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Keywords:

  • hatching date;
  • Hirundo rustica;
  • immunity;
  • life history;
  • longevity;
  • maternal effects

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

1. Longevity is a major determinant of individual differences in Darwinian fitness. Several studies have analyzed the stochastic, time-dependent causes of variation in longevity, but little information exists from free-ranging animal populations on the effects that environmental conditions and phenotype early in ontogeny have on duration of life.

2. In this long-term (1993–2011) study of a migratory, colonial, passerine bird, the barn swallow (Hirundo rustica), we analyzed longevity and, in a subsample of individuals, lifetime reproductive success (LRS) of the offspring that reached sexual maturity in relation to hatching date, which can affect the rearing environment through a seasonal deterioration in ecological conditions. Moreover, we analyzed the consequences of variation in body size and, for the first time in any species, of a major component of immunity on longevity, both by looking at absolute phenotypic values and at deviations from the brood mean.

3. Accelerated failure time models showed that individuals of both sexes that hatched early in any breeding season enjoyed larger longevity and larger LRS, indicating directional selection for early breeding. Both male and female offspring with large T cell-mediated immune response relative to their siblings and female nestlings that dominated the brood size/age hierarchy had larger longevity than their siblings of inferior phenotypic quality/age. Conversely, absolute phenotypic values did not predict longevity.

4. Frailty modelling disclosed marked spatial heterogeneity in longevity among colonies of origin, again stressing the impact of rearing conditions on longevity.

5. This study therefore reinforces the notion that perinatal environment and maternal decisions over timing and site of breeding, and position in the brood hierarchy can have marked effects on progeny life history that extend well into adulthood. In addition, it provides the first evidence from any bird population in the wild that immune response when nestlings predicts individuals’ longevity after sexual maturation.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

The causes and mechanisms that generate variation in the relative contribution of individuals to the genetic composition of the next generations are pivotal to any research field in evolutionary ecology (Williams 1992). While genetic and environmental determinants of variation in Darwinian fitness have been often investigated using cross-sectional information on fecundity or progeny quality and short-term survival as proxies for reproductive success (e.g. Newton 1989), studies of offspring longevity in the wild are rare (Cam, Monnat & Hines 2003; Van de Pol et al. 2006; Wilkin & Sheldon 2009; Bouwhuis et al. 2010a,b). This is unfortunate because longevity is one of the key factors underpinning lifetime reproductive success (LRS) via an effect on number of reproductive events over the entire life (Newton 1989; Reid et al. 2003; Grant & Grant 2011).

Longevity has obvious environmental determinants, such as time-dependent exposure to predation or adverse weather (e.g. Newton 1998). However, environmental factors, including maternal effects (Mousseau & Fox 1998; Badyaev & Uller 2009; Wolf & Wade 2009), which offspring experience during early ontogeny, have the potential to act as major sources of variation in longevity but have been largely neglected in studies of wild populations (but see Cam, Monnat & Hines 2003; Van de Pol et al. 2006; Wilkin & Sheldon 2009; Bouwhuis et al. 2010b). The pathways whereby perinatal environment and maternal effects can translate into variation in offspring viability range from early epigenetic actions on germ cells to developmental consequences of variation in egg composition (Mousseau & Fox 1998; Eising et al. 2001; Saino et al. 2003, 2006; Rubolini et al. 2006; Muller et al. 2007; Badyaev & Uller 2009; Wolf & Wade 2009). Parental decisions on breeding time and site are also expected to set the early environmental scene for the offspring by affecting parental care and rearing conditions (Lindström 1999). Independent of the mechanism through which they operate, such effects can have immediate consequences on progeny viability but also on prime development, physiology and behaviour of the offspring and their life history, with consequences on performance later in life (Mousseau & Fox 1998; Alonso-Alvarez et al. 2006; Groothuis et al. 2006; Rubolini et al. 2006; Carere & Baltazhart 2007; Muller et al. 2007; Badyaev & Uller 2009; Schlichting & Mousseau 2009; Bonisoli-Alquati et al. 2011).

Timing of reproduction in seasonally varying environments typifies the effects of parental decisions over breeding on offspring. Seasonal deterioration of offspring quality and viability has been demonstrated in a number of studies, particularly of birds, and often interpreted as a consequence of the effects of worsening ecological conditions as the breeding season progresses on both parents and offspring (Lack 1950; Verboven & Visser 1998; Dubiec & Cichoñ 2001; Grüebler & Naef-Daenzer 2008; Verhulst & Nilsson 2008). Variation in phenotypic quality or age of parents breeding at different times constitutes an additional cause of variation in offspring phenotype (Newton 1989). Much work on early environmental and maternal effects in birds has used body size, immunity or recruitment into the breeding population as proxies for offspring fitness (Verboven & Visser 1998; Naef-Daenzer, Widmer & Nuber 2001; Verhulst & Nilsson 2008; López-Rull et al. 2011), but we are aware of extremely few studies where the effects of breeding date and phenotypic quality of the offspring on longevity after sexual maturity have been analyzed in any free-living bird population (e.g. Bouwhuis et al. 2010b), and even information from laboratory studies is scant (e.g. De Kogel 1997).

The first aim of our study thus was to analyze variation in longevity and LRS of barn swallows (Hirundo rustica) in relation to their hatching date. Specifically, we focused on longevity of sexually mature individuals recruited into the breeding population as 1-year old adults, because extremely high breeding philopatry allows to gather accurate information on annual survival. Conditions for breeding as well as parental quality in this species may deteriorate as the season progresses (Møller 1994; Turner 2006), and we therefore expected longevity after sexual maturity to decline with hatching date.

