Behavioral Ecology Advance Access originally published online on December 7, 2005
Behavioral Ecology 2006 17(2):236-245; doi:10.1093/beheco/arj015
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Offspring sex ratio allocation in the parasitic jaeger: selection for pale females and melanic males?
a Norwegian Institute for Nature Research, Polar Environmental Centre, N-9296 Tromsø, Norway, b Department of Molecular Biotechnology, Institute of Medical Biology, University of Tromsø, N-9037 Tromsø, Norway, and c Department of Animal Ecology, University of Lund, S-22362 Lund, Sweden
Address correspondence to K. Janssen. E-mail: Kirstin.Janssen{at}tmu.uit.no.
Received 18 March 2005; revised 31 October 2005; accepted 7 November 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The maintenance of plumage color polymorphism in the parasitic jaeger (Stercorarius parasiticus) is still not well understood. Earlier studies indicated that selection may favor pale females and melanic males. If so, females would maximize their fitness, producing pale female and melanic male offspring. We therefore predicted that females might bias their offspring sex ratio toward daughters in pale pairs and toward sons in melanic pairs. Females might also choose to mate assortatively in relation to plumage color, thereby maximizing the probability of producing either pale or melanic offspring. Because females are larger than males, differential rearing costs may affect the offspring sex ratio independent of parental plumage color. We examined offspring sex ratio allocation, breeding variables indicative of parental quality, and mating pattern in relation to plumage color in a colony of parasitic jaegers in northern Norway. Jaegers tended to mate assortatively in relation to plumage color. The reproductive performance declined with season, and matched pairs appeared to be of lower quality than mixed pairs. The proportion of male offspring increased with hatching date in matched pale and mixed pairs, whereas the situation was reversed in matched melanic pairs. Matched pale pairs produced an overall surplus of favorable pale but costly daughters despite their lower quality, while melanic pairs produced a surplus of favorable melanic sons. However, differential offspring rearing costs and parental rearing capacity may have additionally affected the realized offspring sex ratio. Mixed pairs producing an overall surplus of pale and melanic daughters allocated their resources according to differential rearing costs and parental quality only. We suggest that both strategies of sex ratio allocation together with differences in reproductive success in matched versus mixed pairs may have a balancing effect on the mating pattern between plumage morphs and may contribute to the maintenance of the color polymorphism in this species.
Key words: assortative mating, hatching date, offspring sex ratio, parental quality, plumage color polymorphism, selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Genetically determined color polymorphism is found in a variety of taxa and is defined as intraspecific color variation expressed in both sexes, independent of age and season (e.g., Butcher and Rohwer, 1989
; Huxley, 1955). Understanding color polymorphism has been a major challenge both in terms of underlying genetic mechanisms (e.g., Franck et al., 2001; Mundy et al., 2004; Nachman et al., 2003; Ritland et al., 2001) and the evolutionary forces maintaining it (Fowlie and Krüger, 2003; Galeotti et al., 2003; Lank, 2002; Mayr, 1963). In birds, plumage color polymorphism is found in 3.5% of all species and is particularly common among tubenoses (Procellariiformes), birds of prey (Accipitridae and Falconidae), owls (Strigiformes), cuckoos (Cuculiformes), herons (Ardeidae), and jaegers and skuas (Stercorariidae) (Fowlie and Krüger, 2003; Galeotti et al., 2003).
