Behavioral Ecology Advance Access originally published online on November 9, 2005
Behavioral Ecology 2006 17(1):108-116; doi:10.1093/beheco/arj003
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Rapid change in nest size of a bird related to change in a secondary sexual character
Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France
Address correspondence to A.P. Møller. E-mail: amoller{at}snv.jussieu.fr.
Received 30 March 2005; revised 8 September 2005; accepted 27 September 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Among bird species in which males contribute to nest building, sexual selection has favored larger nests. I investigated determinants of nest size in the barn swallow Hirundo rustica and how nest size changed during the period 1977–2003, when tail length (a male secondary sexual character) increased by more than 1.2 standard deviations. Males with short tails contributed more to nest building than long-tailed males, signaling their future investment in food provisioning of offspring. Pairs of barn swallows were consistent in nest size when build ing new nests the same or different years, and level of phenotypic plasticity in nest size was small and could not account for temporal patterns in nest size. Offspring resembled their parents with respect to nest size, indicating a significant heritability of nest size, independent of whether offspring were reared by their parents or by foster parents, and there was a significant negative genetic correlation between male tail length and outer nest volume and amount of nest material. The temporal increase in male tail length was associated with a decrease in nest size, with the amount of nest material in 2003 on average being less than a third of the amount used in 1977. Temporal change in nest size could be accounted for by indirect selection on tail length causing change in nest size to match that predicted from change in tail length and the genetic correlation between male tail length and nest size.
Key words: barn swallow, heritability, Hirundo rustica, nest building, parental care.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Many animals build nests although this behavior is particularly common in insects and birds (Collias NE and Collias EC, 1984
; Hansell, 1984). Because nests are used as containers for protecting dependent offspring from the environment and predators, advantages due to natural selection initially was involved in the evolution of nests (Collias NE and Collias EC, 1984; Hansell, 1984). While nest building by the female is a likely ancestral evolutionary state because females by necessity have to lay eggs and protect these from the environment, nest predators, and parasites, nest building by the male evolved subsequently. However, nest building is temporally associated with courtship and reproduction, providing the opportunity for females to assess features of male quality from their nest-building behavior (Soler et al., 1998b). Surprisingly, bird species in which both males and females contribute to nest building have nests that are almost twice as large as species in which only females contribute to nest building (Soler et al., 1998b). Empirical studies have shown a female preference for males with larger or more nests (Evans and Burn, 1996; Hoi et al., 1994, 1996).
Why should females care about the amount of male nest building, except for the fact that a larger share of building by the male may reduce the share by the female? Nest building may provide females with information about the condition and hence the genetic or phenotypic constitution of a partner. For example, Soler et al. (1999b) showed that male black wheatears Oenanthe leucura that were able to carry many and heavy stones to a potential nest site had stronger T-cell–mediated immune response than other males. In addition, male nest building may provide information about direct fitness benefits in terms of future male parental care. This suggestion is supported by a negative relationship between nest size and the relative duration of the nestling period across species of birds (Soler et al., 1998b). This relationship was independent of a number of different confounding variables, including nest site, that traditionally are considered to be associated with the risk of nest predation. Nest size may be an indication of the ability of the male to provision the offspring. Moreno et al. (1994) showed that male black wheatears fed their offspring more than the average male, if they carried a large number of stones to future nest sites or other sites. Similarly, Palomino et al. (1999) showed that nest size in the rufous bush robin Cercotrichas galactotes predicted variation in prey size and reproductive success. Møller (1994) showed that both nest building and food provisioning by male barn swallows decreased with the expression of a secondary sexual character, tail length. Previous studies of black wheatears, barn swallows, and magpies Pica pica suggested that females use male nest-building behavior to assess male phenotypic quality by investing differentially in reproduction when mated to a male that contributes disproportionately to nest building (De Neve and Soler, 2002; Soler et al., 1996, 1998b, 2001). This assertion is supported by experimental evidence from manipulation of nest size in the magpie (De Neve and Soler, 2002; Soler et al., 2001).
