Behavioral Ecology Advance Access originally published online on March 1, 2007
Behavioral Ecology 2007 18(3):513-520; doi:10.1093/beheco/arm004
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Maternal immune factors and the evolution of secondary sexual characters
a Dipartimento di Biologia, Università degli Studi di Milano, via Celoria 26, I-20133 Milano, Italy b Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, Bâtiment A, 7ème étage, 7 quai Saint Bernard, Case 237, F-75252 Paris Cedex 05, France c Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, José Gutierrez Abascal 2, E-28006 Madrid, Spain d Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK e DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, University of Cape Town, Rondebosch 7701, South Africa f Dipartimento di Biologia Animale, Università di Pavia, piazza Botta 9, I-27100 Pavia, Italy g Avian Science Research Centre, Scottish Agricultural College, Ayrshire KA6 5HW, Scotland
Address correspondence to A. P. Møller. E-mail: anders.moller{at}snv.jussiev.fr.
Received 21 February 2005; revised 16 January 2007; accepted 17 January 2007.
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ABSTRACT |
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Secondary sexual characters have been hypothesized to reveal the ability of males to resist debilitating parasites. Although such reliable signaling of parasite resistance may be maintained by parasite–host coevolution, maternal effects potentially provide a previously neglected factor that could affect the level of genetic variation in resistance to parasites. That could be the case because maternal effects have an entirely environmental basis, or because they can maintain considerable amounts of genetic variation through epistatic effects, even in the presence of strong directional selection. Maternal effects have been shown to occur as maternal allocation of immune factors to offspring, and such allocation may depend on the mating prospects of sons, causing mothers to differentially allocate maternal effects to eggs in species subject to intense sexual selection. Here we show that a maternal effect through innate antibacterial immune defense, lysozyme, which is transferred from the mother to the egg in birds, is positively associated with the evolution of secondary sexual characters. Previous studies have shown that females differentially allocate lysozyme to their eggs when mated to attractive males, and elevated levels of lysozyme are associated with reduced hatching failure and superior health among neonates and adults. In this study, comparative analyses of lysozyme from eggs of 85 species of birds showed a strong positive relationship between brightness of male plumage and egg lysozyme, even when controlling for potentially confounding variables. These findings suggest that maternal immune factors may play a role in the evolution of secondary sexual characters.
Key words: birds, comparative analyses, egg, immunity, lysozyme, maternal effects.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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A distinguishing feature of many models of sexual selection is that females make mate choices for genetic benefits from their partners, even though genetic variation for such benefits may become depleted, because beneficial alleles should go to fixation (Taylor and Williams 1982
; Pomiankowski and Møller 1995). This so-called lek paradox may be resolved if more metabolic pathways, and hence their underlying genetic variation, affect the expression of condition-dependent secondary sexual characters compared with other traits (Rowe and Houle 1996). A second scenario is based on parasite–host coevolution maintaining genetic variation in parasite resistance, with only resistant males being able to develop the most exaggerated characters (Hamilton and Zuk 1982; Folstad and Karter 1992). A third scenario relying on mutational input affecting the expression of secondary sexual characters is based on the observation that males generally have higher mutation rates than females (Bartosch-Harlid et al. 2003; Møller and Cuervo 2003; Kirkpatrick and Hall 2004). Although the relative merits of these hypotheses remain unexplored, they may on their own or in combination be sufficient to explain the small amounts of genetic benefits typically found in studies of sexual selection (Møller and Alatalo 1999).
Despite a number of different explanations potentially accounting for the lek paradox, we cannot exclude the possibility that as yet unexplored factors may be important. Here we suggest that maternal effects may constitute one such factor. Maternal effects occur when the mother, or the environment in which she lives, directly affects the phenotype of her offspring (Mousseau and Fox 1998). Maternal effects may be entirely environmental or may be affected by genes, and they can maintain considerable amounts of genetic variation through epistatic effects, even in the presence of strong directional selection (Wade 1998). The reason for this fact is that selection on maternal effects depends on a combination of within- and among-family components (Wade 1998). Maternal effects may have long-lasting consequences for offspring (Mousseau and Fox 1998; Martin 2000; Metcalfe and Monaghan 2001) and thereby affect adult phenotype.
