Behavioral Ecology Advance Access originally published online on June 12, 2007
Behavioral Ecology 2007 18(4):781-791; doi:10.1093/beheco/arm045
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Intra- and interspecific relationships between nest size and immunity
a Departamento de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (CSIC), General Segura 1, E-04001 Almería, Spain b Departamento de Biología Animal, Universidad de Granada, E-18071 Granada, Spain c Laboratoire de Parasitologie Evolutive, Université Pierre et Marie Curie (CNRS), Bâtiment A, 7ème étage, 7 quai St Bernard, Case 237, FR-75252 Paris Cedex 05, France
Address correspondence to J.J. Soler: jsoler{at}eeza.csic.es.
Received 22 January 2007; revised 11 April 2007; accepted 18 April 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1APPENDIX 2REFERENCES |
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Nest-building behavior has been suggested to represent a postmating sexually selected signal in passerine birds, an hypothesis that has received both comparative and experimental support. Because selection pressure due to parasites and diseases should be particularly high during nest building, mainly due to energetic costs and depression of the immune system associated with this reproductive phase, we predicted a positive association between nest-building effort and immunity. Nest-building effort would reflect the ability to produce efficient immune responses of builders only if individuals with a superior immune system would display exaggerated nest-building effort. We tested this prediction by studying the relationship between volume of nest material used for nest construction and, at the intraspecific level, estimates of innate humoral immune response in barn swallows Hirundo rustica. At the interspecific level, we used responses to the mitogenic phytohemagglutinin as an indicator of adaptive immune response of European passerine species. As predicted, we found, after controlling for several potential confounding factors, that volume of nest material was positively related to immune response both at the intra- and at the interspecific level. Alternative hypotheses explaining the comparative results are discussed.
Key words: innate humoral immunity, nest building, PHA response, postmating sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1APPENDIX 2REFERENCES |
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Nest-building behavior has been proposed to have a sexually selected component, and, therefore, nest size may be a postmating sexually selected signal, as shown by comparative (Soler JJ, Møller, and Soler M 1998) and experimental studies (e.g., Soler et al. 2001
). Nest-building effort by one sex (e.g., male) would reliably inform individuals of the other sex (e.g., female) about willingness to invest in reproduction, causing the latter to adjust its reproductive effort accordingly (Soler JJ, Møller, and Soler M 1998). Nest-building behavior is costly not only because of the associated energetic and time demands (Hansell 2000) but also because of increased predation risk during nest building (Collias NE and Collias EC 1984). An important additional cost of nest building is caused by parasites because susceptibility to parasitism potentially increases with increasing energy demand for nest building (e.g., Hillgarth and Wingfield 1997; Møller 1997). In addition, susceptibility to parasitism should be particularly elevated during nest building because the peak of immunosuppressive hormones (e.g., testosterone) occurs during this stage (Logan and Wingfield 1995; Johnsen 1998; Elekonich and Wingfield 2000; Foerster et al. 2002; Hirschenhauser et al. 2003; Van Duyse et al. 2003 ). Therefore, selection due to parasites should be most important during the nest-building phase. Consequently, parasitism and antiparasite defences such as immunity should explain nest-building behavior and/or nest size characteristics not only because nests are the environment where some parasites live (Hansell 2000) but also due to the energetic costs or the high levels of immunosuppressive hormones associated with nest building.
An important defence against parasites is the immunity, which by discriminating between self and nonself material, allows defence of hosts against parasites (e.g., Wakelin 1996; Playfair and Bancroft 2004). The immune system should have evolved to cope with the risk of parasitism causing a balance between costs and benefits of immune defence, with host species experiencing the highest risks of parasitism having evolved the strongest immune systems (e.g., Møller and Erritzøe 1996; Møller et al. 2001). In general, immunity is considered important in sexual selection because, for instance, choosy females may gain parasite-resistance genes for their offspring from the most ornamented and hence most resistant males (e.g., Hamilton and Zuk 1982; Read 1988; Zuk 1992; Westneat and Birkhead 1998; Møller et al. 1999). Such female preferences for males with extravagant trait expression would thus predict a positive relationship between the expression of sexual traits and level of immunity (Garamszegi et al. 2003). Parasites may influence the expression of secondary sexual characters through the interaction of parasites and immunosuppressive hormones (such as testosterone) (Folstad and Karter 1992) either directly, because both parasites and hormones affect the expression of sexual traits, or indirectly through the immune system of the host, because both parasites and hormones affect the immune system, which is therefore related to the exaggeration of sexually selected traits (Hillgarth and Wingfield 1997). In any case, following condition-dependent handicap models of sexual selection (Zahavi 1975, 1977; Andersson 1986; Iwasa and Pomiankowski 1991; Johnstone and Grafen 1992), only individuals with a high degree of resistance to parasites would be able to display high levels of a handicapping sexual signal.
