypoleuca) found a similar pat-
tern as the present study, with no difference in sperm size
between one German and two Norwegian populations
(Lifjeld et al. 2012). The discrepancy between the coal tit
and red-winged blackbird on one hand and the pied fly-
catcher and barn swallow studies on the other, might be
explained by differences in gene flow among populations.
Both coal tits and red-winged blackbirds are resident or
short distance migratory birds, whereas pied flycatchers
and barn swallows are long distance migrants with clear
differences in dispersal distance (Paradis et al. 1999).
Notably, the East-Mediterranean barn swallow is sedentary
but still is subject to high levels of gene flow supposedly
from migrating European barn swallows (Dor et al. 2012).
Thus, gene flow could be more prominent in the two latter
Notably, it has been shown in Gouldian finches
(Erythrura gouldiae) that males can exhibit plasticity in
Table 2 Descriptive statistics of sperm morphometry in seven populations of barn swallows Hirundo rustica (see supplementary Table S2S4 for
pairwise comparisons between all populations)
Head length (μm) Midpiece length (μm) Tail length (μm) Total length (μm) CV
Mean± SD Range Mean± SD Range Mean± SD Range Mean± SD Range
Czech (n020) 13.1±0.5 11.713.9 62.2 ±2.8 57.366.9 14.7± 2.2 9.718.7 89.9 ± 2.1 86.494.2 2.34 1.52
Italy (n08) 13.0± 0.3 12.613.4 64.4 ± 1.3 62.966.4 13.0±2.6 10.218.7 90.3 ± 2.2 88.094.8 2.54 1.65
Norway (n026) 13.2± 0.5 12.114.2 61.6 ± 3.1 54.265.9 15.8±3.4 11.625.6 90.6 ± 2.4 86.494.6 2.63 1.67
Spain (n013) 13.4± 0.5 12.814.6 62.5 ±2.5 58.366.0 15.0± 2.2 11.520.3 91.0±2.9 85.396.9 3.29 1.66
Ukraine (n025) 13.2± 0.4 12.214.2 62.6 ± 2.3 57.766.6 15.4±2.9 11.024.5 91.2 ± 2.5 86.296.8 2.76 1.92
Israel (n08) 13.2± 0.6 12.414.0 61.7 ± 2.9 57.566.0 13.6±1.2 11.515.5 88.5 ± 2.8 84.392.2 3.13 2.24
Canada (n090) 14.0± 0.7 12.515.5 59.0 ± 2.1 52.363.3 14.8±2.1 10.220.1 87.9 ± 2.5 81.493.0 2.82 1.74
Coefficient of variation of total sperm length calculated as SD/mean*100 and adjusted for sample size following the formula (CV*(1 +(1/4n)))
(Sokal and Rohlf 1995)
Average coefficient of variation of total sperm length within males, based on ten sperms per male
Behav Ecol Sociobiol (2013) 67:301309 305
sperm morphometry within the same breeding season when
the social environment is altered (Immler et al. 2010). Males
were found to increase the relative size of the sperm mid-
piece when placed in intermediate to high competitive envi-
ronments and increase the size of the sperm tail when facing
Fig 1 Sperm ahead, bmidpiece, and ctotal length, in seven popula-
tions of barn swallows Hirundo rustica. Average values are indicated
as small squares,boxes indicate ±SE, and whiskers indicate ±95 %
confidence intervals. Sample sizes are; Czech n020 males, Italy n0
8males,Norwayn026 males, Spain n013 males, Ukraine n025
males, Israel n08 males, and Canada n090 males. See Results
section for test statistics
Fig 2 Relationship between apercentage broods containing extrapair
young and coefficient of variation (adjusted for sample size) (CV
) in
sperm length between males and bpercentage extrapair young and
, in six populations of barn swallows. Numbers represent the
following populations; (1) Czech, (2) Italy, (3) Ukraine, (4) Canada, (5)
Israel, and (6) Spain. See Resultssection for test statistics
306 Behav Ecol Sociobiol (2013) 67:301309
low to intermediate competitive environments (Immler et al.