Natural selection plays an important role in the evolution of nest building and nest phenotype. For example, nest predation has reduced nests to extremely small containers or the complete absence of nests in certain tropical species but has also influenced nest size in the temperate zone (Hansell, 2000; Møller, 1990a; Snow, 1978). Likewise, brood parasites can use nest size as a cue to the quality of parental care provided by potential hosts, thereby selecting for smaller nest size in areas with high levels of brood parasitism (Soler et al., 1999a).
Hardly anything is known about the genetic basis of nest building or nest size. Hybrid cardueline finches build nests that are intermediate in size and shape of those of the parental species (Aarestrup WC, personal communication). Already Darwin (1872: 282) noted that nest building by birds is an innate behavior because related species such as the song thrush Turdus philomelos and the austral thrush Turdus falcklandii build strikingly similar nests, although one is a forest species and the other inhabits open grassland. Collias NE and Collias EC (1984) and Hansell (2000) report that nest building is an innate behavior that is performed even by individuals that have not encountered nest building by conspecifics. Naive individuals are able to build species-specific nests of normal size and shape (Collias NE and Collias EC, 1984; Hansell, 2000).
The aim of this study was to assess the genetic and environmental determinants of nest size in a passerine bird, the barn swallow. I have intermittently studied nest size and nest building in this species since 1977, providing long-term information on nest size and the factors associated with nest size. Previous studies have suggested that nest size is under sexual selection because male contribution to nest building causes an increase in nest size and because female investment in production of eggs is predicted by nest size independent of other phenotypic characters of males (Soler et al., 1998a). First, I tested whether nest size built by the same individuals was consistent among nests built the same year and in different years. Repeatability of nest size would provide an upper limit to the heritability of nest size (Falconer and Mackay, 1996). Second, I assessed the resemblance in nest size between parents and offspring, using data for local recruits, thereby estimating heritability of nest size. In addition, I estimated the genetic correlation between nest size and tail length, a secondary sexual character that is also used in female mate choice (Møller, 1994). Third, I assessed how nest-building behavior covaried with food provisioning and clutch size. This was done to assess the direct fitness benefits of choice of males that build large nests and the extent of female differential parental investment. Fourth, I determined how temporal change in tail length among cohorts of male barn swallows during a long-term study covaried with change in nest size among generations. This change across generations provided a quantitative assessment of how a microevolutionary change in tail length covaried with change in nest size across generations.
The barn swallow is an approximately 20-g aerial insectivorous migratory passerine. Barn swallows are sexually size monomorphic for most morphological characters with the exception of the two outermost tail feathers, which on average are 20% longer in males than in females in a Danish population (Møller, 1994). Females prefer long-tailed males as mates, and such males enjoy an advantage in terms of mating success, access to females for extrapair copulations, and differential parental investment by females (Møller, 1994). Both males and females build a cup-shaped nest from mud, straw, and feathers, and nest construction takes 3–21 days, on average 8 days (Møller, 1994). Attractive, long-tailed males build less than short-tailed males, resulting in pairs with a long-tailed male building small nests because females do not compensate for lack of male nest building (Soler et al., 1998a). Females invest differentially in reproduction when mated to a male that builds extensively (Soler et al., 1998a). Nests are often reused, and refurbishing consists of adding mud to the rim of the nest and a new nest lining (Møller, 1994). Nest reuse is costly in terms of ectoparasitism because the new brood can become infected with parasites that are already present in the old nest (Barclay, 1988; Møller, 1990b). Females incubate on their own, while both sexes provision the offspring. Most pairs have a second brood. Tail length of male barn swallows in the Danish population has on average increased by more than 12 mm since 1984 due to microevolutionary change associated with change in climatic conditions in North Africa during spring migration (Møller and Szép, 2005). This increase in tail length in males can be predicted to result in a decrease in nest size because males with long tails perform little nest building (Møller, 1994; Soler et al., 1998a) and because nest size is a direct function of male nest-building activity (Soler et al., 1998a). Therefore, males should now build less than earlier.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study site and period
I studied barn swallows at Kraghede (57° 12' N, 10° 00' E), Denmark (since 1971), as part of a long-term project. Detailed information on nest size and nest building has been collected intermittently during 1977–2003. The total study area covered approximately 30 km2 between 1977 and 1986, 45 km2 between 1987 and 1997, and 55 km2 between 1998 and 2003. These increases occurred to compensate for the reduction in population size over the years. The study site consists of open farmland with pastures, cereals, potatoes, and rape with mixed plantations, hedges, and ponds. Barn swallows breed within barns and other buildings (see Møller, 1994
, for further details).