Therefore, we predicted a positive relationship between nest-building effort and immunity of nest builders (Barber et al. 2001; Tomas et al. 2006). Here, we test this prediction in barn swallows (Hirundo rustica), a species for which there is evidence of nest building being a heritable and sexually selected trait of males (Soler, Cuervo, et al. 1998; Møller 2006). In addition, we use comparative methods with extensive information on level of immune response and nest size of 49 European bird species to investigate whether nest size is positively correlated with immunity among species.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1APPENDIX 2REFERENCES |
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Data collection
Barn swallow study
The study of barn swallows was performed during the breeding season of 2005 at Kraghede (57°12'N, 10°00'E), Denmark (for details, see Møller 1994
). The study site is an open farmland habitat with barn swallows breeding in barns and stables and only rarely elsewhere under bridges and in culverts. The fields and scattered trees around farms comprise most of the area, with the exception of a few plantations, ponds, ditches, and streams. The main crops are grass, barley, wheat, and potatoes. The range in altitude is 9–28 m a. s. l.
Adults were captured regularly in mist nets before the start of the breeding season until all adults in a given site had been captured. Because many barn swallow nests from previous years are refurbished and used during several years (Møller 1994), we 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 in order to clean their barns, thereby preventing nests from being old. Thus, in total, we used information from 82 males and 91 females pertaining to 112 different nests. We used volume of nest material in the analyses, as defined in Soler JJ, Møller, and Soler M (1998), as this variable should be more closely related to nest-building effort than any other variables related to nest size (Soler, Cuervo, et al. 1998). Moreover, we also collected information on laying date of swallows because it may be related to nest size (Soler, Cuervo, et al. 1998) but also to immune response (Sorci et al. 1997; Dubiec and Cichon 2005; Gasparini et al. 2006).
Interspecific study
Comparative data on nest size parameters were obtained from Niethammer (1937), Dementiev and Gladkov (1966), Haftorn (1971), and Cramp (1998). Volume of nest material estimated in Soler JJ, Møller, and Soler M (1998) was used as an estimate of nest-building effort. Moreover, we also collected information on variables that are known to affect nest size and/or level of immune response of birds. These were the sexes that build the nest (female or female and male), nest site (hole [hole nesting; value: 1], semihole [domed nests or open nests in covered sites; value: 2], and open [open nests in open locations; value: 3]), coloniality (scored either as solitary, between maximally 2 and 10 pairs per colony, between 11 and 100 pairs per colony, and more than 100 pairs per colony), clutch size from Perrins (1987), duration of nestling period from Perrins (1987) and Cramp (1998), and body mass from Perrins (1987), Cramp (1998), and Soler JJ, Møller, and Soler M (1998).
Independently of whether females, or males and females, are responsible for nest building, we used all species for which information on nest-building effort and immune response (see below) was available in our analyses. Partial correlation coefficients between nest material volume and level of PHA response (see later; after controlling for potential confounding variables) did not differ from each other (P = 0.81), independently of whether we only used species in which both males and females contribute to nest building (using phylogenetic independent contrasts, partial r = 0.206, N = 20) or whether we used species in which only females build nests (using phylogenetic independent contrasts, partial r = 0.277, N = 29). Because it is known that the number of sexes involved in nest building affects nest size (Soler JJ, Møller, and Soler M 1998), we included information on sexes involved in nest building in our analysis. Therefore, we statistically controlled our prediction not only for differential nest size due to sexes participating in nest building but also for the possibility of level of immune response being affected by sexes involved in nest building.
The data set is presented in Appendix 1.