2010). This could imply that the relative size of the sperm
midpiece and tail could change across the breeding season
in barn swallows as well. Similarly, a recent study of sperm
size variation in house wrens (Troglodytes aedon) found that
total sperm length was highly consistent across the breeding
season, whereas the flagellum:head length ratio increased
during the season, indicating phenotypic plasticity or adjust-
ment in the relative size of sperm components (Cramer et al.
2012). However, repeated samples across the breeding sea-
son of North American and Czech barn swallows have
shown very high repeatability of all sperm traits (own un-
published data).
Sperm head, midpiece, and flagellum length have been
shown to be heritable in the zebra finch (Birkhead et al.
2005) and in several other taxa (e.g. Ward 2000; Morrow
and Gage 2001a; Baer et al. 2006). Thus, plasticity in sperm
morphometry within the same breeding season might be
rather marginal and not biasing the population differences
reported here.
To the best of our knowledge, this is the first study
examining the relationship between sperm size variation
and extrapair paternity levels across populations within the
same species. A few studies have previously demonstrated
that this relationship is significantly negative in passerine
birds (Calhim et al. 2007; Kleven et al. 2008; Lifjeld et al.
2010). Recently, a similar negative relationship between
sperm size variation and polyandry has been demonstrated
in social insects (Fitzpatrick and Baer 2011). As extrapair
paternity levels are known to vary among populations of the
same species (e.g., Griffith et al. 2002), with barn swallows
being one of the species showing considerable variation
(Saino et al. 1999; Møller et al. 2003; Kleven et al. 2005;
Vortman et al. 2011), we tested associations between CV
and levels of extrapair paternity data across populations of this
species. Both EPB and EPY were negatively related to CV
as predicted from the aforementioned interspecific studies.
The relationship between CV
and EPY was, however, not
statistically significant. Although our sample size in the
present dataset is small, we argue that this indicates that
and risk of sperm competition are negatively related
also within species, further supporting the notion that risk of
sperm competition induces stabilizing selection on sperm size.
The present study shows little variation in sperm size/
morphometry among European and East-Mediterranean
barn swallows, and somewhat larger variation between
European-East-Mediterranean and North American barn
swallows. These results make sense in the light of the
genetic difference and the large geographic distance be-
tween populations. The subspecies rustica and transitiva
are genetically closely related (Dor et al. 2010), and they
do not differ much in sperm morphometry. The subspecies
erythrogaster is genetically quite distant from both rustica
and transitiva (Dor et al. 2010; Johnsen et al. 2010), and this
is also reflected in the observed sperm morphometry. In
conclusion, sperm morphometry might give an indication
of genetic distance, not only between species, but also
between phylogenetic lines within species. Further, we
found negative relationships between CV
and two meas-
ures of extrapair paternity, EPB and EPY, indicating that the
same pattern as have been found among species (Calhim et
al. 2007; Kleven et al. 2008; Lifjeld et al. 2010; Fitzpatrick
and Baer 2011), also is present intraspecifically, and which
strengthens the explanation that sperm competition exerts a
stabilizing selection pressure on sperm size variation.
Acknowledgments We are grateful to all people that assisted with
field work, especially Frode Fossøy in Canada, Bjørn Aksel Bjerke in
Norway, and Luz Garcia-Longoria in Spain. A special thanks to Gustav
Thorsø Mohr for allowing us to trap inside the barn at Thorsø
Herregård. We thank two anonymous reviewers for helpful comments
on an earlier draft of the manuscript. This study was supported by
funding from the Czech Science Foundation (to TA, project no.
P506/12/2472), a Fondazione Cariplo grant (to NS, grant no. 2009
3496), the Ministry of Culture of the Czech Republic (to JC, grant no.
DKRVO 00023272), the Natural Sciences and Engineering Research
Council of Canada (to RJR), the Norwegian Research Council (to JTL,
OK, LEJ and TL), the Samuel Freeman Charitable Trust (to TAM), and
the Spanish Ministry of Economy and Competitivness (to IGH, FdL and
AM, grant no. CGL 201236665).
Ethical standards All authors declare that the present study com-
plies with the current laws and ethical standards of animal research in
Canada, Czech Republic, Israel, Italy, Norway, Spain, and Ukraine.