The parasitic jaeger (Stercorarius parasiticus) (known as Arctic skua to European ornithologists) is a monogamous, size-dimorphic seabird, which represents one of the classic examples of plumage color polymorphism in birds (e.g., Furness, 1987; O'Donald, 1983). Jaeger phenotypes have usually been categorized as pale, intermediate, and dark. Intermediate and dark jaegers are sometimes difficult to distinguish and are often jointly referred to as melanic. Plumage differences were recently found to associate with variation at the melanocortin-1-receptor gene (Mundy et al., 2004), which is a key regulator of melanogenesis in vertebrates (Barsh, 1996). Melanic jaegers are either homozygous or heterozygous for a "dark" allele that is incompletely dominant over the "pale" allele (O'Donald, 1983; Mundy et al., 2004). The ratio of melanic to pale jaegers shows a latitudinal cline throughout the circumpolar breeding range. The melanic plumage morph is more frequent than the pale morph at low latitudes but is virtually absent at high latitudes (O'Donald, 1983). Numerous hypotheses related to feeding ecology, timing of breeding, and sexual selection have been proposed, seeking to explain the observed pattern (Andersson, 1976; Árnason, 1978; Bengtson and Owen, 1973; Berry and Davis, 1970; Berry and Johnston, 1980; Furness BL and Furness RW, 1980; Jones, 2002; O'Donald, 1983, 1987; Paulson, 1973; Phillips and Furness, 1998; for a review, see Furness, 1987). Despite these efforts, the understanding of how the polymorphism may be maintained remains incomplete.
So far, there has been variable evidence for fitness differences among plumage color morphs in the parasitic jaeger. While there were no differences in a study in Foula, Scotland (Phillips and Furness, 1998), other studies suggested sex-related fitness differences in relation to plumage color morph. First, pale females and melanic males were more frequent than would be expected from random distribution of plumage color among sexes in several study sites (Berry, 1977; Berry and Davis, 1970; Cramp and Simons, 1983; Furness, 1987; O'Donald, 1983; Perry, 1948). Second, in an extensive long-term study in Fair Isle, Scotland, O'Donald (1983, 1987) showed that melanic males, including first-time breeders and experienced breeders mating with a new female, had earlier laying dates and higher breeding success than pale males in their first year of breeding but not in subsequent years. These findings suggest a sexual selective advantage in melanic males that may be partly offset because pale birds start breeding at a younger age (O'Donald, 1983). Pale females may then gain a selective advantage over melanic females simply because of their younger age at first reproduction. Thus, pale female and melanic male parasitic jaegers may have a selective advantage in populations inhabited by both plumage morphs, hereafter referred to as "sex-dependent selection hypothesis" (SSH).
According to sex ratio theory, environmental, parental, and social factors may influence the fitness of male and female offspring differentially. Parents would maximize their fitness by facultatively biasing their primary offspring sex ratio (i.e., offspring sex ratio at conception) relative to the expected fitness functions for sons and daughters (Charnov, 1982; Frank, 1990; Sheldon, 1998; Trivers and Willard, 1973; Werren and Charnov, 1978;). An accumulating number of empirical studies have shown that female birds may adjust their brood sex ratio relative to variation in territory quality (e.g., Komdeur et al., 1997), male quality (e.g., Sheldon et al., 1999; Svensson and Nilsson, 1996), female condition (e.g., Nager et al., 1999), timing of breeding within the season (e.g., Daan et al., 1996; Dikstra et al., 1990), or sexual size dimorphism (e.g., Kalmbach et al., 2001) and also with laying order (Badyaev et al., 2002; Clotfelter, 1996; Kilner, 1998; Krebs et al., 2002). However, there are studies that have not found evidence for facultative sex ratio adjustment or that have revealed variable results. Several reasons have been suggested, for example, sample sizes are often too small in relation to the small proportion of variance in sex ratio, which is explained by sex ratio adjustment, or sex ratio allocation will only be favored when the fitness benefits are greater than its costs (West and Sheldon, 2002, and references therein). There are alternative strategies to allocate resources differentially between offspring, like sex-dependent provisioning of eggs (Anderson et al., 1997; Cordero et al., 2000, 2001; Cunningham and Russell, 2000; Magrath et al., 2003) and sex-dependent provisioning of nestlings, which may lead to a biased secondary offspring sex ratio (reviewed in Lessells, 2002).