Measures of immune responses
Estimation of NAbs and complement
For the intraspecific study with swallows, we used estimates of natural antibodies (here after NAbs) and complement, which correspond to constitutive innate humoral immunity and, apart of some behavioral protection (Hart 1990), represent the first line of defence against infections (e.g., Playfair and Bancroft 2004). We have fully reported the methods for these tests elsewhere (Møller and Haussy 2007). In brief, blood was collected from adult barn swallows by puncturing the brachial vein and collecting 2 heparinized capillaries of 75 µl blood that were stored in a cooling box at a temperature just above freezing. In the lab within a period of 2 h, we centrifuged the capillaries for 10 min. Plasma and cells were separated and stored at –20 °C until analysis in the lab.
To estimate the levels of circulating NAbs and complement, we used the procedure developed by Matson et al. (2005). The agglutination part of the assay estimates the interaction between NAbs and antigens in rabbit blood, producing blood clumping. The lysis part of the assay estimates the action of complement from the amount of hemoglobin released from the lysis of rabbit erythrocytes. Quantification of agglutination and lysis is achieved by serial dilution in polysterene 96-well assay plates, with the dilution step at which the agglutination or lysis reaction is stopped. We used fresh rabbit blood with Alsever's anticoagulant, 96 round well assay plates and an EPSON 4490 photo scanner that was set at professional mode, with document type color film, 48 bit color and 300 dpi.
Whole rabbit blood was stored at 4 °C. After determination of the level of hematocrit, we diluted to obtain a solution of 1% of erythrocytes. The protocol for hemolysis and hemagglutination is as follows: The plasma samples were thawed and homogenized using a vortex. Subsequently, 25 µl of plasma was pipetted into each column followed by addition of 25 µl of the solution in all wells. Subsequent wells contained a solution diluted by a factor 2 from a solution of 1 in 2 in the first well to a solution of 1 in 2048 in the 11th well. Well number 12 only contained the dilution of erythrocytes, thus serving as a negative control. Subsequently, 25 µl of the 1% solution of rabbit blood was added to all wells. The assay plate was then covered and shaken for 10 s followed by incubation for 90 min in a bath at 37 °C. The assay plate was then removed from the bath and left at an inclination of 45° at ambient temperature for 20 min. The assay plate was then read by C.H. and scanned. Scoring was based on negative wells having a small round agglutinate at the bottom thus forming a well-defined red round point and positive wells having a diffuse film at the bottom.
This was followed by placing the assay plate at ambient temperature for 70 min followed by assessment of lysis and scanning of the plate. The well is assumed to be positive when there is no sign of whole blood (the action of complement had destroyed the red blood cells and only left hemoglobin).
All tests were made blindly by C.H. with respect to the phenotype of the individual birds, with only an ID number being available. Repeat tests on 17 individuals on 2 different days showed that individual identity accounted for 73% of the variance for hemagglutination reaction (F16,17 = 3.31, r2 = 0.73, P = 0.0088). Similarly, repeat tests on 17 individuals on 2 different days showed that individual identity accounted for 82% of the variance for lysis (F16,17 = 5.36, r2 = 0.82, P = 0.0005).
We also tested for individual differences in scoring of scans of assay plates by A.P.M. assigning scores to 40 individuals blindly with respect to the first series of scores by C.H. Again, there was highly significant consistency in scores between the 2 scorers (hemagglutination: F39,40 = 406.97, r2 = 0.99, P < 0.0001; lysis: F39,40 = 16.18, r2 = 0.94, P < 0.0001).
Estimates of PHA response of different species
For the comparative analyses, we used values of skin swelling elicited by injection of the mitogen phytohemagglutinin (hereafter PHA response). This is commonly used in evolutionary ecology to estimate T-cell–mediated immunity, although it also reflects other components of the immune system such as major histocompatibility complex molecules (e.g., Goto et al. 1978; Martin et al. 2006).