We also predicted that high phenotypic quality of individual offspring, as gauged by absolute body size, and, for the first time in any bird species, by a major component of immune response, predicts longevity. In altricial birds, however, hatching asynchrony often enforces an age/size hierarchy among siblings, which may result in severe competitive asymmetries: later hatched smaller offspring typically suffer restricted access to limiting parental resources compared to their siblings as a result of parental favouritism and/or differences in competitive abilities (Mock & Parker 1997). In such ‘structured families’ (sensu Hall et al. 2010), ‘core’, advantaged offspring enjoy better phenotypic conditions and viability (Lack 1954; Ricklefs 1993; Stenning 1996). In barn swallow broods, even small levels of hatching asynchrony (Boncoraglio & Saino 2008) translate into a size hierarchy which is permanently retained throughout the nestling period. Position in the brood hierarchy and social stress, however, may have long-lasting effects on longevity. We therefore also tested whether phenotypic quality of nestlings relative to their siblings predicted longevity while expecting a positive association between relative phenotypic value and longevity. Because nestlings in large broods experience poor nutritional conditions and harbour more ectoparasites per capita (Saino, Calza & Møller 1997; Saino et al. 2002a), we also had the prediction that longevity declined with brood size.

Sex is a major determinant of variation in longevity (Liker & Székely 2005), and sex-related variation in lifespan may depend on differential susceptibility to rearing conditions (Tschirren, Fitze & Richner 2003; Saino et al. 2006; Boncoraglio, Martinelli & Saino 2008). In the barn swallow, nestling sex ratio is close to parity (Saino, Martinelli & Romano 2008), while sex ratio among adults is male-biased (Møller 1994). We therefore investigated whether sex-related variation in longevity after sexual maturation existed, which may contribute to sex ratio variation among age classes.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Study Organism

The barn swallow is a small, semicolonial, socially monogamous passerine bird whose European breeding populations overwinter south of the Sahara (Møller 1994; Cramp 1998). The large majority of barn swallows breed colonially in rural buildings (Møller 1994; Ambrosini et al. 2002; Turner 2006). Animal farming and quality of the crops in the foraging home range affect the size and demographic trend of the colonies and have some weak effects on nestling phenotype (Møller 1994; Ambrosini et al. 2002; Turner 2006; Ambrosini et al. 2012). In our study population, 70–80% of the females lay four or five eggs per clutch. One to three clutches are laid from April to July. Most yearlings lay one clutch per year whereas most two- or more year old adults have two or three clutches, though the number of clutches may considerably vary among years and areas.

General Methods

In 1993–2011, we studied 14 colonies (=farms) East and South-East of Milano (Northern Italy) that were regularly visited to record clutch size and hatching date (=date of hatching of the first egg to hatch) by inspecting the nests directly or by means of a mirror mounted on a pole, ring the nestlings and measure body mass, tarsus length and response to a standard test of T cell-mediated immunity (‘PHA test’; see Saino, Calza & Møller 1997; Tella et al. 2008) at 10–13 days after hatching (see Statistical Analyses for an account of how we dealt with the potentially confounding effect of age). Because in several years we focused our nestling ringing effort on first clutches, most (>85% depending on the analysis) of the recruits considered here originated from a first clutch. Restriction of the sample to these individuals did never qualitatively alter the results (i.e. the effects that were significant on the entire data set remained such) compared to the analyses on the entire sample. We aimed at analyzing the effect of phenotypic quality of individual nestlings relative to their siblings on longevity. We therefore computed relative phenotypic values of body mass, size and immune response for individual recruits as the difference between the absolute value measured for that recruit and the mean of its brood of origin. As experiments have been carried out in the study population, all the recruits and adults from manipulated groups were excluded.

Our data consist of longevity of individuals that were marked as nestlings and were recruited as 1-year old breeding adults. Because natal dispersal is high (Turner 2006; Balbontín et al. 2009), to increase sample size we used data from our long-term study while appropriately testing for cohort effects. Recruits could be either ‘local’ (i.e. breeding in their colony of origin) or ‘emigrants’ (breeding in a different colony).

In all study years, we did repeated capture sessions in each farm throughout spring and summer (late March–July) to record recruitment and survival. Because barn swallows spend the night inside the buildings where they breed, we could capture all the individuals by putting up nets at all doors and windows before dawn. Importantly, barn swallows in our and neighbouring populations (North-western Italy; Southern Switzerland; see Data S1) show extremely high breeding philopatry (see also Møller 1994; Saino et al. 1999, 2011). High breeding philopatry and capture efficiency imply that recapture probabilities were homogeneous and very close to 1. The case that in few instances death was imputed for birds that in fact skipped breeding cannot be ruled out, although this eventuality was likely to be rare, as nonbreeding individuals are regularly captured at the colonies. As adult breeders do not disperse, longevity of recruits could be estimated accurately based on the information on year of recruitment (1 year of age) and of year of disappearance (i.e. the first year when they were not captured, implying that they had died) (see Møller 1994; Saino et al. 1999, 2011; see also Data S1).

Barn swallows leave the colonies in June-August and survivors return in March–May, implying that exact date of death was unknown. In modelling longevity we thus assumed the year of recruitment as time 0 and imputed longevity of 0·5 years to individuals that did not survive to age 2, 1·5 to those that survived to age 2 but not to age 3, and so forth. Hence, there was no left censoring in our data, whereas right censoring occurred for only 5·7% of the observations.