General field procedures
Barn swallows were captured at least weekly from arrival in spring until the end of the breeding season using mist nets at all entrances to the barns with breeding birds. Mark-recapture analyses of the data have revealed that the capture probability of birds exceeds 98% (Møller and Szép, 2002).
On capture all adults were measured for a large number of phenotypic characters, recorded in a similar, standardized way. In the present study, I only used body mass, recorded with a Pesola spring balance to the nearest 0.1 g, and the length of the outermost tail feathers recorded with a ruler to the nearest millimeter. Repeated measurements of the same individuals in the same season or among seasons revealed a repeatability above 90% (Møller, 1994; Møller AP, de Lope F, Saino N, unpublished data).
All individuals were only included in their first year of capture, which can be considered to equal their first year of life. The latter statement is justified by the fact that among 175 local recruits ringed as nestlings in the study area, all with the exception of a single individual were first recaptured as 1-year-old breeding birds. The single exception was first recaptured as a 2 year old. Likewise, breeding site fidelity is extremely high with only 4 of 3365 adults ever moving to another breeding farm and then also in all cases to the nearest neighboring farm (maximum distance moved 400 m). All individuals that were subjected to various experimental treatments from other field experiments were excluded, but individuals from untreated control groups were included in the analyses. This should not cause any bias because treatments were assigned randomly to individuals.
Estimating nest size and nest building
Nest size can be described by four different parameters, and whenever nest size is mentioned, this refers to all these four parameters. I measured inner diameter, external diameter, and height and depth of nests to the nearest millimeter with a ruler in the years 1977–1985, 1987, 1993, and 1999–2003. Preliminary analyses of data from the first three years have been published previously (Møller, 1982). Because I made all measurements myself, there was no error included due to interobserver variability. Sample sizes for number of nests measured in these years were 58, 46, 20, 14, 28, 53, 47, 53, 48, 31, 19, 37, 73, 57, 58, and 115, in total 757 nests. Because I did not know the owner of nests, when making the measurements, all measurements of nests were made blind with respect to phenotype of the nest owner. Because many barn swallow nests are reused and refurbished, causing them to be used during many years (Møller, 1994), I only used new nests to avoid that estimates of nest size were confounded by certain nests having been built over many years. Many farmers remove old nests every year, thereby preventing nests from being old. I estimated nest cup volume and nest volume as a fraction of an ellipsoid using the equation
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). For nest cup volume the fraction of an ellipsoid is 0.5, while it attains values of 0.5 for outer nest volume when the nest site is on top of a beam, 0.25 when attached to the side of a beam, and 0.125 when placed in a corner. The volume of nest material is simply outer nest volume minus nest cup volume. Nest wall thickness is outer radius minus inner radius.