During the breeding seasons 2000–2003, we spent large parts of April–June capturing adults and searching for nests of different species of passerines for which adults and nestlings were tested for PHA response. Adults with an enlarged incubation patch were released immediately to avoid reproductive failure. Nestlings were injected at a standard relative age during their ontogeny (when they were approximately 2 thirds through their normal nestling period) rather than at a similar absolute age (for a justification of this approach, see Møller et al. 2004). This was done in Southern Spain around Granada and Sierra Nevada and in Northern Denmark. We followed the standard protocol described in Lochmiller et al. (1993) and widely used in evolutionary ecology. Briefly, before injection, we removed the feathers from a small spot of skin on the wing web (patagium) of the right and the left wings and marked the sites of injection with a permanent, water-resistant color marker. We then measured the thickness of the skin to the nearest 0.01 mm with a pressure-sensitive calliper (Teclock SM112). For each wing web, we made 3 measurements to quantify measurement error. As in previous studies, we found highly repeatable measurements, with repeatabilities above 0.95. Subsequently, we injected 0.2 mg phytohemagglutinin dissolved in 0.04 ml physiological water in one wing web and 0.04 ml physiological water in the other wing web. Inflammatory responses to the injection were measured 6 h later in adults and 24 h later in nestlings. Difference in time response between adults and nestlings was due to the inability to recover adults after 24 h of injection, which were thus maintained in captivity. Although estimates of PHA response traditionally have been recorded 24 h after injection, we measured responses after 3, 6, 12, 24, 36, 48, and 72 h in a study of captive house sparrows Passer domesticus and found no significant increase after 6 h (Navarro et al. 2003). A study of chickens showed little evidence of change after an initial swelling (Goto et al. 1978). For 6 species (Delichon urbica, H. rustica, Cyanistes caeruleus, Parus major, P. domesticus, and Passer montanus) with response measured after 6 h and response measured on free-flying individuals after 24 h revealed a strongly positive correlation (Pearson r = 0.998, N = 6, P < 0.0001), with no significant increase in response after 6 h (paired t-test, t5 = 1.29, not significant; see Møller et al. 2003). Therefore, because our predictions concern covariation between relative level of immunity and nest-building effort, but not with absolute values, differences in duration of the period for immune response to develop in adults and nestlings would not affect our results.
The index of PHA response was simply calculated as the difference in thickness of the wing web injected with phytohemagglutinin after 6 and 24 h for adults and nestlings, respectively, and just before injection, minus the difference in thickness of the wing web injected with physiological water. Thus, the measure of response is expressed in millimeters. For nestlings, we calculated mean responses for each brood and then calculated an overall mean based on these brood mean values. We included data on Ficedula hypoleuca from Moreno et al. (1999) and on Panurus biarmicus from H. Hoi (personal communication), who used similar methods to those used by us. For nestlings, we have shown in a previous paper (Møller et al. 2004) that there are consistent differences in PHA response among species, even when only including species with data from both Denmark and Spain. Therefore, the use of our estimates of specific nestling immune responses in the analyses is justified.
To increase statistical power of our analyses, we used mean values of PHA response for each species independently of the locality of capture and sex (i.e., for many species, we have no information on the sex of individuals tested). Even assuming latitudinal trends in parasitism and immunity (Scheuerlein and Ricklefs 2004; Møller et al. 2006), but also the possibility of immune response varying between sexes (Fargallo et al. 2002; Tschirren et al. 2003; but for an extensive study failing to show any overall sex difference across a large number of species, see Møller et al. 1998) and during the breeding season for the same individual (Gonzalez et al. 1999), the use of these mean values of PHA response is justified for several reasons. First, for 18 species with mean estimates available from both Spain and Denmark, there was significantly more variation among than within species in PHA response (1-way ANOVA based on residual PHA response from a regression of log-transformed PHA response on log-transformed body mass, 82.7% of the variance among species—1-way ANOVA: F17,18 = 11.94, P < 0.001; Møller et al. 2003). Second, our estimates can be considered reliable independent of intraspecific differences between sexes because variance within species is significantly smaller than variance among species (63.4% of the variance among species: F41, 371 = 18.55, P < 0.001; data from Denmark 2001). Finally, the hypothesis of nest-building behavior having a sexually selected component applies to both males and females (Soler JJ, Møller, and Soler M 1998), and thus, because females contribute to nest building in all species with data on PHA response, the prediction would not differ for males and females. Moreover, females also experience a peak of immunosuppressive hormones (i.e., testosterone and estradiol) during nest building (Logan and Wingfield 1995), which generates similar predictions for males and females.
Statistical analyses
Intraspecific approach
Volume of nest material of swallows was approximately normally distributed (Kolmogorov–Smirnov tests for continuous variables, P > 0.2). Distribution of frequency of NAbs was skewed to the right, and thus, we used loge-transformed data in our analyses. Values of complement were far from normally distributed, and thus, we used nonparametric and parametric statistical tests to explore the relationship between nest material volume and complement and NAbs.