Conflict of interest The authors declare that they have no conflict of
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... Second, we estimated the proportion of extrapair young from the coefficient of intermale variation in mean total sperm length (hereafter referred to as "sperm length CV"). This metric is strongly, negatively correlated with the proportion of extrapair young in passerine birds [49][50][51]. A similar relationship with sperm competition has also been documented in social insects [52] and rodents [53]. ...
... For the conversion of sperm length CV to the female promiscuity index, we refined the predictive fit of the regression model given in Lifjeld et al. [51] by selecting 24 species from the Passerides only, and from which we had paternity and sperm length data originating from the same study population (Additional file 4). Comparing data from the same study population is important to avoid noise in the model because extrapair paternity rates can vary geographically within a species [50,57] and population variance in mean sperm lengths can vary accordingly [50]. Population mean sperm lengths can also change geographically [58][59][60], which implies that pooling individuals from different populations can inflate the variance estimate. ...
... For the conversion of sperm length CV to the female promiscuity index, we refined the predictive fit of the regression model given in Lifjeld et al. [51] by selecting 24 species from the Passerides only, and from which we had paternity and sperm length data originating from the same study population (Additional file 4). Comparing data from the same study population is important to avoid noise in the model because extrapair paternity rates can vary geographically within a species [50,57] and population variance in mean sperm lengths can vary accordingly [50]. Population mean sperm lengths can also change geographically [58][59][60], which implies that pooling individuals from different populations can inflate the variance estimate. ...
Full-text available
Background: Female promiscuity is highly variable among birds, and particularly among songbirds. Comparative work has identified several patterns of covariation with social, sexual, ecological and life history traits. However, it is unclear whether these patterns reflect causes or consequences of female promiscuity, or if they are byproducts of some unknown evolutionary drivers. Moreover, factors that explain promiscuity at the deep nodes in the phylogenetic tree may be different from those important at the tips, i.e. among closely related species. Here we examine the relationships between female promiscuity and a broad set of predictor variables in a comprehensive data set (N = 202 species) of Passerides songbirds, which is a highly diversified infraorder of the Passeriformes exhibiting significant variation in female promiscuity. Results: Female promiscuity was highly variable in all major clades of the Passerides phylogeny and also among closely related species. We found several significant associations with female promiscuity, albeit with fairly small effect sizes (all R2 ≤ 0.08). More promiscuous species had: 1) less male parental care, particularly during the early stages of the nesting cycle (nest building and incubation), 2) more short-term pair bonds, 3) greater degree of sexual dichromatism, primarily because females were drabber, 4) more migratory behaviour, and 5) stronger pre-mating sexual selection. In a multivariate model, however, the effect of sexual selection disappeared, while the other four variables showed additive effects and together explained about 16% of the total variance in female promiscuity. Female promiscuity showed no relationship with body size, life history variation, latitude or cooperative breeding. Conclusions: We found that multiple traits were associated with female promiscuity, but these associations were generally weak. Some traits, such as reduced parental care in males and more cryptic plumage in females, might even be responses to, rather than causes of, variation in female promiscuity. Hence, the high variation in female promiscuity among Passerides species remains enigmatic. Female promiscuity seems to be a rapidly evolving trait that often diverges between species with similar ecologies and breeding systems. A future challenge is therefore to understand what drives within-lineage variation in female promiscuity over microevolutionary time scales.
... Only few studies, for example, have addressed such fundamental topics as geographical (e.g. Lüpold et al., 2011;Schmoll & Kleven, 2011;Lifjeld et al., 2012;Hogner et al., 2013;Laskemoen et al., 2013a;Støstad et al., 2016) or seasonal (Lüpold et al., 2012;Cramer et al., 2013;Laskemoen et al., 2013a;Edme et al., revision under review) variation in avian sperm morphology. Furthermore, the potential of individual phenotypic plasticity to contribute to intraspecific variation in sperm traits has been largely neglected and evidence for gamete plasticity is scarce in general (Marshall, 2015). ...
... Only few studies, for example, have addressed such fundamental topics as geographical (e.g. Lüpold et al., 2011;Schmoll & Kleven, 2011;Lifjeld et al., 2012;Hogner et al., 2013;Laskemoen et al., 2013a;Støstad et al., 2016) or seasonal (Lüpold et al., 2012;Cramer et al., 2013;Laskemoen et al., 2013a;Edme et al., revision under review) variation in avian sperm morphology. Furthermore, the potential of individual phenotypic plasticity to contribute to intraspecific variation in sperm traits has been largely neglected and evidence for gamete plasticity is scarce in general (Marshall, 2015). ...