Female oviparous animals allocate many different kinds of components to their eggs including hormones, antioxidants, and immune factors (Rose and Orlans 1981; Schwabl 1993; Mousseau and Fox 1998; Gil et al. 1999; Blount et al. 2000; Kudo 2000). Studies of maternal effects of birds have shown that females differentially allocate substances to eggs depending on sexual attractiveness of their partner (Gil et al. 1999, 2004; Saino, Bertacche, et al. 2002; Saino, Ferrari, et al. 2002; Saino, Martinelli, et al. 2002). Early maternal effects can have important consequences for the development of immune function in adults (Martin 2000). Thus, there is scope for maternal effects affecting performance of offspring when these reach adulthood.
In all vertebrates, lysozyme is a fundamental component of innate antibacterial immune defense that is transferred from the mother to the egg in birds, digesting the peptoglycanes that are major components of bacterial cell walls (Tizard 1991; Trziszka 1994; Braun and Fehlhaber 1996; Roitt et al. 1996; Pastoret et al. 1998; Kudo 2000). Concentration of egg lysozyme reflects circulating levels in mothers, and females may trade allocation to eggs against the use of lysozyme for their own immune protection. Egg lysozyme may be carried over into the embryo and nestling (Board and Fuller 1974). Egg lysozyme enhances hatching success and may facilitate offspring survival (Melek 1977; Prusinowska and Jankowski 1996; Prusinowska et al. 2000; Saino, Martinelli, et al. 2002). However, information is unavailable for the duration of the effects of maternal lysozyme transmission to offspring.
The aim of this comparative study was to investigate whether lysozyme as a maternal effect is positively related to the expression of a secondary sexual character, plumage coloration. Females have been shown to allocate lysozyme to their eggs depending on the attractiveness of the mates in one species, the barn swallow Hirundo rustica (Saino, Martinelli, et al. 2002). The positive association between lysozyme concentration in the eggs and paternal ornamentation may occur as a result of selection for larger maternal allocation to eggs laid for high-quality males. We may therefore expect that as secondary sexual characters become exaggerated across species, females would be selected to allocate an ever-larger amount of lysozyme to eggs, which is a potentially very important immune factor that would allow further exaggeration of secondary sexual characters. This is the case because exaggerated male plumage brightness may reflect the long-term effects of intense sexual selection. The possible cost for females of doing so in terms of reduction in their own immune defense would be balanced by an increased benefit in terms of mating success of their sons due to the greater variance in male than in female reproductive success. We tested this prediction by determining whether male and female coloration were positively related to lysozyme concentration of eggs, assuming that a brighter coloration of males compared with females would reflect an increase in the intensity of sexual selection. In fact, sexual dichromatism has been shown to reflect interspecific variation in sperm competition and in the level of polygyny (e.g., Andersson 1994; Møller and Birkhead 1994). We controlled for similarity in phenotype among taxa due to common descent by calculating standardized linear contrasts that reveal convergent evolution rather than similarity among species due to common descent (Felsenstein 1985).
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METHODS |
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Field procedures
We collected nonincubated eggs of 85 species of birds under permit in Europe (n = 60), North America (n = 1), and South Africa (n = 21) (plus Gallus gallus, Numida meleagris, and Phasianus colchicus eggs collected from captive stocks) during 2000–2003. Sample sizes were kept to a minimum for ethical reasons, while still allowing for tests of variance among and within species. For 14 species, some eggs could not be univocally assigned to their original clutch at the time of lysozyme analysis. For the remaining 71 species, the mean number of eggs collected per clutch was 1.58 (0.07 standard error [SE], range 1–6). We based our analyses on the general mean lysozyme concentration for each species computed on all eggs available for that species, irrespective of the clutch of origin. For the 71 species for which all eggs available to lysozyme analysis could be assigned to their original clutch, there was an extremely high correlation between the mean lysozyme concentration computed over all eggs of each species, irrespective of their clutch of origin, and the mean of the clutch means for that species (r = 0.996, n = 71, P < 0.0001). Because the mean values computed in the 2 ways were highly positively correlated, and the adoption of the general mean allowed us to include the 14 species for which assignment of some eggs was uncertain, we decided to adopt this approach.