Comparative approach
Phylogenetic relationships between different species were estimated following Sibley and Ahlquist (1990) and more recent publications (Sheldon and Winkler 1993; Blondel et al. 1996; Cibois and Pasquet 1999) (see Appendix 2). We assumed all polytomies (N = 5) to be unresolved. Branch lengths were assigned using 3 different methodologies: 1) all were set equal to one; 2) by arbitrarily assigning all internode branch segments equal to one but constraining tips to be contemporaneous (Pagel 1992); and 3) by tips being contemporaneous, the depth of each node being arbitrarily set to one less the number of tip species that descend from it (Grafen 1989).
To control for the possible effect of common phylogenetic descent, we used Felsenstein's (1985) independent comparison method as implemented in the computer program PDAP (version 6.0, module PDTREE) by Garland et al. (1999) and Garland and Ives (2000). This method finds a set of independent pairwise differences or contrasts, assuming that changes along the branches of the phylogeny can be modeled by a Brownian motion process (successive changes are independent of one another) and that the expected total change over many independent changes is zero (Harvey and Pagel 1991). Therefore, pairwise differences in the phylogenetic tree are independent of each other (Harvey and Pagel 1991). The advantage of the independent comparison approach is that, by partitioning the variation appropriately, all contrasts can be used to assess a hypothetical comparative relationship (Harvey and Pagel 1991). These contrasts were estimated for each variable using the 3 kinds of trees differing in branch length (see above). Moreover, to check whether the contrasts were adequately standardized, we plotted absolute values of standardized contrasts versus their standard deviations (square roots of sums of corrected branch lengths) (Garland et al. 1991; Garland 1992; Pagel 1992). For nestlings, in no case did we find a significant correlation (P > 0.05) when branch length was assigned to one. However, when branch lengths were assigned following either Pagel's or Grafen's methods, absolute values of standardized contrasts resulted significantly related to their standard deviations (P < 0.05). Thus, we used estimated contrasts of all variables when branch lengths were all equal to one. With respect to adults, results were quite similar, but absolute standardized contrasts of log-transformed body mass were significantly related to their standard deviation when branch lengths were set to one but not when they were resolved by Pagel's or Grafen's methods. However, when using these methods, absolute standardized contrasts of immune response were significantly related to their standard deviation (P < 0.01). Thus, we used contrasts of body mass estimated from trees with branch lengths resolved following Pagel's method (P > 0.05), whereas all other contrasts were estimated in phylogenetic trees with all branch lengths equal to one (P > 0.05) (Garland et al. 1992; Pagel 1992).
Species varied substantially in sample sizes for PHA response (Appendix 1). The resulting variation in confidence with which species means were estimated was taken into account using weighted regressions. Briefly, by following Møller and Nielsen (2006), weights for each contrast were calculated as the mean sample size for the taxa subtended by that node. The resulting contrasts for each variable were subsequently used in multiple regression analyses through the origin for volume of nest material (dependent variable) and level of PHA response (independent variable), as well as body mass, clutch size, the duration of the nestling period, nest site, coloniality, and the sex building the nest as additional independent variables. Moreover, we also performed multiple regression analyses with PHA response as the dependent variable because sexual selection would simultaneously favor immunocompetent individuals with exaggerated ornaments (see in the Introduction). Therefore, level of immune response at the species level would depend on degree of nest-building effort.
Possible models explaining both PHA response and nest material volume were evaluated using the Akaike information criterion (AIC), and we used models with the smallest AIC values as the most parsimonious models (Burnham and Anderson 2002), assuming that models that differed by more than 2.0 in AIC being different. Subsequently, we used variables in these best-fit models in multiple regression analyses with the regression forced through the origin.
Conservatively, we estimated degrees of freedom by subtracting the number of polytomies in the phylogenetic trees (N = 5) from those estimated by the statistical program, and we used 2-tailed P values.
Nest size parameters, body mass, and immune response of adults were log10 transformed before estimation of contrasts to achieve approximately normal distributions. Moreover, discrete characters were used as dummy continuous variables (nest site: hole = 1, semihole = 2, and open = 3; coloniality: solitary = 0, maximum 10 pairs per colony = 1, maximum 100 pairs per colony = 2, and maximum 1000 pairs or more per colony = 3; and sex building the nest: females = 1, males and females = 2), thereby allowing estimation of phylogenetically independent contrasts for those variables.