... Examples include age-dependent effects on sperm size in insects (Green, 2003) and fishes (Gasparini et al., 2010, Mehlis & Bakker 2013 or temperature-dependent effects on sperm size in insects (Blanckenhorn & Hellriegel, 2002), fishes (Adriaenssens et al., 2012) and molluscs (Minoretti et al., 2013). Only four studies, however, all using bird model systems, were able to demonstrate seasonal variation in sperm morphology (Lüpold et al., 2012;Cramer et al., 2013;Laskemoen et al., 2013a;Edme et al., revision under review). In contrast to our results in great tits, Lüpold (revision under review) demonstrated an increase in sperm total length over the breeding season in the collared flycatcher Ficedula albicollis. ...
Background: Spermatozoa display impressive variation in size and form among and within animal species. In birds, comparative evidence suggests that post-copulatory sexual selection resulting from extra-pair copulations is a major driver of interspecific sperm trait variation. However little is known about the extent, determinants and dynamics of intraspecific variation in avian sperm traits. Goal: Characterize and analyze variation in sperm morphology within and among two natural populations of great tits (Parus major) — a socially monogamous passerine with frequent extra-pair matings. Methods: We studied both a German and a Norwegian population of P. major. In the German population we sampled spermatozoa during both the first clutch egg-laying and the nestling period (partly from the same individual males). In the Norwegian population we sampled spermatozoa during the pre-laying/egg-laying period. We measured the length of spermatozoa with separate measurements of sperm head, midpiece and tail length. Results: In the German population, spermatozoa were significantly shorter during the nestling period than during the egg-laying period. Individual phenotypic plasticity was responsible for the seasonal dynamics in sperm morphology. Changes in flagellum length (sum of midpiece and tail length) rather than changes in head length accounted for the change observed in total length. We found that changes in flagellum length were attributable to both midpiece and, in particular, tail shortening. Consequently the ratio, 'midpiece/total length,' increased over the breeding cycle. Controlling statistically for seasonal variation, sperm total length was significantly repeatable across sperm samples from the same males. Furthermore, spermatozoa sampled in a Norwegian population early in the season differed from those obtained from the German population during egg-laying, but not from those obtained from the German population during the nestling period. Conclusions: Individual phenotypic plasticity across the breeding season may contribute to intraspecific variation in avian sperm morphology. Our comparison across populations illustrates that seasonal variation in sperm dimensions within populations may confound between-population comparisons unless one controls for sampling date in relation to reproductive phenology.
... Semen characteristics, especially sperm phenotypic and performance traits, represent important physiological features that may either be used as biomarkers or be of interest per se (Reinhardt et al. 2015;Lemaître and Gaillard 2017). Given their fundamental role in male reproductive success, sperm traits can serve as biomarkers of male fertility and reproductive fitness (Gomendio et al. 2006), or predict population and species differences in extrapair paternity rate (Lifjeld et al. 2010;Laskemoen et al. 2013;Šandera et al. 2013). Sperm traits further show pronounced environmentdriven plasticity, implying their potential as biomarkers of environmental conditions (Reinhardt et al. 2015). ...
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Physiological and biochemical traits hold great promise for demographic research as potential proxies (biomarkers) of various biotic and environmental variables that determine individual fitness and ultimately demographic rates. Integrating such biomarkers into demographic models can thus provide insights into drivers of population dynamics or increase predictive power of the models by refining estimation of vital rates. Biomarkers also represent promising means to characterise population structure and dynamics on much shorter time-scales compared to classical demographic approaches. Functional traits further emerge as direct targets of conservation efforts directed towards conserving functional diversity. Yet, biomarkers and functional traits remain underutilised in demography and population ecology, indicating that their benefits still await wider recognition. This chapter briefly reviews the most prominent physiological and biochemical traits (e.g. metabolic rates, hormones, oxidative stress markers, telomeres) that may be of interest in animal and plant demographic research, including the methods for collection, storage, and analysis, and the criteria to be met before the trait is validated as a biomarker. Hopefully, this effort will stimulate further integration of physiological and biochemical data into demographic framework.