Breeding pairs were assigned to their nest by direct observation of breeding behaviour of the individuals that could be recognized, thanks to unique combinations of colour rings and markings on breast and belly feathers that were applied at first capture in any given year (see e.g. Saino et al. 1999). We could thus obtain information on breeding performance through the entire life (i.e. until the last year when they were captured) on a subsample (= 54 individuals; 45 males; 9 females) of the recruits that could be included in the present study. As a proxy for LRS we used total number of eggs because this datum was available for a larger number of nests and it was collected in a more standardized way, as number of fledglings could not always be recorded at the same breeding stage. However, in different samples from several years and the same area, clutch size has been found to be highly positively correlated (> 0·85) with number of fledglings, as expected based on very low mortality in barn swallow broods (e.g. Boncoraglio, Caprioli & Saino 2009; see also Møller 1994; Cramp 1998; see also above).

Statistical Analyses

We used accelerated failure time (AFT) and frailty models to investigate variation in longevity in relation to hatching date, brood size and nestling phenotype (covariates), cohort (=year of birth; multilevel factor) and sex (binary factor) (see Data S1). In the models, we entered the phenotypic values of individual recruits relative to their brood’s mean and also the mean phenotypic value of the brood as a covariate. Hence, an effect of relative phenotypic values implies that the phenotypic quality of an offspring relative to its siblings predicts longevity independently of average phenotypic quality of the brood. Conversely, a significant effect of the mean brood value while accounting for relative phenotypic quality would imply that offspring of higher absolute quality are more viable (see Van de Pol & Wright 2009 for a discussion of within- vs. between-broods effects). We assumed a Weibull distribution of longevity (D) because the models with a gamma distribution often failed to converge and alternative distributions of D provided a poorer fit. The σ parameter in the models (see Data S1) accounts for any change in error variance, so that when σ > 1 the instantaneous risk (hazard) of death decreases with time, when 0·5 < σ < 1·0 the hazard of death increases at a decreasing rate, while 0 < σ < 0·5 indicates that the hazard of death increases at an increasing rate. Cox regression models provided a poorer fit of longevity data. Because breeding phenology of the population may vary among years depending on ecological conditions (e.g. weather), relative hatching date (i.e. the difference between hatching date of the focal swallow and the population mean in that year) rather than absolute hatching date may be seen as a better indicator of the conditions under which an individual was reared. We thus re-ran the model of longevity using relative hatching date. In models of longevity in relation to offspring phenotypic traits, inclusion of the effect of age at measurement did never alter the quality of the results (i.e. the statistically significant or, respectively, nonsignificant effects remained such).

Because spatial heterogeneity has been acknowledged with a major role in determining population dynamics and viability (e.g. Bearhop, Ward & Evans 2003) and breeding habitat apparently varies in quality among barn swallow colonies (see above), we also used a frailty modelling approach to test for spatial structuring in longevity (e.g. Fox et al. 2006). Briefly, frailty terms modelling accounts for sources of variation due to unmeasured covariates by including a ‘random’ term which statistically accounts for intragroup dependence in hazard (see Fox et al. 2006).

In all models we accounted for right censoring of some (5·7%) observations. The 157 recruits that represent the overall sample of birds included in the study were derived from 148 different broods, implying that data dependence due to kinship was negligible. All analyses were run using PROC LIFETEST, LIFEREG and NLMIXED in SAS 9.2 (Allison 2010).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

The dataset included 157 (131 males; 26 females) recruits. Longevity data for nine individuals were right-censored (see Methods). The proportion of male recruits largely and significantly exceeded the null expectation based on an even nestling sex ratio (see Saino, Martinelli & Romano 2008), and this was the case when all recruits (goodness-of-fit inline image = 70·22, < 0·001) and when only local recruits (goodness-of-fit inline image = 66·73, < 0·001) were considered.

There was no significant difference in longevity between males and females in an AFT model where the effect of sex was entered as the only predictor (inline image = 0·34, = 0·559). Comparison of the survivor functions by the actuarial method again provided no evidence for sex-related variation (Wilcoxon test; inline image = 0·01, = 0·913) (Fig. 1a). In addition, while local recruits (119 males; 22 females) had somewhat reduced longevity compared to emigrants (12 males; 4 females) (Fig. 1b), the difference between the two groups was statistically nonsignificant (inline image = 2·72, = 0·099), and the same held true (inline image = 2·75, = 0·097) when we controlled for the effect of sex.

image

Figure 1.  Survivor functions and 95% confidence limits for a) male (= 131) and female (= 26) recruits and b) local (= 141) or emigrant (= 16) recruits. Age 1 year is the first spring after that of birth, when the individuals were recovered as recruits. Few individuals (= 9; 5·7%) with right-censored observations are not shown to improve graphical clarity.

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Longevity significantly declined with hatching date, with no significant differences between sexes (Table 1; Fig. 2a). The parameter estimated for hatching date (Table 1) yields a reduction in longevity of 0·58 years for an increase in hatching date of 2 standard deviations (1 SD = 18 days). In turn, 0·58 years correspond to c. 50% of life expectancy estimated at age 1. The Weibull scale parameter (σ) comprised between 0·5 and 1 (Table 1) implies that the hazard of death was increasing with time but at a decreasing rate. When we ran the model in Table 1 with relative hatching date (see Statistical Analyses) as a predictor, the results were qualitatively similar (effect of relative hatching date: inline image = 19·94, < 0·001, coefficient = −0·017 (0·004); sex: inline image = 0·85, = 0·36).

Table 1.   Weibull accelerated failure time (AFT) models of longevity in relation to hatching date or relative individual phenotype, expressed as deviation from the brood mean. In the models with offspring phenotype, within-brood mean was also included as a covariate. Log-likelihood values are given for the model with main effects only (first value for each variable), for the model also including the interaction between phenotypic value and sex (second value), or for the null model. Differences in deviance between the three models are also given. χ2 and P-values of main effects refer to the model excluding the interaction, except for body mass where the interaction was significant
AFT model−2 log likelihoodd.f.DevianceResidual d.f.Wald χ2 P
  1. Sample size of recruits was as follows: hatching date: 157; tarsus length: 114; body mass: 115; immune response: 87. Range of σ values was 0·693–0·754.