Values reported are means (standard error [SE]).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1APPENDIX 2REFERENCES |
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Intraspecific approach
Lysis (i.e., complement) and agglutination (i.e., NAbs) values were positively related in females (Spearman rank correlation [rs] = 0.22, N = 91; P = 0.03), but not in males (rs = 0.16, N = 82; P = 0.14; see also Møller and Haussy 2007
). Therefore, to avoid redundancy of independent variables, we separately performed analyses with NAbs and complement. Barn swallows with larger levels of NAbs and complement built larger nests than did those with smaller values. That was the case for males (Figure 1; NAbs: Beta (SE) = 0.37(0.11), t80 = 3.20, P = 0.002; Lysis: rs = 0.41, N = 82, P = 0.0001) and females (Figure 1; Beta (SE) = 0.22(0.10), t89 = 2.11, P = 0.037; Lysis: rs = 0.21, N = 91, P = 0.048). When the single male and female of lysis category 2 was removed from the analyses, conclusions did not change for males (rs = 0.39, N = 81, P = 0.0003), whereas the relationship between NAbs and nest material volume became nonsignificant for females (rs = 0.19, N = 90, P = 0.07). Addition of laying date as an independent variable did not affect these conclusions (results not shown).
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Interspecific approach
Phylogenetically independent contrasts of volume of nest material were positively correlated with adult PHA response after controlling for the allometric effects of body mass and other possible confounding factors (Table 1, Figure 2). This conclusion was confirmed when all nonsignificant variables in Table 1 were removed from models with either PHA response (nest material volume; Beta (SE) = 0.31 (0.14), t41 = 2.32, P = 0.025) or volume of nest material (PHA response; Beta (SE) = 0.33 (0.14), t41 = 2.32, P = 0.025) as dependent variables. In addition, when using AIC for model selection, adult PHA response and volume of nest material entered in all better models (i.e., AIC < minimum + 2) explaining interspecific variation in nest material volume and PHA response, respectively (except for 9B in Table 2). Finally, we run the best models (i.e., smallest AIC values in Table 2) explaining volume of nest material and PHA response in multiple regression analyses. On the one hand, the best model explaining volume of nest material (R2 = 0.32, F4,39 = 5.18, P = 0.002) includes coloniality (Beta (SE) = –0.44 (0.14), t39 = 3.18, P = 0.003), duration of the nestling period (Beta (SE) = 0.42 (0.13), t39 = 3.19, P = 0.003), PHA response (Beta (SE) = 0.43 (0.13), t39 = 3.25, P = 0.002), and "sexes that build the nest" (Beta (SE) = 0.16 (0.13), t39 = 1.29, P = 0.205). On the other hand, the best model explaining PHA response of adults (R2 = 0.38, F5,38 = 5.31, P = 0.002) included coloniality (Beta (SE) = 0.42 (0.13), t38 = 3.20, P = 0.003), body mass (Beta (SE) = 0.32 (0.15), t38 = 2.10, P = 0.04), nest material volume (Beta (SE) = 0.30 (0.14), t38 = 2.18, P = 0.036), duration of the nestling period (Beta (SE) = – 0.41 (0.14), t38 = 3.15, P = 0.003), and clutch size (Beta (SE) = 0.26 (0.14), t38 = 1.91, P = 0.063).