I obtained estimates of nest-building behavior in 1987, 1988, 1996, 1997, and 2003. I watched pairs during the nest-building period when collecting mud for the nest cup, making observations for at least 1 h on three different days. Nest building was recorded separately for males and females, and it was quantified as building visits per hour. I estimated relative nest building by males as the number of nest-building visits by the male divided by the total number of nest-building visits by the pair. These estimates of nest-building behavior are highly repeatable because one-way ANOVAs show consistent differences in nest-building activity among pairs (Soler et al., 1998a, Figure 1). I recorded feeding behavior during the same years as nest building. Nests were watched for 1 h when nestlings were 12 days old, and the number of feeding visits by male and female parents was tallied. I estimated relative male feeding as the number of male feeding visits divided by the total number of feeding visits by the pair. These estimates of feeding behavior are highly repeatable among pairs, as shown by one-way ANOVAs (Møller, 1994). Data on feeding rates were available for 1985–1988, 1996–1999, and 2003.
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Reproductive variables
Reproduction of barn swallows was recorded at least twice per week during regular visits to nests throughout the breeding season and often daily around the time of laying, hatching, and fledging. This allowed collection of information on laying date, clutch size, brood size at hatching, and brood size at fledging.
I made extensive cross-fostering experiments in 1989, 1990, 1998, and 1999, involving a total of more than 200 nests, when nestlings were 1–2 days old, and hence did not yet have open eyes, allowing comparison of the phenotype of offspring in relation to the phenotype of parents and foster parents. A total of 18 recruits provided information for this test, where nest dimensions of offspring were related to nest dimensions of parents and foster parents.
Recruitment
During regular capture of adult birds, I also captured local recruits, resulting in a total of 175 recruits over the years. Nest size information was only available for these recruits and their parents in 100 cases, and information was only available for one recruit for each parent. Local recruits only comprise a small fraction of all recruitment, explaining the low degree of variance in recruitment among individuals. The fact that local recruitment only comprised a fraction of total recruitment does not differ from the situation in other population studies of birds (or other organisms), where local recruitment also only comprises a fraction of total recruitment.
Statistical analyses
To avoid problems of pseudoreplication, I only included barn swallows the first time they were captured as a yearling.
I calculated repeatability of nest-building behavior and nest size within and among years. This was done using one-way ANOVAs (Becker, 1984).
I related nest building to male tail length within and among years, using estimates of nest size and tail length of attending males, as described above.
I estimated heritability of nest size from linear regressions of nest size of offspring on nest size of parents, using data for 100 local recruits. The heritability estimate is the slope of the linear regression (Falconer and Mackay, 1996). I controlled statistically for any effects of year and maternal phenotype by inclusion of these variables as additional factors or variables in the parent-offspring regression models. Similarity in nest dimensions between offspring and their parents and foster parents was assessed in multiple regression analyses with the offspring value as the dependent variable and the parental and foster-parental value as predictor variables. The two genetic correlations between tail length and nest variable were calculated from tail length of father and nest variable of son and nest variable of father and tail length of son, respectively (Falconer and Mackay, 1996).
Not all information was available for all individuals, and sample sizes therefore differ among tests.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Repeatability of nest size and nest dimensions
Males that contributed a lot to nest building for the first nest of the year did likewise for the second nest (Table 1). Repeatability for nests built the same year for the four variables describing nest size variation was intermediate to large and highly significant (Table 1). Likewise, repeatability analyses of nest size between years for the same pairs were highly significant (Table 1). Thus, barn swallows were consistent in their nest-building behavior and nest size among nest-building events.
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Heritability of nest size and genetic correlations
Heritability estimates ranged from 0.33 for nest cup volume to 0.68 for outer volume (Figure 1; Table 2). These conclusions did not change if year was entered as a factor in the analyses (outer volume: F = 95.51, df = 1,98, p < .001, h2 [SE] = 0.68 [0.07]; nest cup volume: F = 12.36, df = 1,98, p = .007, h2 [SE] = 0.32 [0.09]; nest material: F = 62.51, df = 1,98, p < .001, h2 [SE] = 0.62 [0.08]; nest wall thickness: F = 57.21, df = 1,98, p < .001, h2 [SE] = 0.46 [0.06]). Likewise, the parent-offspring resemblance did not change if variables potentially associated with maternal effects such as brood size, laying date, or maternal body mass were entered as predictors. None of these showed a significant independent effect in the parent-offspring regressions (results not shown).