... Extrapair paternity is generally high (e.g., ca. 20% of young in the European subspecies, H. r. rustica) but varies markedly across populations, and sperm morphology tracks the frequency of extrapair paternity in each population (i.e., small and variable sperm in a population with low extrapair paternity; Laskemoen et al. 2013;Hasegawa et al. 2019). Although sperm quality is found to be related to some traits in this species (e.g., Møller et al. 2008 for covariation between sperm swimming performance and male tarsus length), the relationship between pheomelanin-based coloration and sperm quality has not been reported. ...
Full-text available
Sexual selection favors the evolution of pre-copulatory sexual traits such as ornamentation and post-copulatory sexual traits such as long sperm, but the interrelationships of the two types of sexual traits remain unclear. Here, using Japanese barn swallows, Hirundo rustica gutturalis, and an interspecific analysis of the family Hirundinidae, we examined sperm length in relation to pheomelanin-based plumage coloration. As predicted by the fact that pheomelanogenesis consumes antioxidants, which would be detrimental to develop long sperm, reddish coloration (but not other ornaments) were negatively related to sperm length both within and across species, suggesting an evolutionary tradeoff between these traits.
... The total sperm length, the flagellum-, head-and midpiece length, and the head and midpiece width were measured using ImageJ v 1.45. Additionally, the head-to-tail ratio ((head length + midpiece length)/flagellum length) (Humphries et al. 2008) was calculated, and the coefficient of variation of sperm length within males (CV wm ) and between males (CV bm ) (see Laskemoen et al. 2007;Laskemoen et al. 2013) was calculated and adjusted for sample size (Sokal and Rohlf 1995). Furthermore, the maximum sperm length per individual was noted and a mean was calculated for each species. ...
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Fishes show a great diversity of mating systems and fertilization mechanisms. This diversity creates an enormous potential for sperm competition. Typically, monogamous species face a low risk of sperm competition and invest less into sperm, and thus show smaller relative testis mass compared to polygamous species with high sperm competition. In cichlids, sperm competition risk is very variable. In lacustrine East African cichlids, large sperm are interpreted as an adaptation to sperm competition, as in those species sperm length correlates with sperm swimming speed. The aim of the present study was to examine variation in sperm and testis traits of substrate breeding cichlids from West African river systems and its relationship to sperm competition. Therefore, sperm traits (total sperm size, flagellum-, midpiece-, and head size) and sperm number were related to the gonadosomatic index (GSI), an indicator of sperm competition, in eight species of two large informal tribes, the chromidotilapiines and the haplotilapiines. We found significant differences between species in all examined sperm traits, sperm number, and GSI with pronounced differences between chromidotilapiines and haplotilapiines. We used a generalized least-squares approach to control for non-independence of data. GSI was positively correlated with sperm number but negatively correlated with total sperm size (also negatively with the flagellum and head size but not significantly with midpiece size). Sperm number and sperm size were negatively correlated suggesting a trade-off between sperm size and quality. Our results suggest that large sperm can evolve in species with relatively low sperm expenditure and probably in absence of high sperm competition between males.
... The morphology of male gametes (spermatozoa) may be an example of such sexual traits . Spermatozoa exhibit remarkable variability in size and shape among species (Pitnick et al. 2009) and sometimes undergo rapid and substantial divergence even between closely related species or populations of the same species (e.g., Breed 1983;Landry et al. 2003;Pitnick et al. 2003;Hogner et al. 2013;Laskemoen et al. 2013a;Albrechtová et al. 2014). The diversity in spermatozoa (despite the common function of sperm cells to fertilize the ova) has been mostly attributed to postcopulatory sexual selection, including sperm competition and cryptic female choice (e.g., Snook 2005;Simmons and Fitzpatrick 2012;Rowe et al. 2015). ...