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In a second series of analyses, we used immune response of nestlings instead of that of adults. However, the relationship between PHA response of nestlings and volume of nest material did not reach statistical significance after controlling for all possible confounding variables (partial Beta (SE) = 0.06 (0.14), t37 = 0.42, P = 0.68). In addition, when running in multiple regression analyses, the best models selected with AIC that included PHA response of nestlings (i.e., model 7C in Table 2) or volume of nest material (i.e., model 8D in Table 2) as independent variables, none of them explained a significant proportion of variance of dependent variables. In short, when using PHA response of nestlings and not that of adults, the best AIC model that explained variation in nest material volume (R2 = 0.33, F5,39 = 4.29, P = 0.001) included PHA response of nestlings (partial Beta (SE) = 0.10 (0.14), t39 = 0.71, P = 0.48), also included "sexes that build the nest" (partial Beta (SE) = 0.37 (0.13), t39 = 2.84, P = 0.007), body mass (partial Beta (SE) = 0.49 (0.13), t39 = 3.34, P = 0.002), coloniality (Beta (SE) = –0.36 (0.14), t39 = 2.61, P = 0.013), and clutch size (partial Beta (SE) = 0.22 (0.14), t39 = 1.52, P = 0.14). On the other hand, PHA response of nestlings was better explained by nest site (partial Beta (SE) = –0.29 (0.14), t41 = 2.16, P = 0.036), body mass (partial Beta (SE) = 0.38 (0.14), t41 = 2.60, P = 0.013), and volume of nest material (partial Beta (SE) = –0.05 (0.14), t41 = 0.34, P = 0.74), which corresponds to model 7D in Table 2 (R2 = 0.18, F3,41 = 3.46, P = 0.025). Therefore, specific immune response of adults, but not that of nestlings, was predicted by volume of nest material.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1APPENDIX 2REFERENCES |
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Nest building is an energetically expensive and time-consuming activity that has been proposed to be a generalized postmating, sexually selected signal of birds reflecting the willingness of males to invest in reproduction (Soler JJ, Møller, and Soler M 1998). This hypothesis has received both experimental (Møller et al. 1995
; Soler et al. 1996, 2001; De Neve, Soler JJ, Soler M, and Perez-Contreras 2004), observational (e.g., Palomino et al. 1998; Soler, Cuervo, et al. 1998; Fargallo et al. 2001; De Neve, Soler JJ, Soler M, Perez-Contreras, Martin-Vivaldi, and Martinez 2004; Tomas et al. 2006), and comparative support in different species of birds (Soler JJ, Møller, and Soler M 1998; Soler et al. 1999). Moreover, nest-building behavior or nest characteristics have been demonstrated to be important for mate choice in a number of different species including birds (Hansell 2000), fishes (Barber et al. 2001; Svensson and Kvarnemo 2003; Clotfelter et al. 2006), and crabs (Christy et al. 2002, 2003). Sexual selection on nest characteristics may benefit choosy individuals because nest traits affect probability of predation (e.g., Svensson and Kvarnemo 2003), thermal isolation (e.g., Hoi et al. 1994), or simply attract potential mates (e.g., Borgia 1985; Christy et al. 2002; Brouwer and Komdeur 2004). Benefits of selecting high-quality nest builders for reproduction could be explained if nests reliably signaled intrinsic aspects of builders such as parental quality (De Neve, Soler JJ, Soler M, and Perez-Contreras 2004; Clotfelter et al. 2006), dominance status (Borgia 1985), or ability to produce efficient immune responses (Barber et al. 2001; Brouwer and Komdeur 2004; Tomas et al. 2006). In that sense, we propose that nest-building effort could reliably reflect the ability of builders to raise an efficient immune response, following condition-dependent handicap models of sexual selection (Zahavi 1975, 1977; Andersson 1986; Iwasa and Pomiankowski 1991; Johnstone and Grafen 1992). This is mainly because the risk of parasitism is particularly high during nest building due to associated energetic costs and elevated concentration of immunosuppressive hormones during nest building. Therefore, only individuals with superior immune systems would be able to build large nests during a period when the probability of infection is high due to suppression of the immune system. In accordance with this prediction, we found a positive relationship between volume of nest material and immunity of builders not only at the intraspecific but also at the interspecific level.
At the intraspecific level, as measures of immunity we used NAbs and complement, 2 components of innate humoral immunity. Innate humoral immunity is assumed to be less sensitive to short-term variation in environmental conditions than acquired immunity (Matson et al. 2005) and, apart from behavioral resistance, it represents the first line of defence against parasite attack. NAbs facilitate initial pathogen recognition and initiate adaptive immune responses, whereas complement, which in a cascade system of proteins that activates one another, but that does not always need antibody for its activation, would initiate and amplify acquired immune responses (e.g., Playfair and Bancroft 2004).
We found that estimates of innate humoral immunity of male barn swallows, but to a lower extent also that of females, predicted volume of nest material and, therefore, nest-building effort. For the barn swallow, correlative and comparative evidence suggests that nest-building effort of males is a sexually selected trait (Soler, Cuervo, et al. 1998; Møller 2006). Moreover, nest-building effort of males, but not that of females, reflects final volume of nest material (Soler, Cuervo, et al. 1998). Thus, the association between immunity of males and nest material volume suggests that only males in prime immunological condition are able to exaggerate their nest-building effort. For females, we found a weaker but significant association between nest volume and immunity. Because female barn swallows also contribute to nest building, it is possible that they may also signal their immunity to males in a context of postmating sexual selection (Tomas et al. 2006). However, the result for females can also be explained in a context of female choice because there is evidence of female preference for males with efficient immune responses (Møller et al. 1999) but also of assortative mating with respect to tail length in barn swallows (Møller 1993).