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Rearing environment did not cause resemblance in nest size across generations, as shown by cross-fostering experiments. A total of 18 cross-fostered offspring resembled their true parents but not their foster parents in terms of nest size because nest size of foster parents never entered as a significant predictor of nest size of offspring (Table 3). This provides evidence of resemblance to parents but not to foster parents.
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Aspects of nest size were genetically correlated with male tail length. Parent-offspring correlations revealed statistically significant negative genetic correlations for outer nest volume and nest material but not for nest cup volume or nest thickness (Figure 2; Table 4). Thus, outer nest volume and the amount of nest material decreased with increasing tail length of male barn swallows. In contrast, there was no evidence of significant genetic correlations with female tail length for any of the four measures of nest size (rG < 0.15, p > .15, n = 96).
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Nest building, food provisioning, and clutch size
Male barn swallows that contributed the most to nest building were also those that provided the largest proportion of food for their offspring (Figure 3). This was also the case in individual years and in another study of the same species (Soler et al., 1998a
). Thus, male nest construction is a predictor of later male parental care.
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Clutch size increased with three measures of nest size (analyses of covariance [ANCOVA] with year as a factor—outer volume: F = 35.20, df = 1,679, p < .0001, slope [SE] = 0.74 [0.13]; nest cup volume: F = 23.16, df = 1,679, p < .0001, slope [SE] = 0.46 [0.09]; nest material: F = 21.85, df = 1,673, p < .0001, slope [SE] = 0.43 [0.09]; nest wall thickness: F = 3.50, df = 1,675, p = .0005, slope [SE] = 0.011 [0.003]). A stepwise analysis with year as a factor only resulted in outer nest volume and year entering as significant predictors of clutch size (results presented above). The amount of variance explained by nest dimensions in these models never exceeded 5%.
Temporal change in nest size and nest dimensions
Nest size changed dramatically during the period 1977–2003. There was a significant decrease in outer nest volume, nest cup volume, nest material, and nest wall thickness during the study period (Figure 4). Both outer volume and nest cup volume decreased by more than two-thirds during the period of 25 years, while the amount of nest material and nest wall thickness decreased by half during the same period.
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Change in mean nest size during the period 1977–2003 was similar for pairs with yearling and older birds. In these analyses, a pair was either classified as composed of yearlings only or at least one bird that was older than 1 year. ANCOVA with mean nest dimension for each year as the response variable, age as a factor, and year and year by age as predictor variables never showed a significant effect of age or year by age interaction (analyses based on log10-transformed data—effect of age: F < 0.17, df = 1,12, p > .90; effect of year by age: F < 0.28, df = 1,12, p > .090). Thus, changes in nest size were independent of age of barn swallows.
Nest size did not change because nest material became less available. Mud can become unavailable during period with drought, causing nest building to be delayed (Møller, 1994). However, the amount of rain in May, which is the main month of nest building, for the nearest meteorological station 2 km south of the study area remained stable during the period 1977–2003 (F = 0.03, df = 1,25, p = .86). Thus, it seems unlikely that availability of nest material could explain variation in nest size.
We can use differences in nest size between years for the same pairs to test whether phenotypic plasticity is likely to account for the observed differences in nest size during the study. If phenotypic plasticity was an important factor determining the decrease in nest size over the years, we would expect change in nest size from one year to the next to decrease. Mean change in nest size between two subsequent years due to phenotypic plasticity was for outer volume 1.4 cm3 (SE = 128.0), nest cup volume –28.3 cm3 (19.1), nest material 29.7 cm3 (121.2), and nest thickness 1 mm (4). None of these estimates differed significantly from zero. Likewise, all these estimates were much smaller than the differences in nest dimensions recorded during this study (Figure 4). Thus, we can conclude that differences in nest dimensions recorded during 1977–2003 are unlikely to be explained by phenotypic plasticity.