  2. aCoefficient from the model including main effects only = −0·0164 (0·0033 SE).

  3. bCoefficient for males = −0·036 (0·087 SE), χ2 = 0·17, = 0·681; females = 0·470 (0·193 SE), χ2 = 4·96, = 0·015.

  4. cCoefficient from the model including main effects only = 0·641 (0·238 SE).

Hatching datea359·42121·6215424·85<0·001
Sex 1  0·460·497
Hatching date × sex359·1710·251530·250·614
 Null381·04     
Relative tarsus length275·0111·651100·040·833
Sex 1  0·350·557
Mean brood tarsus length 1  1·570·210
Relative tarsus length × sex273·1211·891091·800·180
 Null276·66     
Relative body mass274·7212·271104·000·046
Sex 1  1·830·176
Mean brood body mass 1  2·870·090
Relative body mass × sexb268·7415·981106·020·014
 Null276·99     
Relative immune responsec195·55110·73837·240·007
Sex 1  0·010·909
Mean brood immune response 1  2·890·089
Relative immune response × sex194·1411·41821·230·268
 Null206·281    
image

Figure 2.  Mean (+SE) hatching date (a) or T cell-mediated immune response (b) of recruits with different longevity relative to their siblings. Immune response data are expressed as deviation from the mean of the brood to which the individual recruits belonged. Hence, negative values indicate that a recruit’s immune response was smaller, whereas positive values indicate that it was larger than that of its siblings. Longevity = 1 indicates the individuals that died between their first (=age 1 year) and second (=age 2 years) breeding seasons. Longevity 2 indicates individuals that died between age 2 and 3, and so forth. Numbers above bars are sample sizes. The nine censored individuals are excluded from the calculations.

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In AFT models (see Table 1), mean brood phenotypic values were never found to significantly predict longevity. In the same models, relative tarsus length did not significantly predict longevity. However, relative body mass had a differential effect on longevity of either sex, as females but not males benefited from being large relative to their siblings (Table 1). Moreover, nestlings that had large immune response relative to their siblings enjoyed significantly larger longevity, independently of sex (Fig. 2b). An inspection of Fig. 2b clearly shows that high immune response differentiated the individuals that survived up to age 2 years or more from those that did not. Hence, the results from the models including both relative and mean brood phenotypic values imply that recruits’ relative but not absolute phenotypic values predicted longevity. Simplified models relating longevity to offspring-relative phenotypic values confirmed the results in Table 1 (details not shown for brevity). Similarly, models relating longevity to absolute phenotypic values always confirmed the lack of effect on longevity (details not shown for brevity). Brood size did not predict longevity either per se or in combination with the effect of sex (> 0·88 in both tests; other details not shown).

An AFT model simultaneously including the main terms of sex and all the covariates accounting for relative individual phenotypic values listed in Table 1 and brood size confirmed the significant negative effect of hatching date (inline image = 14·00, < 0·001) as well as the positive effect of immune response (inline image = 4·94, = 0·026) on longevity in a subset of 83 individuals for which information on all traits was available.

When we scrutinized the data for any cohort effect, in an AFT model there was no effect on longevity (inline image = 12·12, = 0·518). Moreover, in different models longevity of different cohorts was not differentially affected by hatching date (interaction: inline image = 16·03, = 0·140), relative tarsus length (inline image = 13·61, = 0·192), body mass (inline image = 10·29, = 0·415) or immune response (inline image = 7·50, = 0·585). Hence, the effects of hatching date and immunity on longevity were consistent among cohorts.

Finally, we investigated structured heterogeneity of longevity data in frailty models including sex and hatching date and the frailty term of colony of origin. Inclusion of farm of origin caused a reduction in deviance of 53·1 (residual deviance = 306·3) compared to the model including sex and hatching date only (see also Table 1). Hence, there was large spatial variance in longevity at the among-colonies level.

In a subsample of 45 males, LRS could be measured. As expected from the negative relationship between hatching date and longevity, and the positive effect of age on number of clutches laid per season (see Methods), there was a significant negative relationship between LRS and hatching date in a linear regression analysis (F1,43 = 9·76, = 0·003, coefficient = −0·20 (0·07); Fig. 3). The sample of nine females was too small to be amenable to statistical analysis.

image

Figure 3.  Lifetime reproductive success (=total lifetime number of eggs in their nests) in relation to hatching date of 45 male recruits. Line is fitted by simple regression analysis.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Longevity shows considerable variation within populations of organisms, but there is little knowledge of the mechanism that may operate early in life in producing such variation (Cam, Monnat & Hines 2003; Van de Pol et al. 2006; Ricklefs & Cadena 2008; Wilkin & Sheldon 2009; Bouwhuis et al. 2010a,b). Long-term consequences of perinatal conditions on longevity are indeed to be expected, however, given the importance of environmental and early maternal effects in shaping offspring life history (see Introduction).