Postcopulatory sexual selection may promote evolutionary diversification in sperm form, but the contribution of between‐species divergence in sperm morphology to the origin of reproductive isolation and speciation remains little understood. To assess the possible role of sperm diversification in reproductive isolation, we studied sperm morphology in two closely related bird species, the common nightingale (Luscinia megarhynchos) and the thrush nightingale (L. luscinia), that hybridize in a secondary contact zone spanning Central and Eastern Europe. We found: (1) striking divergence between the species in total sperm length, accompanied by a difference in the length of the mitochondrial sperm component; (2) greater divergence between species in sperm morphology in sympatry than in allopatry, with evidence for character displacement in sperm head length detected in L. megarhynchos; (3) interspecific hybrids showing sperm with a length intermediate between the parental species, but no evidence for decreased sperm quality (the proportion of abnormal spermatozoa in ejaculates). Our results demonstrate that divergence in sperm morphology between the two nightingale species does not result in intrinsic postzygotic isolation, but may contribute to postcopulatory prezygotic isolation. This isolation could be strengthened in sympatry by reinforcement. This article is protected by copyright. All rights reserved
Diversification of sperm design is a common feature in animals. Considerable intra-individual variation has been detected even in species whose males produce a monomorphic sperm. The evolutionary forces that shape the variation in the gross morphology of these gametic cells are still not completely understood. Previous studies suggest that the intra-individual variation in sperm size reduces as a result of post-copulatory sexual selection. To our knowledge, for the first time, we provide evidence here that pre-copulatory sexual selection can also play a role. By studying the Neotropical paper wasp, Polistes simillimus, a monandrous species, we found reduced variation in sperm length in males bearing sexual ornamentation preferred by females. Besides, the female spermatheca contains a less variable sperm compared to that in the male seminal vesicles. Thus, the scope of selection, acting on this sperm trait, seems broader than previously acknowledged.
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In birds with extrapair mating, older males usually have higher fertilization success than younger males. Two hypotheses can potentially explain this pattern: 1) females prefer older, and often more ornamented males, or 2) older males invest more in reproduction and fertility than younger males. Here we studied factors associated with age-related male fertilization success in a population of barn swallows Hirundo rustica in Canada. We document that male fertilization success increased gradually up to a minimum age of four-year old. The age effect was especially strong for the number of extrapair offspring obtained and the occurrence of a second brood. The higher fertilization success of older males was also associated with an early start of breeding in spring. The length of the elongated outermost tail feathers, a postulated male ornament preferred by females, also increased with age (in both sexes), but it was not a significant predictor of male fertilization success within age classes. Male fertility traits, especially testis size, but also sperm motility and sperm velocity, increased significantly across age groups. Our results suggest that the higher fertilization success by older males is due to their higher reproductive investments and that their longer tails are an adaptation to early arrival on the breeding grounds. Significance statement The barn swallow is a socially monogamous passerine with extensive extrapair mating. We found that males become more successful in siring both withinpair and extrapair offspring as they become older. Their increased fertilization success was associated with a higher reproductive effort as indicated by larger testes, more motile sperm, and an earlier start of breeding in spring. The length of the outer tail feathers increased with age in both sexes, but long tails did not enhance male fertilization success among males of the same age. Long tails are probably an adaptation to rapid migration and earlier arrival on the breeding grounds. Our findings suggest that the commonly observed age-related increase in male fertilization success in passerine birds is better explained by life history theory than by sexual selection theory.
Basic knowledge about the genetic mating system is lacking for the great majority of the approximately 10,000 extant bird species. Filling this knowledge gap is not only critical for a comprehensive understanding of the reproductive ecology of each particular species, but also for increasing the power of comparative approaches to uncover and explain interspecific patterns of variation in avian reproductive traits. Using six polymorphic microsatellite markers, we here present the first parentage study in the socially monogamous Fieldfare Turdus pilaris. In parallel, we also examine variation in sperm morphology and relationships between sperm traits and paternity loss of social males. Across two study years, extra-pair paternity was detected in 46.4% (95% CI: 28.9–64.9%) of 28 broods, and on average 27.6% (95% CI: 16.8–41.9%) of nestlings per brood were extra-pair offspring in a population in central Norway. These observed extra-pair paternity rates fall within the range of reported estimates of extra-pair paternity for four congeneric Turdus species (between 36 and 65% of broods and 27 and 46% of nestlings). Sperm total length was 87.0 ± 2.9 (SD) μm (range 79.7‒96.8 μm) and 59.3% (95% CI: 37.1–73.3%) of the total phenotypic variation in sperm total length was explained by differences between sperm samples collected from 17 different males. The among-sample coefficient of variation in mean sperm total length was 2.70% (95% CI: 1.99–3.17%). We found no evidence for effects of sperm total length or relative midpiece length on loss of paternity among broods of 13 males.