Change in nest size and change in adult morphology
Temporal change in tail length was a significant predictor of change in nest size. Outer nest volume, nest cup volume, nest material, and nest wall thickness all decreased as mean tail length of males in the population increased (Figure 5). Similar but weaker relationships were recorded for female tail length (linear regressions based on mean log-transformed nest size each year: F = 11.72–22.29, df = 1,14, r2 = .46–.61, p < .004). Stepwise regression analyses only showed significant partial regressions for male tail length but none for female tail length (Table 5).
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Clutch size did not change significantly during the study period (linear regression based on mean estimates per year: F = 0.05, df = 1,25, r2 = .004, p = .88). Hence, changes in nest size could not be attributed to changes in clutch size and hence the amount of material needed for accommodating offspring.
Body mass increased significantly during the study period in males (linear regression based on mean estimates per year: F = 37.39, df = 1,25, r2 = .60, p < .0001, slope [SE] = 0.044 [0.007]), but less so in females (F = 9.61, df = 1,25, r2 = .28, p = .005, slope [SE] = 0.05 [0.01]). If an increase in body mass reflects improved body condition, and if nest building is condition dependent, then we can predict that nest-building activity should increase and nests become larger as body mass increased. However, larger mass of males and females did not account for changes in nest size because neither body mass of males nor females entered as significant predictors of nest size in stepwise regression analyses (Table 5). Body size measured in terms of tarsus length decreased significantly during the study period in both adult males and females (linear regression based on mean estimates per year—males: F = 59.69, df = 1,25, r2 = .71, p < .0001, slope [SE] = –0.027 [0.004]; females: F = 48.06, df = 1,25, r2 = .66, p < .0001, slope [SE] = –0.028 [0.004]). However, change in nest size was not associated with change in tarsus length because neither male nor female tarsus length was a significant predictor of nest size in stepwise regression analyses (Table 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Nest size in the Danish barn swallow population changed dramatically during a period of only 25 years, providing a unique opportunity to test a number of predictions relating to the adaptive significance of nest building. The main novel findings of this study were as follows. Individual barn swallows consistently built nests of a given size for different broods and in different years. A similar consistency was observed across generations because nest size of offspring resembled nest size of their parents, independently of whether they were cross fostered or reared by their parents, implying that nest building and nest size had a heritable basis. Nest size was significantly negatively genetically correlated with male tail length. Females benefited from choosing a male with a large nest because males that contributed significantly to nest building, and therefore had large nests, also contributed disproportionately to provisioning of offspring. The rapid reduction in nest size across generations followed an increase in tail length of adult male barn swallows. Finally, both direct selection on nest size and indirect selection through tail length may have accounted for the temporal change in nest size. I will discuss each of these findings.
The findings reported here are based on correlational evidence, making confounding variables of potential importance when interpreting the results. First, changes in tail length and nest size are associated with a decrease in overall population size (Engen et al., 2001; Møller, 2004). However, it seems unlikely that the relationship between change in tail length and change in nest size is confounded by changes in population size. Colony size has not changed, and the proportion of solitarily breeding barn swallows and the proportion breeding in large colonies have remained constant (Møller, 2004). This implies that the intensity of interactions including intraspecific competition during the breeding season has remained unchanged during the study. Second, the changes observed here may arise from changes in environmental conditions. For example, mean temperature in April in the study area has increased by more than 2.5° since 1971. However, this change in temperature has not caused a change in breeding date, which has remained stable since 1971 (Møller, 2002). Changing environmental conditions may also affect availability of nest material, although this explanation seems unlikely to account for changes in nest size. Mud used for nest building is collected near farms where barn swallows are breeding. Mud is readily available at ponds and other open water bodies, and there is no evidence that availability of nest material affects timing or duration of nest building. Thus, population density or environmental conditions in the breeding area seem unlikely causes of change in nest size.