Quantifying lysozyme in eggs
Eggs were separated into egg white and yolk, and the egg white was used for lysozyme analysis. Both components of the eggs were frozen as soon as possible after separation (usually within 1 day) and then transferred into a –20 °C freezer until analysis. Lysozyme activity was determined using the lysoplate method on egg white (Osserman and Lawlor 1966), modified in order to carry out the assay using a micromethod. The test was performed on an agar gel with a dried strain of Micrococcus lysodeikticus (M-3770, Sigma Chemical Co., Milano, Italy), which is particularly sensitive to lysozyme activity, by inoculating each test hole with 12.5 µl albumen. Crystalline hen egg white lysozyme (L-6876, Sigma Chemical Co.) was used to prepare a standard curve in each plate. Agar gels were incubated at 27 °C for 20 h, and the area of the gel surrounding the plasma inoculation site where bacterial growth was inhibited was measured using an ad hoc ruler and converted into hen egg lysozyme equivalents (HEL equivalents, expressed in µg/ml) according to the standard curve. Hence, lysozyme activity is expressed as HEL per milliliter throughout this study (µg/ml) and assumed to reflect concentration (Brightman et al. 1991). Intra-assay coefficient of variation for the albumen was 9.6%. Interassay coefficient of variation was 10.3%. Lysozyme activity was log10 transformed to achieve normality. There was considerably more variance among than within species in lysozyme content of eggs (F84,583 = 72.42, P < 0.001, r2 = 0.90) based on log10-transformed data. The data set is reported in the Appendix.
Color scores of adult birds
We scored the brightness of the plumage of adult males and females in full breeding plumage using color plates in field guides (Peterson et al. 1988; National Geographic Society 1992; Sinclair et al. 1993). Color scores on a scale from 1 to 6, where 1 is uniform and drab and 6 is conspicuous and bright, were highly repeatable among 3 independent scorers, who were unaware of the purpose of the study (male scores: F84,170 = 15.30, P < 0.0001, r2 = 0.825; female scores: F84,170 = 8.70, P < 0.0001, r2 = 0.718; sex difference in scores: F84,170 = 29.58, P < 0.0001, r2 = 0.904). Color scores were only assessed for the part of the spectrum that is visible to humans.
Confounding variables
Breeding habitat was classified as either aquatic, including marshes, meadows, and other humid habitats (score of 0) or terrestrial (score of 1). Mating system was scored as monogamous (score of 0) or nonmonogamous (score of 1). Breeding sociality was scored as 0 for solitary species, 1 for species breeding in colonies with 2–10 pairs, 2 for species breeding in colonies with 11–100 pairs, 3 species breeding in colonies with 101–1000 pairs, and 4 species breeding in colonies with more than 1000 pairs. We used maximum colony size. Information was obtained from Glutz von Blotzheim (1966–1997), Cramp et al. (1982–1994), and Fry et al. (1982–2004) combined with our own field experience.
Comparative methods
We constructed a composite phylogeny of the species based on Sibley and Ahlquist (1990), Sheldon and Winkler (1993), Crochet et al. (2000), and Barker et al. (2001) (Figure A1). The phylogeny is presented in the Appendix.
We calculated statistically independent linear contrasts for each variable according to the method developed by Felsenstein (1985) using the software CAIC (Purvis and Rambaut 1995). All branches were assigned the same length, although a second set of analyses based on uneven branch lengths, assuming a gradual evolution model as implemented in the software, produced qualitatively similar results. We tested for violations of statistical assumptions by regressing standardized contrasts against their standard deviations (Garland et al. 1992). None of these tests revealed any significant deviations, after Bonferroni adjustment for multiple tests. Contrasts with extreme residuals were deleted from analyses to test for robustness of results (Jones and Purvis 1997), and this did not change any of the conclusions presented here. Similarly, tests using ranked independent variables in cases with extreme residuals did not produce qualitatively different results. Contrasts were analyzed by forcing regressions through the origin because the dependent variable a priori is expected not to have evolved when the independent variable has not shown any evolutionary change (Harvey and Pagel 1991).