If selection favors pale females and dark males in polymorphic populations of parasitic jaegers, parents would maximize their fitness by adjusting their brood sex ratio relative to their plumage color. Thus, a prediction in line with the SSH would be that pale females bias their offspring sex ratio toward daughters when mated to pale males, while melanic females overproduce sons when mated to melanic males. Additionally, females might choose to mate assortatively with a partner of the same plumage color to maximize the probability of producing either pale or melanic offspring. However, further factors may potentially influence decisions on brood sex ratio. In species with sexual size dimorphism, offspring of the larger sex typically consume more parental resources (e.g., Anderson et al., 1993; Daunt et al., 2001; Fiala and Congdon, 1983), which has been shown to affect the brood sex ratio in favor of the smaller, less costly sex under adverse conditions (e.g., Kalmbach et al., 2001; Nager et al., 1999). In parasitic jaegers, females are, on average, 16% larger than males (Furness, 1987), suggesting differential rearing costs between the sexes. Consequently, pairs with low quality and/or under poor environmental conditions may bias their brood sex ratio toward smaller, less costly sons. Thus, predictions based on differential rearing costs may either enhance or be in conflict with those from the SSH.
We examined offspring sex ratio allocation, reproductive variables indicative of parental quality, and mating pattern in relation to plumage color in pairs of parasitic jaegers in a colony of parasitic jaegers in northern Norway in order to test the above hypotheses and to deepen our understanding of how the plumage color polymorphism is maintained in this species.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Fieldwork and sampling
Fieldwork was carried out at a colony of approximately 250 breeding pairs of parasitic jaegers at Slettnes, northern Norway (71° 05' N, 28° 13' E), during the 1997 and 1998 breeding seasons. Thus, large sample sizes could be obtained for robust statistical analyses. Two plumage color morphs, pale and melanic, were recorded among breeding adult jaegers. The pale morph has a pale ventral plumage, sometimes with a dark breast band, and is easily distinguishable from the melanic morph, which is more or less uniformly brown, consisting of both homozygous dark and heterozygous birds (Mundy et al., 2004
; O'Donald, 1983). In 1998, we attempted to divide the melanic morph further into the dark (homozygous) and the intermediate (heterozygous) morph, in order to analyze allele frequencies among sexes and to estimate the probability of producing pale and melanic offspring in different pair combinations. The intermediate morph has paler neck sides, which are sometimes expressed as only a few straw-colored feathers on either side of the neck, contrasting with the darker cap, while dark birds are uniformly dark brown (O'Donald, 1983).
In morph-uniform matings, the sex ratio must be equal within melanic x melanic and pale x pale pairs, respectively. In mixed pairs, we sexed the individuals by either observing courtship feeding or copulations or simply making use of the fact that females rarely leave the territory during the incubation period while males provide them with food (Furness, 1987). Pairs were divided into four color morph combinations: pale female x pale male (matched pale), pale female x melanic male, melanic female x pale male, and melanic female x melanic male (matched melanic). These sex and plumage color combinations were successfully determined in 165/208 nests in 1997 and 186/196 nests in 1998. The frequencies of pair combinations were also used to test for nonrandom assortment of color morphs within pairs and proportion of plumage morphs among adult females and males (see below).
Nests contained one or two eggs that were marked individually. Nests were checked every second day until hatching to determine the exact hatching date and hatching order of chicks. Hatching date of the clutch was defined by the hatching date of the first egg (expressed in number of days from 15 June). Egg size was determined by calculating their volume [(length x breadth2)/2000]. In some clutches, one or both eggs failed to hatch (17.9% of chicks in clutches with known parental plumage color combination in 1997 [46 broods] and 15.6% in 1998 [42 broods]). Chicks were individually marked with masking tape attached around the tarsus, until large enough for permanent leg bands. Blood samples for molecular sexing were taken from the underwing vein when chicks were about 2 days old to determine the sex ratio as close as possible to the primary sex ratio. Some chicks were lost between hatching and blood sampling due to death, predation, or our failure to find them (9.3% of hatchlings in clutches with known parental plumage color combination in 1997 [19 broods] and 3.0% in 1998 [eight broods]). Approximately 10–20 µl of blood was stored in 500 µl SET buffer (0.1 M Tris–HCl, pH 8.0, 0.01 M NaCl, 1.0 mM EDTA [ethylenediaminetetracetic acid]) and kept cool until later analysis.