Consistency in nest building and nest size among nest-building events for the same pairs, estimated in terms of repeatability, provides an upper limit to heritability (Falconer and Mackay, 1996). Repeatabilities of male contribution to nest building and nest size were all intermediate to large (Table 1). Heritability estimates based on parent-offspring regressions were all statistically significant, and the estimates were in the range 0.33–0.66 (Table 2). This suggests that there is a quantitative genetic basis for nest size. It seems unlikely that resemblance in nest size among relatives is due to learning because nest building is an innate behavior that offspring do not acquire by watching their parents or other adults (Collias NE and Collias EC, 1984; Hansell, 1984). In addition, offspring see little or no nest building when in their nest or after fledging because most nest building has ceased for the year. Analyses of nest size of nestlings reared by their parents or foster parents showed that offspring nest size resembled that of their parents, but not of their foster parents, suggesting that rearing environment during the nestling period does not affect the size of nests constructed when adult. Because nest size differed among years, the heritability estimates may be biased due to temporal change in nest size. This is potentially a general problem in all field studies of quantitative genetics because the environment is never constant, not even within a single breeding season. However, the estimates did not change after including year as a factor in the regression models. There was no evidence of resemblance between offspring and their foster parents in a small sample of cross-fostered recruits, while there was significant resemblance with parents. Because nestlings were cross fostered before they opened their eyes, this suggests that nestlings did not build nests dependent on what they experienced during rearing but rather built nests dependent on the nest of origin. I found evidence of a genetic correlation between tail length of male barn swallows and the outer volume of the nest and the amount of nest material (Table 4). In contrast, there was no evidence of a significant genetic correlation for nest cup volume or nest thickness (Table 4). This difference among characters can be explained by the role of the male and the female in determining different components of nest size. Males and females contribute significantly to nest building, but it is the female that constructs the nest cup and the rim of the nest when the nest is almost finished (Møller, 1982).
Nest size and shape differ considerably among taxa of birds and other organisms (Collias NE and Collias EC, 1984; Hansell, 1984, 2000). In fact, nest size and shape has considerable predictive power in terms of phylogeny (Winkler and Sheldon, 1993). This implies that nest size and shape can evolve and that different selection pressures may have contributed to this evolutionary diversity. What are the selection pressures that may account for evolution of nest size? Natural and sexual selection may both be important determinants of nest size, and trade-offs between natural and sexual selection may be responsible for the change in nest size in the barn swallow, as suggested by Soler et al. (1999a). Sexual selection accounted for within- and among-cohort patterns of nest building and nest size. Males with long tails built less and had smaller nests than males with short tails, both in individual years and across generations when male tail length increased by more than 12 mm or 1.2 standard deviations (SDs). Male nest building was an indicator of food provisioning of nestlings, and I hypothesize that this is the main benefit obtained by females mated to the most intensely nest-building males. Previous studies of the barn swallow have shown that relatively greater male feeding effort translates into heavier offspring and fewer feeding trips by the female partner (Saino and Møller, 1995). Females responded to male nest building by laying larger clutches, and clutch size was only weakly predicted by outer nest volume but not by size of the nest cup or thickness of the rim of the nest. This finding is similar to what has been found in a Spanish population of barn swallows (Soler et al., 1998a). In contrast to these results for males, there was no relationship between tail length of females and nest building or nest size. Body mass of males increased significantly over the years, as expected, because tail length has increased across generations and because tail length is condition dependent (Møller, 1989, 1990c, 1993, 1994; Møller and de Lope, 1999). Greater body condition should reduce the physiological costs of nest building. However, nest size was not significantly related to body mass of males. These findings are consistent with the hypothesis that female barn swallows either acquire good gene benefits from pairing with a long-tailed male or direct fitness benefits in terms of nest building and food provisioning from pairing with a short-tailed male (Soler et al., 1998a). What are the natural selection pressures associated with nest building? At least three are possible. First, larger and more solid nests may less often fall before fledging of offspring. As stated in the Introduction, this selection pressure seems weak because only 0.18% of all nests ever fell while containing eggs or nestlings. Second, ectoparasitism may comprise an important natural selection pressure. Old nests are more likely to contain ectoparasites than new nests, and this considerably reduces reproductive success (Barclay, 1988; Møller, 1990b). Finally, I cannot exclude the possibility that predation is a natural selection cost of nest building. Domestic cats and other predators are commonly seen attempting to catch nest-building barn swallows at puddles where mud for nests is collected (own observations).