We thus investigated longevity of barn swallows and found that it declined with hatching date, independently of any cohort effect. Moreover, we could show for the first time in any bird species that nestlings that mounted an intense T cell-mediated immune response relative to their siblings and female nestlings that were high in the size/age brood hierarchy had larger longevity. Our study focused on longevity of individuals that had reached sexual maturity, thus by-passing the effect of intense selection during the first year of life (e.g. Møller 1994; Turner 2006; Grüebler & Naef-Daenzer 2008). Importantly, hatching date negatively predicted LRS, although this relationship could be tested only in males due to small sample size of females, which ultimately depends on heavy sex bias in natal dispersal distance. Such negative relationship between LRS and hatching date could be expected based on the observed negative relationship between longevity and hatching date. In fact, most barn swallows have a single clutch in their first breeding season, whereas most individuals have two (seldom three) clutches per breeding season when two- or more years old. Thus, broodedness increases with age in this species where more than 80% of the individuals that reach sexual maturity have only two breeding seasons (see Fig. 1). Moreover, variance in clutch size is relatively small (see Methods). Finally, more than 90% of the individuals breed every year (our unpublished data; see also Møller 1994). Hence, a major mechanism accounting for variation in Darwinian fitness according to longevity is larger broodedness of older individuals. As reduction in longevity and LRS with hatching date was marked, present results imply that selection for early breeding is intense.

Birds at temperate latitudes experience seasonal worsening of environmental conditions during the breeding season (Lack 1950; Turner 2006; see Introduction), which can cause a progressive deterioration of offspring quality and viability (Newton 1989; Møller 1994; Grüebler & Naef-Daenzer 2008). Constraints on early breeding set by migration schedule, particularly on European trans-Saharan migrants like the barn swallow (McNamara & Houston 2008; Newton 2008; Møller, Fiedler & Berthold 2010), may exacerbate these negative seasonal effects, with long-term repercussions on viability after sexual maturation. In addition to extrinsic factors, the phenotypic quality of parents may also decline late in the breeding season. In fact, conditions experienced during wintering and migration, which are known to predict interannual variation in spring arrival date and breeding performance of barn swallows (Saino et al. 2004), may carry-over to affect physiological state of individuals that adopt different migration strategies, generating variance in parental quality. Because individuals in prime condition arrive and thus breed early (Møller 1994), a decline in longevity with hatching date may reflect a negative covariation between parental quality and arrival/breeding date. Overall, the negative relationship between longevity and hatching date is compatible both with an effect of parental quality and of seasonal effects, and these two alternative sources of variation may be difficult to tease apart, because quality of adults and their breeding date may be strongly correlated, and the flow of causation between these variables may be ancipital. Indeed, low parental quality may entail a late breeding because, for example, it causes a late arrival. Conversely, adults that for any reason unrelated to their inherent quality are forced to breed late under relatively adverse conditions may, because of this, perform poorly at parental duties. Two lines of evidence, however, suggest that parental age/quality was unlikely to be the major (or sole) determinant of variation in offspring longevity. First, two- or more years old adults breed earlier but offspring quality declines already after the first or second year of life (Møller 1994; Saino et al. 2002b). Second, we observed that relative rather than absolute phenotypic values of the offspring predicted longevity. Hence, within-brood rather than among-broods (and thus among-parents) variation in offspring quality affects longevity.

The specific mechanisms that cause a decline in longevity with hatching date are a matter of speculation. Egg quality is a candidate as a vector of long-term maternal effects on longevity (Beamonte-Barrientos et al. 2010). Biochemical egg quality in birds can vary seasonally (López-Rull, Salaberria & Gil 2010), and experiments have disclosed short-term effects of egg quality on offspring phenotype but also ‘developmentally entrenched’ (see Badyaev 2008) long-term effects of egg antioxidants, immune factors and maternal hormones which carry-over into adulthood (Groothuis et al. 2005; Badyaev et al. 2006; Rubolini et al. 2007; Bonisoli-Alquati et al. 2011). In mammals, prenatal and early postnatal exposure to low-quality diets is causally linked to ageing and longevity (Sayer et al. 2001). The quality and amount of food received during the pre- and postfledging stages, when development of some physiological functions (e.g. immunity) is still under way, is an obvious additional candidate actor of maternal effects on longevity (De Kogel 1997). Other mechanisms may involve seasonal variation in parasitism or carry-over effects on autumn migration, which may in turn impose viability costs later in life (Mërila & Svensson 1997; Fitze, Clobert & Richner 2004). In addition, antioxidant protection strongly predicts annual survival of barn swallows (Saino et al. 2011; see Bize et al. 2008) and may decline seasonally (Costantini, Carello & Fanfani 2010). Poor egg or dietary antioxidants supply can have long-lasting detrimental effects on antioxidant absorption and protection from oxidative damage later in life (Monaghan, Metcalfe & Torres 2009). Hence, impaired antioxidant defence is a potential mechanism linking hatching date to longevity.

Nestlings with superior immunity and body mass (females only) relative to their siblings enjoyed larger longevity, suggesting that prevailing in brood competition for food has long-term, besides obvious short-term, effects on viability (Mock & Parker 1997). In barn swallow broods, even small hatching asynchrony determines a size/age hierarchy that is consistently retained throughout the nestling period. Present results thus highlight the long-term positive fitness consequences of hatching early relative to siblings and acquiring a dominant position in the size hierarchy (Ricklefs 1993) particularly for females, which are competitively inferior to males in barn swallow broods (Boncoraglio, Martinelli & Saino 2008). Because functioning of the immune system is strongly dependent on nutritional conditions (Klasing 2007), a positive effect of immune response on longevity may also reflect the general consequences of nutrition on viability. A positive effect of T cell-mediated immune response and body mass on longevity after sexual maturation is consistent with the observation that these traits predict local recruitment in several birds (e.g. Møller & Saino 2004; Cleasby et al. 2010; López-Rull et al. 2011). A differential effect of rearing conditions on longevity and breeding success has been observed also in great tits (Parus major), where males but not females benefitted from being raised under benign conditions (Wilkin & Sheldon 2009). In the present study, females, not males, benefitted from ranking high in the brood size/age hierarchy, possibly because position in the hierarchy is more critical to the competitively inferior females.