Regression analyses require that models not be overparameterized relative to the number of observations in the data set (Neter et al. 1989; Sokal and Rohlf 1995; Zar 1996). Therefore, we attempted not to increase the number of predictors in order to strike a balance between having exhaustive models and having models with a low number of predictor variables. We scrutinized multiple regression analyses for multicollinearity of independent variables. However, in no case did the condition index indicate that parameter estimates were substantially biased by multicollinearity problems, as also suggested by the low values of the pairwise correlations between independent variables (r < 0.56 in all cases). Residuals of lysozyme concentration on independent variables were normally distributed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Mean concentration of lysozyme was 295.18 µg/ml, range 0.03–8719.35 µg/ml, n = 85 species and 668 eggs, or on average 7.9 eggs per species. If maternal effects through lysozyme in eggs affected the evolution of plumage brightness, we should expect a positive association between plumage brightness and lysozyme across taxa. Indeed, there was a strong positive relationship for male plumage brightness across 85 species of birds (Figure 1A; F1,83 = 39.40, r2 = 0.32, P < 0.0001, slope [SE] = 0.45 [0.07]), as predicted, whereas the relationship was not statistically significant for plumage brightness of females (Figure 1B; F1,83 = 3.72, r2 = 0.04, P = 0.06), which can be considered to act as an internal control group. When we excluded from the analysis 7 data points (i.e., those corresponding to Anas platyrhynchos, Euplectes orix, G. gallus, Merops hirundineus, Nectarinia chalybea, P. colchicus, and Ploceus velatus) in the upper right part of Figure 1A that subjectively appeared to stretch the relationship between lysozyme and male plumage brightness, the relationship was still positive and highly significant (F1,76 = 23.00, r2 = 0.23, P < 0.001). The difference in plumage brightness between males and females (dichromatism) was positively associated with lysozyme concentration in eggs (Figure 1C; F1,83 = 24.01, r2 = 0.22, P < 0.0001, slope [SE] = 0.44 [0.09]). A multiple regression showed no significant interaction between male and female brightness, whereas the main effect of male brightness remained significant (Table 1). Based on sum of squares reported in Table 1, the effect of the interaction would be significant in an analysis of as many as approximately 170 species. Analysis of contrasts revealed similar conclusions, with a significant effect of male plumage brightness and no effect of the interaction with female plumage brightness, indicating that the slope of the relationship between lysozyme concentration and plumage brightness of either sex did not vary according to plumage brightness of the other sex (Table 1). However, in this case, only approximately 100 data points (i.e., contrasts) would make the effect of the interaction significant. These conclusions are robust with respect to the topology of the phylogeny because any uncertainty in the phylogeny will be reflected in estimates of rates of evolution for both males and females.
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Regression analyses of lysozyme concentration in eggs based on species-specific data where we also included body mass as a regressor revealed that levels were elevated in species from terrestrial habitats (F1,82 = 12.56, P = 0.001, r2 = 0.17, slope [SE] = 0.95 [0.27]), solitary breeders (F1,82 = 18.26, P < 0.001, r2 = 0.16, slope [SE] = –0.33 [0.08]), and monogamous species (F1,82 = 8.17, P = 0.005, r2 = 0.08, slope [SE] = 0.71 [0.25]). A multiple regression based on species-specific values where we included the effects of male and female plumage brightness together with their interaction showed that only habitat and coloniality retained their significant effects (Table 2), whereas the effect of mating system could be excluded by step-down selection of nonsignificant regressors (Crawley 1993
). In this analysis, although the effect of plumage brightness on lysozyme concentration was still highly significant and positive after controlling for the concomitant effect of female plumage brightness and other confounding effects, female plumage brightness did not predict lysozyme concentration (Table 2). Removal of nonsignificant terms presented in the raw data model in Table 2 did not alter the results concerning significant predictors.
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A multiple regression approach for the linear contrasts only showed significant effects of male plumage brightness, with the effects of female brightness and its interaction with male plumage brightness, breeding habitat, and breeding sociality not being statistically significant (Table 2). Thus, our conclusions of a relationship between lysozyme concentration and male plumage brightness based on contrasts were unaffected by potentially confounding variables (details not shown). Step-down exclusion of nonsignificant terms from the contrasts-based model in Table 2 disclosed a marginally significant negative effect of coloniality (F1,78 = 3.95, P = 0.050, r2 = 0.08, slope [SE] = 0.71 [0.25]).
In an analysis of species-specific data, lysozyme was predicted by sexual dichromatism, expressed as the within-species difference between male and female plumage brightness scores (F1,83 = 24.01, P < 0.001, r2 = 0.22, slope [SE] = 0.44 [0.09]). A multiple regression model of species-specific data with lysozyme as the dependent variable and sexual dichromatism, habitat, and coloniality as predictors produced a model that explained 47% of the variance (F3,81 = 23.99, P < 0.001). The partial regressions were significant for sexual dichromatism (F1,81 = 24.62, P < 0.001, slope [SE] = 0.38 [0.08]), habitat (F1,81 = 9.68, P = 0.003, slope [SE] = 0.67 [0.22]), and coloniality (F1,81 = 9.64, P = 0.003, slope [SE] = –0.24 [0.08]).