Territories were revisited at day 25 after hatching to measure relative chick mortality by recovery rate. Chicks not present either were dead or had an unknown fate, including our failure to find them (chicks leave the nests and hide in the territory well camouflaged against the tundra vegetation). The latter was assumed to be independent of parental plumage color.
Chick mortality could not be measured for late clutches (hatched later than 26 days after 15 June in both years) because of logistic reasons, and data from 8.5% of chicks (14 broods) in 1997 and 14.5% of chicks (27 broods) in 1998 were lost in clutches with known parental plumage color combination.
Laboratory analyses
The laboratory work was carried out at the Department of Animal Ecology, University of Lund, Sweden (samples from 1997), and at the Department for Molecular Biotechnology, University of Tromsø, Norway (samples from 1998). Total genomic DNA was isolated from blood samples using standard sodium dodecyl sulfate lysis and proteinase K digestion followed by phenol–chloroform extraction and ethanol precipitation protocols (Sambrook et al., 1989). Offspring sex was determined using polymerase chain reaction (PCR) amplification of a part of the CHD1 gene present on the avian sex chromosomes (CHD1-W gene on the W chromosome and CHD-Z gene on the Z chromosome). In 1997, we followed methods described by Griffiths et al. (1996) using primers P2 and P3. The PCR product (110 bp) was digested with HaeIII (restriction site present in the CHD1-W gene only), and the resulting fragments were electrophoresed in a 10% native acrylamide gel at 4 Vcm–1 for 2–3 h. In 1998, we followed methods described in Griffiths et al. (1998), using primers P2 and P8. PCR products (ca. 300 and 500 bp) were separated by electrophoresis in a 3% agarose gel at 8 Vcm–1 for 40 min. Both types of gels were stained with ethidium bromide, and products (one DNA band in males and two in females in both methods) were visualized in UV light. The sex ratio is given as the proportion of males.
Statistical analyses
The original data on plumage color morphs within parasitic jaeger pairs were biased toward pairs in which both individuals had the same plumage color (matched pairs), which should be accounted for when testing for nonrandom assortment of color morphs within pairs and calculating differences in plumage color morphs and allele frequencies between sexes. It was impossible to determine the sex of every adult, but in matched pairs, one individual had to be the female and the other the male. Therefore, there are relatively more matched pairs than pairs in which the individuals look different (mixed pairs). We calculated the proportion of pairs with known sex out of all mixed pairs. Then, we corrected the number of matched pairs by subtracting an equivalent proportion. Because there were less mixed pairs with undetermined sex in 1998 than in 1997, we present data for 1998 only.
The plumage morph of juveniles produced by different pair combinations could not be identified by their phenotype because juvenile plumage color is only to a certain degree correlated with the plumage color these birds will have as adults (Janssen, 1998; O'Donald, 1983). Therefore, we estimated the probability of plumage color morph frequencies among chicks produced by different pair combinations, based on parental genotypes and Mendelian inheritance of the gene determining plumage color (single locus with two alleles, pale [a] and dark [A]), assuming random segregation of alleles. We determined adult genotypes by using three plumage morph categories in data from 1998 (see above), thereby separating between homozygous and heterozygous melanic birds. For each combination of color morphs in adults, we calculated the expected proportions of the color morphs in offspring, based on the empirically derived proportion of heterozygosity among melanic birds (Table 1). Matched pale pairs (pale female x pale male) are expected to produce all pale offspring. Mixed pairs, containing one pale and one melanic parent, are expected to produce 62% melanic offspring (all heterozygous), while matched melanic pairs (melanic female x melanic male) are expected to produce 86% melanic offspring (both heterozygous and homozygous dark).