Nests with larger amount of material may also be those with better properties (i.e., insolation and support for eggs and nestlings) that only males in better shape are able to build. However, that does not seem to be the case in barn swallows because females paired with long-tailed, attractive males (which contribute very little to nest building) increase capacity of their nest cups by reducing the thickness of the nest wall without reducing breeding success (Soler, Cuervo, et al. 1998). Thus, at least in barn swallows, exaggerated nest material volumes would not simply imply better insulated and protected nests. Therefore, our results suggest that the previously detected differential allocation to reproduction by female barn swallows when paired with males with exaggerated building effort (Soler, Cuervo, et al. 1998) could be explained by nest-building effort reflecting the ability of males to produce efficient immune responses that could be inherited by their offspring (indirect benefits; Sheldon 2000) and not only by the fact that such males also provided their offspring with more food (direct benefits).
At the interspecific level, we did not evaluate the same immunological components that we used for the intraspecific study in swallows because, at the time of sampling, standardized protocols (Matson et al. 2005) for wild birds were not established. Instead, we used values of skin swelling elicited by injection of the mitogen phytohemagglutinin (i.e., PHA response). Results from the comparative analyses of immunity and nest building also showed a positive relationship between volume of nest material and level of PHA response of adults across bird species after controlling for possible confounding variables. We controlled this relationship for variables known to affect specific levels of immune response (nest site [Møller and Erritzøe 1996] and breeding sociality [i.e., degree of coloniality, Møller and Erritzøe 1996; Møller et al. 2001; Tella 2002]) but also variables known to affect nest-building effort (clutch size and duration of the nestling period [e.g., Slagsvold 1982, 1989a, 1989b]). Introduction of all these variables in the same model is justified because nest site and breeding sociality may also affect nest-building effort and brood size and nestling period may affect level of immune response (e.g., Saino et al. 1997, 1998). Finally, we also included body mass and information on sex building the nest in the models, which may affect the 2 variables under investigation.
Because we captured individual adults throughout the breeding season, but not exclusively before or during nest building, our results could alternatively be interpreted as the result of nests of larger size being able to harbor a larger parasite population. In other words, nest size per se could affect the probability of parasitism after the nest-building stage because parasites reproducing in the nest would be better hidden in nests with more nest material (see in the Introduction). This effect was partially controlled by including information on sexes involved in nest building because the number of sexes participating in nest building is positively associated with final nest size (Soler JJ, Møller, and Soler M 1998). More importantly, this scenario predicts a positive relationship between nest size and immunity not only for adults but also for nestlings. However, we did not find support for this prediction because nest size did not explain PHA response of nestlings after adjusting for potentially confounding variables (see Results). Consequently, the alternative hypothesis of selection due to parasitism during nesting is not supported. Although this is a correlational study from which causation cannot be inferred, the fact that PHA response of adults, but not that of nestlings, positively covaried with nest -building effort suggests that nest material volume is a reliable signal of immunity of nest builders.
In summary, we found intra- and interspecific evidence consistent with the hypothesis of nest-building effort (and thus nest size) reliably reflecting the ability of builders to raise an efficient immune response. Although this hypothesis should be experimentally tested, correlational and comparative results presented here open the possibility that nest-building activity is a signal that birds may use as an indicator of the nest builder to raise efficient immune responses.
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APPENDIX 1 |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1APPENDIX 2REFERENCES |
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APPENDIX 2 |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIX 1APPENDIX 2REFERENCES |
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Phylogenetic relationships among passerine species included in the analyses. Codes of species names are given in the Appendix.
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ACKNOWLEDGEMENTS |
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W.C. Aarestrup, Ph. Christe, E. Flensted-Jensen, M. Houmøller, K. Klarborg, J.M. Marín, P. Pap, and T. Pérez kindly helped search for nests and/or to make phytohemagglutinin tests. Their efforts were indispensable for the success of our study. The authorization for carrying out the fieldwork in Spain was granted by Dirección General de Gestión del Medio Natural, Consejería de Medio Ambiente, Junta de Andalucía. H. Hoi kindly provided unpublished information on T-cell response of adult Panurus biarmicus. J.J.S. and M.M.V. were partially supported by the Junta de Andalucía (RNM-340 and RNM-339, respectively).
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REFERENCES |
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