An analysis of contrasts with lysozyme as the dependent variable and sexual dichromatism as the independent variable showed a significant, positive effect (F1,79 = 5.60, P = 0.020, slope [SE] = 0.18 [0.08]).
A multiple regression of contrasts including lysozyme as the dependent variable showed a positive effect of sexual dichromatism (F1,77 = 5.75, P = 0.02, slope [SE] = 0.18 [0.08]) and a negative effect of coloniality (F1,77 = 4.13, P = 0.046, slope [SE] = –0.18 [0.09]).
An analysis of species-specific lysozyme data with ranked values of the same independent variables included in the model presented in Table 2 led to qualitatively identical results with, in particular, a significant positive effect of male plumage brightness on lysozyme concentration (F1,79 = 15.91, P < 0.001, slope [SE] = 0.02 [0.01]). Similarly, an analysis of ranked contrasts of independent variables with the same model as in Table 2 confirmed a significant positive effect of male plumage brightness on lysozyme concentration (F1,75 = 9.76, P = 0.003, slope [SE] = 0.005 [0.002]).
We also repeated these analyses with ranked values of sexual dichromatism, rather than plumage brightness of the 2 sexes separately, and found that lysozyme concentration was positively predicted by species-specific sexual dichromatism (F1,81 = 21.00, P < 0.001, slope [SE] = 0.02 [0.004]) as well as by the linear contrasts in sexual dichromatism (F1,78 = 6.82, P = 0.01, slope [SE] = 0.003 [0.001]).
Exclusion of the 3 species from captivity (G. gallus, P. colchicus, and N. meleagris) did not change the conclusions (results not shown).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Our main findings were that 1) females allocated more lysozyme to their eggs in species with bright male plumage; 2) therefore, eggs contained more lysozyme in sexually dichromatic species than in monochromatic species; and 3) this was the case even when taking potentially confounding variables into account and when controlling for similarity among species due to common descent. However, the statistical effect of a unit change in plumage brightness of either sex on lysozyme concentration did not depend on the concomitant effect of plumage brightness of the other sex, as indicated by the nonsignificant interaction. We will discuss the implications of these observations.
Sexual dichromatism explains variation in egg lysozyme concentration even after controlling for other variables that were independently related to lysozyme concentration. None of the potentially confounding variables accounted for additional variation in lysozyme content in the contrast analyses, and apparent relationships based on analyses of species-specific data must therefore be ascribed to similarity due to common descent rather than convergent evolution. Although we cannot infer causality in this comparative study, this observation can be interpreted in at least 2 different ways. First, mothers affect the ability of offspring to cope with the parasite environment during early development, providing sons with a benefit when they encounter the costs of developing and maintaining their costly secondary sexual characters. Second, susceptibility to parasitism is often elevated in species with sexual dichromatism, in particular in sons, and mothers may compensate for this susceptibility by allocation of lysozyme to eggs. Adult males are often differentially susceptible to parasitism (Alexander and Stimson 1989; Zuk 1990; Poulin 1996; Møller, Sorci, and Erritzøe 1998), and empirical studies have generally shown that males with the most exaggerated secondary sexual characters tend to have fewer parasites and stronger immune response or larger immune defense organs than less adorned males (Møller et al. 1999). In addition, species with more exaggerated sexual dichromatism tend to have larger immune defense organs (Møller, Dufva, and Erritzøe 1998). Finally, adult but not juvenile males tend to have smaller immune defense organs than females, and this reduction in size of immune defense organs of adult males increases with the intensity of sexual selection as reflected by the frequency of extrapair paternity (Møller, Sorci, and Erritzøe 1998). These findings imply that males in species of birds with exaggerated sexual coloration indeed may be more susceptible to parasitism than females. If this is generally the case, then we can interpret the elevated lysozyme levels in eggs of more sexually dichromatic species we demonstrated in the analyses based on the within-species difference in brightness between the sexes as a maternal mechanism to compensate for immunosuppression in sons when sons reach adulthood. Both of these interpretations are based on the assumption that mothers benefit from differential allocation of maternal effects to eggs when sons have greater variance in reproductive success than daughters because such sons will enjoy an additional probability of reproducing.
There is a dearth of information on the effects of lysozyme on free-living birds, with almost all knowledge being attributed to studies of domesticated chickens and turkeys. The only extensive study of lysozyme in birds is on the barn swallow H. rustica (Saino, Martinelli, et al. 2002). Female barn swallows differentially allocate lysozyme to eggs of long-tailed males. This is allocation in the strict sense because the concentration of lysozyme in eggs is considerably higher than in maternal plasma, as also reported for other species (Bizzarri et al. 1999).