Sex ratio of barn swallow nestlings is c. 1:1, though with some interannual variation (Saino, Martinelli & Romano 2008). Similarity in longevity of adult males and females observed here therefore suggests that male-biased tertiary sex ratio is caused by larger mortality of females during the first year of life. An alternative, though unlikely, explanation is that the postnatal dispersal/immigration balance differs between sexes in the population we studied.

Dispersal did not predict longevity, consistently with observations on Danish swallows, but in contrast with the reduced viability of male emigrants in Spain (Balbontín et al. 2009; see Bouwhuis et al. 2010b). If anything, emigrants had nonsignificantly larger longevity, implying that viability costs of dispersal vary geographically. However, we caution that the analyses of dispersal concerned a small number of emigrants, reducing the power of the statistical test.

Much of the variance in longevity remained unexplained by offspring traits. This is not a surprise because barn swallows are long-distance migrants on which sources of mortality unrelated to perinatal conditions likely operate. Inclusion of the frailty effect of colony of origin, however, led to a considerable reduction in the model’s deviance, again stressing the importance of rearing conditions in determining longevity. Spatially structured heterogeneity in longevity has consequences for analyses of population trends and viability (see Bearhop, Ward & Evans 2003). The barn swallow is a common farmland species whose populations have markedly declined throughout Europe (BirdLife International 2004) as well as in our study area (−8·4% year−1; Ambrosini et al. 2012). Present results demonstrate that spatial heterogeneity in a major demographic trait is large and may need to be incorporated in analyses of demographic trends.

In conclusion, this is the first study of birds we are aware of showing that longevity after sexual maturity depends on hatching date and on phenotypic quality of nestlings relative to brood mates, although other studies have provided evidence for effects of rearing conditions on LRS and longevity. This supports the idea that early environmental and maternal effects mediated by decisions on the time of breeding and resource allocation can have long-term consequences on major fitness trait such as longevity after sexual maturation and LRS. Although their mechanisms are unknown, these effects afford a link translating parental reproductive decisions into variation in population demographic parameters and viability. Finally, we showed that spatial structuring in longevity exists at the inter-colony level, which may need to be incorporated into demographic models of this declining bird.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