Nest size of the barn swallow decreased significantly during the period 1977–2003, with outer nest volume and nest cup volume decreasing by two-thirds, while the amount of nest material and nest wall thickness were reduced by half (Figure 4). These changes are very large, and the difference in nest size between 1977 and 2003 is just as large as differences in nest size between many species of birds. I investigated a number of factors that were hypothesized to account for the decrease in nest size. Body mass, tarsus length, and tail length of adults changed significantly during the study period. However, only change in tail length of adult male barn swallows was a significant predictor of change in nest size (Figure 5; Table 5). This finding is as predicted because long-tailed males build less than short-tailed males, male nest-building activity determines nest size (Soler et al., 1998a), and mean tail length of cohorts of male barn swallows has increased by more than 12 mm on average during the study.
The temporal change in nest phenotype can either be due to phenotypic plasticity or a microevolutionary change. Which of these alternatives is more likely? Barn swallows are highly consistent in nest-building and nest size parameters among nest-building events (Table 1). The change in nest size among years is considerably larger than the difference in nest size among nest-building events by the same individuals. Therefore, phenotypic plasticity is an unlikely explanation for the observed change. The alternative interpretation that the change is due to microevolution is supported by two pieces of evidence. First, nest size is significantly heritable, and outer nest volume and the amount of nest material have significant negative genetic correlations with male tail length but not with female tail length. This provides two necessary requirements for an evolutionary change in nest size when tail length changes. Second, male tail length has increased by more than 1.2 SD units, associated with a change in selection pressures during spring migration in North Africa (Møller and Szép, 2005). Given the negative genetic correlation between tail length and nest size, we should expect nest size to decrease in response to an increase in tail length. Thus, the simplest explanation for the change in nest size since 1977 is that this has happened as a consequence of a microevolutionary change in male tail length. This hypothesis is supported by the observation that change in nest size across generations can be predicted by change in tail length across generations (Figure 5). The change in nest size due to indirect selection on male tail length can be predicted to be the change in tail length (measured in units of SDs) times the genetic correlation between nest material and tail length. Thus, we should expect this change to amount to 1.2 (change in tail length) x 0.282 (mean genetic correlation from Table 4) = 0.34. Because nest volume was 2.41 (in log units, SD = 0.36) in 1977, this indirect selection should cause nest size to decrease to 2.07 during the study period. In fact, nest material in 2003 was 2.08 (SD = 0.26). For outer nest volume the same calculations gave 1.2 x 0.302 = 0.36. Because outer nest volume was 2.63 (in log units, SD = 0.51) in 1977, this indirect selection should cause outer nest volume to decrease to 2.27 during the study period. In fact, outer nest material in 2003 was 2.28 (SD = 0.19). This suggests that indirect selection on male tail length is fully sufficient to account for the observed decrease in nest size during the last 25 years. Although observed and predicted values are very similar, we do not know to which extent the parameter estimates used for the calculations are biased. Several sources of bias were investigated, but none were found to be of major importance. In conclusion, indirect response to selection on tail length is a more likely cause of decrease in nest size than direct selection on nest size.
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ACKNOWLEDGEMENTS |
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N. Cadée, A. Camplani, E. Flensted-Jensen, and C. Spottiswoode kindly helped with fieldwork. This study benefited greatly from discussions with M. Hansell and J.J. Soler. The French Biodiversity Program ACI CLIMPOP supported my research in 2003–2004.
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REFERENCES |
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