The range of lysozyme concentration spanned 6 orders of magnitude across 85 species of birds. We can only speculate about the function of this enormous amount of variation. We suggest that lysozyme functions to protect eggs and neonates from bacterial infection, as shown for chickens and turkeys (Melek 1977; Prusinowska and Jankowski 1996; Prusinowska et al. 2000). Very little is known about the importance of bacteria as a cause of mortality in natural populations of birds, with studies by Cook et al. (2003, 2005) being a notable exception. Lysozyme allocation to eggs may be costly to mothers because lysozyme allocated to eggs is unavailable to mothers, thus potentially trading maternal viability against egg viability (Saino, Martinelli, et al. 2002). The selection pressures that have resulted in the evolution of lysozyme concentrations are likely to be caused by bacteria, and, therefore, we can use data from the present study to make predictions about the species of birds that are likely to suffer particularly from health problems due to bacteria. It could be argued that, because parasite load is known to increase with colony size (e.g., Loye and Zuk 1991), lysozyme concentration should be higher in colonial than in solitary species. The effect of coloniality on lysozyme concentration, however, was found to be negative rather than positive. A possible interpretation of this finding is that a trade-off may exist between allocation of lysozyme to the eggs and maternal immune defense, whereby mothers of colonial species, being more exposed to virulent bacteria, tend to allocate more to own immune defense at the expense of their eggs.
Finally, we suggest that the priming effects of early maternal effects on the development of immunity may be important. Many studies have suggested that the early embryonic environment, which is strongly influenced through maternal effects, may have important implications for the development of immunity (reviewed in Martin 2000).
The results presented here have several implications. First, the lek paradox, which arises from the puzzling observation that directional preferences for genetic benefits of mate choice appear to be common despite the fact that genetic variation in such benefits should disappear, may be resolved if a major source of variation in male quality derives as a consequence of genetic and nongenetic maternal effects, as suggested here. Second, the evolution of sexual dichromatism is linked to maternal innate immunity, suggesting that maternal effects may have played an important role in the evolution of such characters. Third, the interspecific patterns of phenotypic variation observed here also have implications for the evolution of immunity. Studies of chickens, turkeys, and barn swallows have shown positive correlations between lysozyme concentrations in maternal plasma and in eggs and offspring (Melek 1977; Prusinowska et al. 2000; Saino, Martinelli, et al. 2002), suggesting that patterns of phenotypic variation in lysozyme concentration among adults should parallel the patterns observed for eggs. Thus, the importance of this component of immunity varies considerably among species with potential consequences for sexual selection and life history.
In conclusion, we have shown that in species with more sexual dichromatism, eggs receive more maternally derived lysozyme. This suggests that maternal effects may have played a role in the evolution of sexual dichromatism and hence in interspecific variation in sexual selection.
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APPENDIX |
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Information on lysozyme concentration (µg/ml) (SE), sample size (number of eggs), male color, female color, breeding habitat (0, aquatic; 1, terrestrial), and breeding sociality (0, solitary; 1, colonies 2–10 pairs; 2, 11–100 pairs; 3, 101–1000 pairs; 4, more than 1000 pairs).
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ACKNOWLEDGEMENTS |
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We are thankful to N. Baccetti, M. Caffi, M. Fasola, R. Visagie for help in collecting the eggs. We are also grateful to the Northern Cape Province's Department of Tourism, Environment, and Conservation for egg-collecting/research permits. Two referees provided constructive comments to earlier drafts of the paper.
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REFERENCES |
|---|
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
|---|
Alexander J, Stimson WH. Sex hormones and the course of parasitic infection. Parasitol Today (1989) 4:1891–1893.
Andersson M. Sexual selection (1994) Princeton (NJ): Princeton University Press.
Barker FK, Barrowclough GF, Groth JG. A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proc R Soc Lond B Biol Sci (2001) 269:295–308.
Bartosch-Harlid A, Berlin S, Smith NGC, Møller AP, Ellegren H. Life history and the male mutation bias. Evolution (2003) 57:2398–2406.[CrossRef][Web of Science][Medline]
Bizzarri D, Giardini A, Voi M, Renon P, Corsico G. Tenore di lisozima nelle uova di struzzo (Sthrutio camelus). Riv Avicol (1999) 68:36–41.