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The following analyses are based on pairs in which plumage morph (pale and melanic) and sex was determined in both parents (n = 165 in 1997 and n = 186 in 1998). Of these, 28 out of 165 (1997) and 19 out of 186 (1998) produced one-egg clutches, while the remaining produced two-egg clutches. Analyses including effects of hatching order were restricted to two-egg clutches only. To analyze sex ratio and offspring mortality, we employed general linear mixed models with binominal errors and a logit link function. Analyses were carried out in SAS utilizing the PROC MIXED procedure (SAS Institute Inc., 1999
). To analyze the sex ratio and chick mortality at the brood level, we used either the number of male offspring or the number of chicks surviving to day 25 as response variable and brood size or number of chicks hatched as the binominal denominator. Furthermore, we carried out analyses of sex ratio and chick mortality at the individual level. In these analyses, either the sex of offspring or chick mortality was the response variable and hatching order of chicks was a factor. To correct for overdispersion, we used nest identity as a random factor. The dispersion factor was close to 1 or slightly above in all analyses, and the significance of the parameters was tested by F tests. The analyses were performed employing the glimmix macro developed by SAS (http://support.sas.com/rnd/app/da/glimmix.html). In all logistic models, we used a backward procedure in which all nonsignificant explanatory variables and interaction terms were removed. The variation in egg volume was analyzed employing general linear models. These analyses were also carried out both at the brood level and at the individual level, using egg hatching order as a factor. At the individual level, we used nest identity as a random factor to correct for pseudoreplications.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Adult plumage color morphs
In both years, the proportion of the pale color morph was about 30% among breeding parasitic jaegers at Slettnes. The following analyses of nonrandom mating and proportion of plumage color among sexes are based on data from 1998 only. The sample includes 175 pairs with known plumage color and sex after correction for sampling bias (see Methods). A total of 33.1% of females and 26.3% of males were pale. Although indicating a surplus of pale females and melanic males, this ratio was not significantly different from 1:1 (
2 = 1.97, n = 350, df = 1, p = .16). However, frequencies of the pale and dark allele as obtained from data using three plumage morphs including 164 pairs differed between sexes (2 = 3.89, n = 656, df = 1, p = .05). The proportion of the pale allele was higher among females (61.0%) than males (53.4%). Frequencies of pair combinations of plumage color morphs showed a trend for nonrandom assortment (Table 2).
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Breeding data
The mean hatching date did not differ between the four pair combinations (F = 0.77, df = 3,311, p = .51) but was different between years (1997: 18.6 ± 0.5; 1998: 16.8 ± 0.7, F = 4.5, df = 1,311, p = .03). Females produced either one-egg or two-egg clutches, the latter being the most common in both years (1997: 83.0%, n = 165; 1998: 89.7%, n = 186). A logistic model showed that clutch size did not vary among pair combinations (
2 = 0.25, df = 3,350, p = .97), but clutches tended to be larger in 1998 than in 1997 (2 = 3.26, df = 1,350, p = .07). Mean egg volume did not differ between pair combinations (F = 0.36, df = 1, 265, p = .47) but decreased strongly with later hatching date (F = 11.5, df = 1, 265, p < .001). Also, the mean egg volume was slightly larger in two-egg compared to one-egg clutches (F = 3.64, df = 1,265, p = .06) and was larger in 1998 than in 1997 (F = 23.8, df = 1,265, p < .001). We analyzed the variation in egg volume in more detail in two-egg clutches only, including also egg hatching order and offspring sex in the model. This model showed that egg volume differed significantly between years, pair combinations, and with offspring sex and hatching date but did not relate to egg hatching order (Table 3). Mean egg volume was smaller among matched pair combinations compared to mixed pairs (Table 4). Moreover, egg volume decreased with later hatching date among all pair combinations. Interestingly, mean egg volume was larger in male eggs than in female eggs (Table 4).
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Sex ratio
We determined the sex of 572 hatchlings from completely hatched clutches. The offspring sex ratio (here reported as the proportion of males) was 49.5% and did not depart from unity but tended to be lower in 1997 than in 1998 (1997: 46.9%, n = 277; 1998: 51.9%, n = 295). There was also a tendency for sex ratio being higher among two-egg clutches (50.2%, n = 534) than among one-egg clutches (44.7%, n = 38). However, neither year nor clutch size proved significant in the logistic model (Table 5). Overall, the brood sex ratio at hatching differed between pair combinations, as illustrated by a lower offspring sex ratio in matched pale and mixed pairs compared to matched melanic pairs (Figure 3). A strong interaction between hatching date and pair combination suggested that pair combinations produced different sex ratios at different times throughout the breeding season (Table 5). We analyzed this effect in more detail by using only two-egg clutches, including also hatching order of chicks in the model. The results were similar: offspring sex did not relate to hatching order or year but differed significantly among pair combinations. Likewise, there was a strong interaction between pair combination and hatching date (Table 6). Apparently, pair combinations in which one or both of the partners were pale produced a surplus of daughters early and more sons late in the season. The opposite trend was evident in melanic pairs. They produced males early and daughters late in the season (Figure 1a).