Sperm competition can theoretically affect sperm morphology; however, it remains unclear whether and how sperm morphology tracks the intensity of sperm competition in each population. The barn swallow Hirundo rustica is a model species used in the study of sexual selection, and exhibits considerable variation in extra-pair paternity (percentage extra-pair young, ca. 3-30%) among populations. In the Joetsu population of the barn swallow, extra-pair paternity is virtually absent (< 3%), providing a rare opportunity to study sperm morphology under limited sperm competition, and to compare it with those reported in populations with frequent extra-pair paternity (>15%). We found that head, midpiece, and total sperm length were significantly shorter in the Joetsu population than in populations with frequent extra-pair paternity. Moreover, the variability in total sperm length, measured as the coefficient of variation in the Joetsu population, was twice as high as that of populations with frequent extra-pair paternity. These results are consistent with a positive, directional, and stabilizing effect of sperm competition on sperm morphology. Together with previous studies in populations with frequent extra-pair paternity, the current study provides one of few sets of evidence to show a link between the intensity of sperm competition and the mean and variance of sperm morphology within a wild bird species.
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Post-copulatory sexual selection (PCSS) is thought to be one of the evolutionary forces responsible for the rapid and divergent evolution of sperm design. However, whereas in some taxa particular sperm traits are positively associated with PCSS, in other taxa, these relationships are negative, and the causes of these different patterns across taxa are poorly understood. In a comparative study using New World blackbirds (Icteridae), we tested whether sperm design was influenced by the level of PCSS and found significant positive associations with the level of PCSS for all sperm components but head length. Additionally, whereas the absolute length of sperm components increased, their variation declined with the intensity of PCSS, indicating stabilizing selection around an optimal sperm design. Given the diversity of, and strong selection on, sperm design, it seems likely that sperm phenotype may influence sperm velocity within species. However, in contrast to other recent studies of passerine birds, but consistent with several other studies, we found no significant link between sperm design and velocity, using four different species that vary both in sperm design and PCSS. Potential reasons for this discrepancy between studies are discussed.
Sperm length varies considerably amongst closely related species and the variation can be positively related to interspecific variation ill the risk of sperm competition. In addition, a comparative study has shown that traits involved in sexual selection may often be sex linked. This study examined the quantitative genetics of sperm length in the yellow dung fly Scathophaga stercoraria (L.). There was a significant heritability of sperm length, h(2) = 0.673. In addition, a significant non-linear epistatic interaction between determinants on the X chromosome and on the autosomes was identified in a three-generation breeding experiment. The ratio of the additive to epistatic components was approx. 5:1, though this is probably an overestimate, and the total proportion of the variance in sperm length accounted for by these genetic factors was > 80%. I argue that selection acting in both males and females is relevant for the evolution of this trait.
Within the past twenty years, Drosophila subobscura (Collin 1936), endemic to the Old World, has rapidly colonized South America and the west coast of North America. Despite the recent colonization, inversion polymorphism and body size clines in North America have converged on clines found in Europe, indicating rapid evolutionary responses. One rapidly evolving trait in Drosophila is sperm length, which varies 180 fold between species. In species of the obscura group, to which D. subobscura belongs, sperm length also varies within individuals, a phenomenon known as sperm heteromorphism, in which males produce both short and long sperm. I examined sperm length evolution in males from eleven North American populations of D. subobscura representing a latitudinal transect of 1750 km. Significant differences between the populations in short and long sperm head lengths, and the total length of long sperm were found. However, these differences were not explained by latitude. A significant effect of males within a population on sperm length parameters was found indicating that sperm length variation within a population was equal to or exceeded variation across populations. Additionally, a potential constraint or stabilizing selection on sperm design was identified in that the ratio of short head to short tail compared to that ratio of long sperm did not differ. Results from this analysis suggest that significant inter-population variance in sperm length is unrelated to predictable environmental variation that mediates other traits, such as body size.