We thank several people who helped in the field and the farmers who allowed us to regularly visit their farms for so many years.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
  • Allison, P.D. (2010) Survival Analysis Using SAS. SAS Institute Inc., Cary, NC.
  • Alonso-Alvarez, C., Bertand, S., Devevey, G., Prost, J., Faivre, B., Chastel, O. & Sorci, G. (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution, 60, 19131924.
  • Ambrosini, R., Bolzern, A.M., Canova, L., Arieni, S., Møller, A.P. & Saino, N. (2002) The distribution and colony size of barn swallows in relation to agricultural land use. Journal of Applied Ecology, 39, 524534.
  • Ambrosini, R., Rubolini, D., Trovò, P., Liberini, G., Bandini, M., Romano, A., Sicurella, C., Scandolara, C., Romano, M. & Saino, N. (2012) Maintainance of livestock farming may buffer population decline of the Barn Swallow Hirundo rustica. Bird Conservation International (in press) doi: 10.1017/S0959270912000056.
  • Badyaev, A.V. (2008) Maternal effects as generators of evolutionary change: a reassessment. The Year in Evolutionary Biology 2008 (eds C.D. Schlichting & T.A. Mousseau), pp. 151161, Wiley-Blackwell, New York.
  • Badyaev, A.V. & Uller, T. (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philosophical Transactions of the Royal Society of London B, 364, 11691177.
  • Badyaev, A.V., Acevedo Seaman, D., Navara, K.G., Hill, G.E. & Mendonca, M.T. (2006) Evolution of sex-biased maternal effects in birds: III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins. Journal of Evolutionary Biology, 19, 10441057.
  • Balbontín, J., Møller, A.P., Hermosell, I.G., Marzal, A., Reviriego, M. & de Lope, F. (2009) Geographic patterns of natal dispersal in barn swallows Hirundo rustica from Denmark and Spain. Behavioral Ecology and Sociobiology, 63, 11971205.
  • Beamonte-Barrientos, R., Velando, A., Drummond, H. & Torres, R. (2010) Senescence of maternal effects: aging influences egg quality and rearing capacities of a long-lived bird. The American Naturalist, 175, 469480.
  • Bearhop, S., Ward, R.M. & Evans, P.R. (2003) Long-term survival rates in colour-ringed shorebirds – practical considerations in the application of capture-recapture models. Bird Study, 50, 271279.
  • BirdLife International (2004) Birds in Europe: Population Estimates, Trends and Conservation Status. BirdLife International, Cambridge.
  • Bize, P., Devevey, G., Monaghan, P., Doligez, B. & Christe, P. (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology, 89, 25842593.
  • Boncoraglio, G., Caprioli, M. & Saino, N. (2009) Fine-tuned modulation of competitive behaviour according to kinship in barn swallow nestlings. Proceedings of the Royal Society of London B, 76, 21172123.
  • Boncoraglio, G., Martinelli, R. & Saino, N. (2008) Sex-related asymmetry in competitive ability of sexually monomorphic barn swallow nestlings. Behavioral Ecology and Sociobiology, 62, 729738.
  • Boncoraglio, G. & Saino, N. (2008) Barn swallow chicks beg more loudly when broodmates are unrelated. Journal of Evolutionary Biology, 21, 256262.
  • Bonisoli-Alquati, A., Matteo, A., Ambrosini, R., Rubolini, D., Romano, M., Caprioli, M., Dessì-Fulgheri, F., Baratti, M. & Saino, N. (2011) Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant. Hormones and Behavior, 59, 7582.
  • Bouwhuis, S., Charmentier, A., Verhulst, S. & Sheldon, B.C. (2010a) Individual variation in rates of senescence: natal origin effects and disposable soma in a wild bird population. Journal of Animal Ecology, 79, 12511261.
  • Bouwhuis, S., Charmentier, A., Verhulst, S. & Sheldon, B.C. (2010b) Trans-generational effects on ageing in a wild bird population. Journal of Evolutionary Biology, 23, 636642.
  • Cam, E., Monnat, J.-Y. & Hines, J.E. (2003) Long-term fitness consequences of early conditions in the kittiwake. Journal of Animal Ecology, 72, 411424.
  • Carere, C. & Baltazhart, L. (2007) Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends in Endocrinology and Metabolism, 18, 7380.
  • Cleasby, I.R., Nakagawa, S., Gillespie, D.O.S. & Burke, T. (2010) The influence of sex and body size on nestling survival and recruitment in the house sparrow. Biological Journal of the Linnean Society, 101, 680688.
  • Costantini, D., Carello, L. & Fanfani, A. (2010) Relationships among oxidative status, breeding conditions and life-history traits in free-living Great Tits Parus major and Common Starlings Sturnus vulgaris. Ibis, 152, 793802.
  • Cramp, S. (1998) The Complete Birds of the Western Palearctic on CD-ROM. Oxford University Press, Oxford.
  • De Kogel, C.H. (1997) Long-term effects of brood size manipulation on morphological development and sex-specific mortality of offspring. Journal of Animal Ecology, 66, 167178.
  • Dubiec, A. & Cichoñ, M. (2001) Seasonal decline in health status of Great Tit (Parus major) nestlings. Canadian Journal of Zoology, 79, 18291833.
  • Eising, C.M., Eikenaar, C., Schwabl, H. & Groothuis, T.G.G. (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proceedings of the Royal Society of London B, 268, 839846.
  • Fitze, P.S., Clobert, J. & Richner, H. (2004) Long-term life-history consequences of ectoparasite-modulated growth and development. Ecology, 85, 20182026.
  • Fox, G.A., Kendall, B.E., Fitzpatrick, J.W. & Woolfenden, G.E. (2006) Consequences of heterogeneity in survival probability in a population of Florida scrub-jays. Journal of Animal Ecology, 75, 921927.
  • Grant, P.R. & Grant, B.R. (2011) Causes of lifetime fitness of Darwin’s finches in a fluctuating environment. Proceedings of the National Academy of Sciences of the United States of America, 108, 674679.
  • Groothuis, T.G.G., Muller, W., von Engelhardt, N., Carere, C. & Eising, C. (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience Biobehavioral Reviews, 9, 329352.
  • Groothuis, T.G.G., Eising, C.M., Blount, J.D., Surai, P., Apanius, V., Dijkstra, C. & Müller, W. (2006) Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. Journal of Evolutionary Biology, 19, 13041313.
  • Grüebler, M.U. & Naef-Daenzer, B. (2008) Fitness consequences of pre- and post-fledging timing decisions in a double-brooded passerine. Ecology, 89, 27362745.
  • Hall, M.E., Blount, J.D., Forbes, S. & Royle, N.J. (2010) Does oxidative stress mediate the trade-off between growth and self-maintenance in structured families. Functional Ecology, 24, 365373.
  • Klasing, K.C. (2007) Nutrition and the immune system. British Poultry Science, 48, 525537.
  • Lack, D. (1950) The breeding seasons of European birds. Ibis, 92, 288316.
  • Lack, D. (1954) The Natural Regulation of Animal Numbers. Clarendon Press, Oxford.
  • Liker, A. & Székely, T. (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evolution, 59, 890897.
  • Lindström, J. (1999) Early development and fitness in birds and mammals. Trends in Ecology and Evolution, 14, 343348.