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Offspring mortality
The offspring mortality as measured at day 25 increased rapidly in later hatching clutches (Table 7, Figure 1b). However, mixed pairs produced more offspring than matched pale and melanic pairs (Figure 2). There was also an interaction between pair combination and hatching date in the model (Table 7), which was due to the fact that offspring mortality in matched melanic pairs was relatively higher in early and relatively lower in late clutches compared to other pair combinations (Figure 1b). There was no difference in mortality between male and female offspring or first- and second-hatched chicks when controlling for hatching date (Table 7).
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Chicks produced by different pair combinations
Because matched pale pairs and mixed pairs skewed their offspring sex ratio toward daughters early in the season, when the offspring mortality was low, they produced even more daughters at day 25 (Figure 3). The opposite was true for matched melanic pairs. They produced an excess of sons early in the season, resulting in more surviving male offspring (Figure 3). Thus, the bias in sex ratio at hatching was enhanced at day 25 by producing the favored sex when mortality was the lowest. By assuming an independent segregation of alleles (relative to offspring sex), we can calculate the probability of offspring plumage color frequencies produced by different pair combinations (see above). The biased sex ratios would then translate into an excess of pale daughters in matched pale pairs, an excess of daughters of which 62% would be melanic in mixed pairs, and a surplus of sons of which 86% would be melanic in matched melanic pairs.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sex-biased parental investment
Female parasitic jaegers at Slettnes biased their clutch sex ratios independent of hatching sequence. We assume that the observed sex ratio, here measured 2 days after hatching, is closely related to the primary sex ratio, although we were not able to control for prehatching mortality. Because parasitic jaegers have only two chicks that had equal survival prospects, it seems unnecessary for a female jaeger to allocate resources differentially with hatching order. The biased secondary sex ratio (day 25 after hatching) was the result of seasonally changing sex ratios together with increasing mortality in later clutches rather than differential mortality between the sexes. Eggs of the smaller male sex were significantly larger than eggs of the larger female sex, independent of hatching order. Such disparities in egg size between sexes have previously been reported in other size-dimorphic species, for example, American kestrel (Falco sparverius, Anderson et al., 1997
) and brown song lark (Cinclorhamphus cruralis, Magrath et al., 2003). It has been suggested that chicks of the smaller sex may be at a considerable size disadvantage when competing for food with their faster growing siblings (Stamps, 1990; Oddie, 2000). Mothers may therefore seek to temporarily offset this disadvantage by provisioning eggs of the smaller sex with more resources (Magrath et al., 2003).
Differential offspring sex allocation between parent pair combinations
According to the SSH, pale females and melanic males may gain a selective advantage in polymorphic parasitic jaeger populations. Therefore, we predicted that females might bias their offspring sex ratio when mated to a partner of the same plumage morph, thereby utilizing the high probability of producing either pale female or melanic male offspring. However, the female's decision of what offspring sex to produce may also be influenced by parental quality and/or environmental conditions because costs of rearing male and female offspring are likely to differ in the parasitic jaeger, in which females are 16% larger than males (Furness, 1987). Experimental studies in the related great skua (Catharacta skua, Kalmbach et al., 2001) and lesser black-backed gull (Larus fuscus, Nager et al., 1999) support the hypothesis that females in size-dimorphic species overproduce the smaller sex under adverse conditions. Increased rearing costs of the larger sex have been demonstrated in several species (e.g., Anderson et al., 1993; Daunt et al., 2001; Fiala and Congdon, 1983; Teather, 1987).