Blount JD, Houston DC, Møller AP. Why egg yolk is yellow. Trends Ecol Evol (2000) 15:47–49.[CrossRef][Medline]
Board RG, Fuller R. Non-specific antimicrobial defences of the avian egg, embryo and neonate. Biol Rev (1974) 49:15–49.[Medline]
Braun P, Fehlhaber K. Studies of the inhibitory effect of egg albumen on gram-positive bacteria and on Salmonella enteritidis strains. Arch Geflügel (1996) 60:203–207.
Brightman AH, Wachsstock RS, Erskine R. Lysozyme concentrations in the tears of cattle, goats, and sheep. Am J Vet Res (1991) 52:9–11.[Web of Science][Medline]
Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ. Trans-shell infection by pathogenic micro-organisms reduces the shelf life of non-incubated bird's eggs: a constraint on the onset of incubation? Proc R Soc Lond B Biol Sci (2003) 270:2233–2240.[Medline]
Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ. Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behav Ecol (2005) 16:30–36.
Cramp S, Simmons KEL, Perrins CM, eds. Handbook of the birds of Europe, the Middle East and North Africa (1982 –1994) Vol. I–IX. Oxford: Oxford University Press.
Crawley MJ. GLIM for ecologists (1993) Oxford: Blackwell Scientific.
Crochet P-A, Bonhomme F, Lebreton J-D. Molecular phylogeny and plumage evolution in gulls (Larini). J Evol Biol (2000) 13:47–57.[CrossRef][Web of Science]
Felsenstein J. Phylogenies and the comparative method. Am Nat (1985) 125:1–15.[CrossRef][Web of Science]
Folstad I, Karter AJ. Parasites, bright males, and immunocompetence handicap. Am Nat (1992) 139:603–622.[CrossRef][Web of Science]
Fry CH, Keith S, Urban K, eds. The birds of Africa (1982 –2004) Vol. 1–7. London: Academic Press.
Garland T Jr, Harvey PH, Ives AR. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Am Nat (1992) 141:18–32.
Gil D, Graves JA, Hazon N, Wells A. Male attractiveness and differential testosterone investment in zebra finch eggs. Science (1999) 286:126–128.
Gil D, Leboucher G, Lacroix A, Kreutzer M. Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav (2004) 45:64–70.[CrossRef][Medline]
Glutz von Blotzheim UN, ed. Handbuch der Vögel Mitteleuropas (1966 –1997) Vol. 1–14. Wiesbaden (Germany): AULA-Verlag.
Hamilton WD, Zuk M. Heritable true fitness and bright birds: a role for parasites? Science (1982) 218:384–387.
Harvey P, Pagel M. The comparative method in evolutionary biology (1991) Oxford: Oxford University Press.
Jones KE, Purvis A. An optimum body size for mammals? Comparative evidence from bats. Funct Ecol (1997) 11:751–756.[CrossRef]
Kirkpatrick M, Hall DW. Male-biased mutation, sex linkage, and the rate of adaptive evolution. Evolution (2004) 58:437–440.[CrossRef][Web of Science][Medline]
Kudo S. Enzymes responsible for the bactericidal effect in extracts of vitelline and fertilisation envelopes of rainbow trout eggs. Zygote (2000) 8:257–265.[CrossRef][Web of Science][Medline]
Loye JE, Zuk M. Bird-parasite interactions. In: Ecology, evolution, and behaviour (1991) Oxford: Oxford University Press.
Martin JT. Sexual dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur J Pharmacol (2000) 405:251–261.[CrossRef][Web of Science][Medline]
Melek OI. The lysozyme content of egg protein in fowls and embryo mortality. Sb Nauchnykh Moskovskaya Veterinarnaya Akad (1977) 92:71–74.
Metcalfe NB, Monaghan P. Compensation for a bad start, grow now, pay later? Trends Ecol Evol (2001) 16:254–260.[CrossRef][Medline]
Møller AP, Alatalo RV. Good genes effects in sexual selection. Proc R Soc Lond B Biol Sci (1999) 266:85–91.