We tested the novel hypothesis that arrival date in migratory birds represents a reliable indicator of male quality that can be used by females as a cue in extrapair mating decisions. Secondary sexual characters are often condition-dependent, and competition for early arrival leads to condition-dependent migration. Hence, both secondary sexual characters and arrival date are predicted to be condition-dependent indicators of male phenotypic quality. We studied the relationship between expression of a secondary sexual character, arrival date, and condition, respectively, and extrapair paternity in a Spanish population of barn swallows, Hirundo rustica. By using microsatellite markers to determine paternity, we showed that 17.8% of all offspring (N e 674) and 32.4% of all broods (N e 170) were due to extrapair paternity. Quasi-parasitism (in which the male nest owner fathered the offspring, but the eggs were laid by another female) occurred in 2.6% of all nestlings and 2.9% of all broods. Individuals were consistent in the frequency of extrapair paternity among first, second, and third broods. Males with long outermost tail feathers, arriving early and in prime body condition, had little extrapair paternity in their nests. This was also the case when controlling for the confounding effects of male age. Partial correlation analysis was used to investigate the direct and indirect effects of tail length, arrival date, and body condition on extrapair paternity. Body condition accounted for most of the variance in extrapair paternity, whereas tail length and arrival date accounted for a smaller proportion of the variance. Body condition was strongly correlated with tail length and arrival date. However, because females cannot directly assess condition or arrival date (males arrive before females), females may obtain an indirect measure of condition and migration ability from tail length and other phenotypic traits of males. This suggests that extrapair paternity depends on the effects of condition, through its indirect effects on arrival date, tail length, and other variables. Copyright 2003.
Previous studies of the socially monogamous barn swallow (Hirundo rustica) have shown that males that most frequently engage in extrapair copulations and whose partners are least involved in copulations with extrapair males are those with long tail ornaments. In this study, through the use of three highly polymorphic microsatellite markers, we analyze the relationships between length of tail ornaments of male barn swallows and proportion of nestlings fathered in own broods, number of offspring fathered in broods of other pairs, and total number of offspring fathered, using both a correlational and an experimental approach. Consistent with our predictions, we show that males with either naturally long or experimentally elongated tails have higher paternity (proportion of biological offspring in own broods), and they produce more biological offspring during the whole breeding season than males with naturally short or experimentally shortened tails. Males with naturally long tails also had more offspring in extrapair broods than short-tailed males, but the effect of tail manipulation on the number of offspring fathered in extrapair broods, although being in the predicted direction, was not statistically significant. Cuckolded males that did not fertilize extrapair females had smaller postmanipulation tail length than cuckolders. We conclude that there is a causal, positive relationship between male tail length and paternity. Since female barn swallows have extensive control over copulation partners and heritability of tail length is high, this study shows that female choice is a component of selection for larger male ornaments. Benefits from extrapair fertilizations to females may arise because they acquire 'good' genes for sexual attractiveness or high viability for their offspring.
The Zebra Finch Taeniopygia guttata is a model bird species for the experimental study of behavioural and evolutionary concepts in captivity and especially sexual selection. The validity of sexual selection studies of domesticated birds is of long-standing concern as little is known about the influence of domestication on sexually selected traits. Most domesticated Zebra Finch populations are maintained under a strict breeding regime to avoid potential inbreeding. However, these breeding regimes may interfere with the processes of sexual selection and influence the evolution of sexually selected traits because they may limit or prohibit active mate choice. Here, we investigated the potential impact of a monogamous breeding scheme in a domesticated population in which active mate choice is largely inhibited, on the evolution of sperm morphometry as a sexually selected trait. We compared sperm morphometric traits (total sperm length and length of sperm head, midpiece and flagellum), and the variance thereof, between a domesticated and two wild Zebra Finch populations. Although we found significant differences between the three populations for certain sperm traits (head length, midpiece length), which may be of importance in postcopulatory sexual selection, overall, variance in sperm morphometry did not differ between the domesticated and the wild Zebra Finch populations. Our results validate the use of domesticated Zebra Finches for further studies of postcopulatory sexual selection and sperm competition.