  • López-Rull, I., Salaberria, C. & Gil, D. (2010) Seasonal decline in egg size and yolk androgen concentration in a double brooded passerine. Ardeola, 57, 321332.
  • López-Rull, I., Celis, P., Salaberria, C., Puerta, M. & Gil, D. (2011) Post-fledging recruitment in relation to nestling plasma testosterone and immunocompetence in the spotless starling. Functional Ecology, 25, 500508.
  • McNamara, J.M. & Houston, A. (2008) Optimal annual routines: behaviour in the context of physiology and ecology. Philosophical Transactions of the Royal Society of London B, 363, 301319.
  • Mërila, J. & Svensson, E. (1997) Are fat reserves in migratory birds affected by condition in early life? Journal of Avian Biology, 28, 279286.
  • Mock, D.W. & Parker, G.A. (1997) The Evolution of Sibling Rivalry. Oxford University Press, Oxford.
  • Møller, A.P. (1994) Sexual Selection and the Barn Swallow. Oxford University Press, Oxford.
  • Møller, A.P., Fiedler, W. & Berthold, P. (2010) (eds) Effects of Climate Change on Birds. Oxford University Press, Oxford.
  • Møller, A.P. & Saino, N. (2004) Immune response and survival. Oikos, 104, 299304.
  • Monaghan, P., Metcalfe, N.B. & Torres, R. (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters, 12, 7592.
  • Mousseau, T.A. & Fox, C.W. (1998) (eds) Maternal Effects as Adaptations. Oxford University Press, Oxford.
  • Muller, W., Lessells, C.M., Kortsen, P. & von Engelhardt, N. (2007) Manipulative signals in family conflict? On the function of maternal yolk hormones in birds. The American Naturalist, 169, e84e96.
  • Naef-Daenzer, B., Widmer, F. & Nuber, M. (2001) Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. Journal of Animal Ecology, 70, 730738.
  • Newton, I. (1989) Lifetime Reproduction in Birds. Academic Press, London.
  • Newton, I. (1998) Population Limitation in Birds. Academic Press, London.
  • Newton, I. (2008) The Migration Ecology of Birds. Academic Press, London.
  • Reid, J.M., Bignal, E.M., Bignal, S., McCracken, D.I. & Monaghan, P. (2003) Environmental variability, life-history covariation and cohort effects in the red-billed cough Pyrrhocorax pyrrhocorax. Journal of Animal Ecology, 72, 3646.
  • Ricklefs, R.E. (1993) Sibling competition, hatching asynchrony, incubation period, and lifespan in altricial birds. Current Ornithology (ed. D.M. Power), Vol. 11, pp. 199276. Plenum Press, New York.
  • Ricklefs, R.E. & Cadena, C.D. (2008) Heritability of longevity in captive populations of nondomesticated mammals and birds. Journal of Gerontology, 5, 435446.
  • Rubolini, D., Romano, M., Martinelli, R., Leoni, B. & Saino, N. (2006) Effects of prenatal androgens on armaments and ornaments of the ring-necked pheasants. Behavioral Ecology and Sociobiology, 59, 549560.
  • Rubolini, D., Martinelli, R., von Engelhardt, N., Romano, M., Groothuis, T.G.G., Fasola, M. & Saino, N. (2007) Consequences of prenatal androgen exposure for the reproductive performance of female pheasants (Phasianus colchicus). Proceedings of the Royal Society of London B, 274, 137142.
  • Saino, N., Calza, S. & Møller, A.P. (1997) Immunocompetence of nestling barn swallows (Hirundo rustica) in relation to brood size and parental effort. Journal of Animal Ecology, 66, 827836.
  • Saino, N., Martinelli, R. & Romano, M. (2008) Ecological and phenological covariates of offspring sex ratio in barn swallows. Evolutionary Ecology, 22, 659674.
  • Saino, N., Calza, S., Ninni, P. & Møller, A.P. (1999) Barn swallows trade survival against offspring condition and immunocompetence. Journal of Animal Ecology, 68, 9991009.
  • Saino, N., Ferrari, R.P., Romano, M., Ambrosini, R. & Møller, A.P. (2002a) Ectoparasites and reproductive trade-offs in the barn swallow (Hirundo rustica). Oecologia, 133, 139145.
  • Saino, N., Ambrosini, R., Martinelli, R. & Møller, A.P. (2002b) Mate fidelity, senescence in breeding performance, and reproductive trade-offs in the barn swallow. Journal of Animal Ecology, 71, 309319.
  • Saino, N., Ferrari, R.P., Romano, M., Martinelli, R. & Møller, A.P. (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proceedings of the Royal Society of London B, 270, 24852489.
  • Saino, N., Szép, T., Ambrosini, R., Romano, M. & Møller, A.P. (2004) Ecological conditions during winter affect sexual selection and breeding in a migratory bird. Proceedings of the Royal Society of London B, 271, 681686.
  • Saino, N., Ferrari, R.P., Romano, M., Martinelli, R., Lacroix, A., Gil, D. & Møller, A.P. (2006) Maternal allocation of androgens and antagonistic effect of yolk androgens on son and daughters. Behavioral Ecology, 17, 172181.
  • Saino, N., Caprioli, M., Romano, M., Boncoraglio, G., Rubolini, D., Ambrosini, R., Bonisoli-Alquati, A. & Romano, A. (2011) Antioxidant defences predict long-term survival in a passerine bird. PLoS ONE, 6, e19593.
  • Sayer, A.A., Dunn, R., Langley-Evans, S. & Cooper, C. (2001) Prenatal exposure to a maternal low protein diet shortens life span in rats. Gerontology, 47, 914.
  • Schlichting, C.D. & Mousseau, T.A. (2009) (eds). The Year in Evolutionary Biology 2008. Wiley-Blackwell, New York.
  • Stenning, M.J. (1996) Hatching asynchrony, brood reduction and other rapidly reproducing hypotheses. Trends in Ecology and Evolution, 11, 243246.
  • Tella, J.L., Lemus, J.A., Carrete, M. & Blanco, G. (2008) The PHA test reflects acquired T-cell mediated immunocompetence in birds. PLoS ONE, 9, e3295.
  • Tschirren, B., Fitze, P.S. & Richner, R. (2003) Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. Journal of Animal Ecology, 72, 839845.
  • Turner, A. (2006) The Barn Swallow. T & AD Poyser, London.
  • Van de Pol, M. & Wright, J. (2009) A simple method for distinguishing within- versus between-subject effects using mixed models. Animal Behaviour, 77, 753758.
  • Van de Pol, M., Bruinzeel, L.W., Heg, D., van der Jeugd, H.P. & Verhulst, S. (2006) A silver spoon for a golden future: long-term effects of natal origin on fitness prospect of oystercatchers (Haematopus ostralegus). Journal of Animal Ecology, 75, 616626.
  • Verboven, N. & Visser, M.E. (1998) Seasonal variation in local recruitment of great tits: the importance of being early. Oikos, 81, 511524.
  • Verhulst, S. & Nilsson, J.A. (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Proceedings of the Royal Society of London B, 363, 399410.
  • Wilkin, T.A. & Sheldon, B.C. (2009) Sex differences in the persistence of natal environmental effects on life histories. Current Biology, 19, 19982002.
  • Williams, G.C. (1992) Natural Selection. Oxford University Press, Oxford.
  • Wolf, J.B. & Wade, M.J. (2009) What are maternal effects (and what are not)? Philosophical Transactions of the Royal Society of London B, 364, 11071115.

Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Data S1. General methods.

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