Møller AP, Birkhead TR. The evolution of plumage brightness in birds is related to extra-pair paternity. Evolution (1994) 48:1089–1100.[CrossRef][Web of Science]
Møller AP, Christe P, Lux E. Parasite-mediated sexual selection: effects of parasites and host immune function. Q Rev Biol (1999) 74:3–20.[CrossRef][Medline]
Møller AP, Cuervo JJ. Sexual selection, germline mutation rate and sperm competition. BMC Evol Biol (2003) 3:1–11.[CrossRef][Medline]
Møller AP, Dufva R, Erritzøe J. Host immune function and sexual selection in birds. J Evol Biol (1998) 11:703–719.[CrossRef][Web of Science]
Møller AP, Sorci G, Erritzøe J. Sexual dimorphism in immune defense. Am Nat (1998) 152:605–619.[CrossRef][Web of Science]
Mousseau TA, Fox CW. Maternal effects as adaptations (1998) New York: Oxford University Press.
National Geographic Society. Field guide to the birds of North America (1992) 2nd ed. Washington (DC): National Geographic Society.
Neter J, Wassermann W, Kutner MH. Applied linear regression models (1989) 2nd ed. Homewood (CA): Irwin.
Osserman EF, Lawlor DP. Serum and urinary lysozyme (muraminidase) in monocytic and monomyelocytic leukaemia. J Exp Med (1966) 124:921–951.[Abstract]
Pastoret P, Gabriel P, Bazin H, Govaerts A. Handbook of vertebrate immunology (1998) San Diego (CA): Academic Press.
Peterson R, Mountfort G, Hollom PAD. Guida degli Uccelli d'Europa (1988) Padova (Italy): Muzzio & C.
Pomiankowski A, Møller AP. A resolution of the lek paradox. Proc R Soc Lond B Biol Sci (1995) 260:21–29.
Poulin R. Sexual inequalities in helminth infections: a cost of being a male? Am Nat (1996) 147:287–295.[CrossRef][Web of Science]
Prusinowska I, Jankowski J. The relationship between serum lysozyme activity and reproductive performance in turkeys. J Anim Feed Sci (1996) 5:395–401.
Prusinowska I, Jankowski J, Sowinski G, Wawro K. An evaluation of lysozyme usability in turkey improvement. Zivocisna Vyroba (2000) 45:225–228.
Purvis A, Rambaut A. Comparative analysis by independent contrasts (CAIC). Comput Appl Biosci (1995) 11:247–251.
Roitt I, Brostoff J, Male D. Immunology (1996) London: Mosby.
Rose ME, Orlans E. Immunoglobulins in the egg, embryo and young chick. Dev Comp Immunol (1981) 5:315–319.
Rowe L, Houle D. The lek paradox and the capture of genetic variance through condition-dependent traits. Proc R Soc Lond B Biol Sci (1996) 263:1415–1421.
Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R. Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B Biol Sci (2002) 269:1729–1733.[Medline]
Saino N, Ferrari RP, Martinelli R, Romano M, Rubolini D, Møller AP. Early maternal effects mediated by immunity depend on sexual ornamenation of the male partner. Proc R Soc Lond B Biol Sci (2002) 269:1005–1011.[Medline]
Saino N, Martinelli R, Dall'Ara P, Møller AP. Maternal effects and antibacterial immune defence and fitness in the barn swallow Hirundo rustica. J Evol Biol (2002) 15:735–743.[CrossRef][Web of Science]
Schwabl H. Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA (1993) 90:11446–11450.
Sheldon FH, Winkler DW. Intergeneric phylogenetic relationships of swallows estimated by DNA-DNA hybridization. Auk (1993) 110:798–824.[Web of Science]
Sibley CG, Ahlquist JE. Phylogeny and classification of birds (1990) New Haven (CT): Yale University Press.
Sinclair I, Hockey P, Tarboton N. Birds of Southern Africa (1993) Cape Town (South Africa): Struik Publishers.
Sokal RR, Rohlf FJ. Biometry (1995) 3rd ed. New York: Freeman.
Taylor PD, Williams GC. The lek paradox is not resolved. Theor Popul Biol (1982) 22:392–409.[CrossRef][Web of Science]
Tizard I. Veterinary immunology (1991) Philadelphia (PA): W. B. Saunders.
Trziszka T. Lysozyme and its functions in the egg. Arch Geflügelk (1994) 58:49–54.
Wade MJ. The evolutionary genetics of maternal effects. In: Maternal effects as adaptations—Mousseau TA, Fox CH, eds. (1998) Oxford: Oxford University Press. 5–21.
Zar JH. Biostatistical analysis (1996) 3rd ed. Upper Saddle River (NJ): Prentice Hall.
Zuk M. Reproductive strategies and sex differences in disease susceptibility: an evolutionary viewpoint. Parasitol Today (1990) 6:231–233.[CrossRef][Web of Science][Medline]
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