Although the overall population offspring sex ratio at hatching did not depart from unity, there were two clearly opposing strategies of sex ratio allocation among different pair color combinations in parasitic jaegers at Slettnes, indicating that costs and benefits of allocating resources to either offspring sex may differ between these. Matched pale and mixed pairs biased their offspring sex ratio toward daughters among early hatchlings and toward sons in late clutches. In contrast, matched melanic pairs produced male hatchlings early and daughters late. Because of the strong seasonal decline in reproductive success, jaegers should produce the most beneficial and/or the most costly sex in early clutches and the less beneficial and/or less costly sex in late clutches. In the following, we will discuss possible costs and benefits potentially affecting offspring sex ratio in different pair combinations in detail.
Matched pale and melanic pairs that have the highest probabilities of conceiving pale and melanic offspring, respectively, allocated their resources concordant with the SSH, producing a surplus of either pale female or melanic male offspring in early clutches as well as in total. Mixed pairs produced a surplus of daughters of which 62% are likely to be melanic, which is inconsistent with the SSH. Because of higher rearing costs of female compared to male offspring, parents should bias their offspring sex ratio toward daughters in early clutches and toward sons in late clutches. Matched pale pairs and mixed pairs allocated their resources accordingly, while results for matched melanic pairs were contrary to expectations. However, differences in parental resources may be more subtle between pair combinations than simply showing a decline from early to late breeders. Mixed pairs may generally be of better quality than matched pairs. Neither mean clutch size nor mean laying date differed between pair combinations, but mean egg volume and reproductive success were higher in mixed than matched pairs. Egg volume and chick survival are positively correlated in a wide range of bird species (e.g., Williams, 1994) and are often an indicator of parental quality. So far, studies have not found considerable differences in reproductive success among parasitic jaeger plumage color phenotypes (Furness, 1987; O'Donald, 1983, 1987; Phillips and Furness, 1998). In our study, mixed and matched melanic pairs produced offspring sex ratios corresponding to their "mean" quality, costly daughters in high-quality mixed pairs and less costly sons in low-quality matched melanic pairs. In contrast, matched pale pairs invested in costly daughters despite their comparably low quality, indicating that the benefits of producing pale female offspring may be so strong that they are willing to pay extra costs, in support of the SSH. Thus, the offspring sex ratio produced by different pair combinations cannot be explained by differential rearing costs of female and male offspring in relation to seasonal decline and/or differences in parental quality or selection for pale females and melanic males alone but is more likely a combination of these factors. Conversely, the female-biased offspring sex ratio in late-breeding matched melanic pairs is in conflict with any of the above explanations.
Interestingly, the offspring sex ratio over the season was correlated with chick mortality in different pair combinations. Although chick mortality increased with hatching date in all pair combinations, it was always relatively lower when the sex ratio was biased toward costly daughters, for example, offspring mortality was relatively higher among matched melanic pairs early in the season when they favored male offspring but was relatively lower in late-breeding pairs when they biased their offspring sex ratio toward daughters. The relative differences in chick mortality over the season may reflect a difference in relative parental quality between pair combinations, in contradiction to the SSH. Alternatively, not contradictory to the SSH, parents may feed female-biased clutches more. It has been shown that seabirds, including jaegers and skuas, have a considerable scope to adjust activity budgets, making them capable of increasing the amount of time spent foraging (Caldow and Furness, 2000; Hamer et al., 1993; Monaghan et al., 1989; Phillips et al., 1996; Uttley et al., 1994).
One further aspect is striking. Matched pale and mixed pairs constitute about half of the population at Slettnes, while matched melanic pairs represent the other half. Reproductive strategies with respect to offspring sex ratio were opposite in these two groups, also changing between early and late breeders. If one group maximizes its fitness by skewing the offspring sex ratio toward one sex, it may be advantageous for the other group to overproduce the opposite offspring sex. Such frequency-dependent selection resulting in an equal sex ratio at the population level was first proposed by Fisher (1930). However, empirical evidence is scarce (Bensch et al., 1999, and references therein).
Overall, several costs and benefits, which appear to differ between plumage color pair combinations, may affect a female's decision of which offspring sex to produce. Thereby, different pair combinations overproduce a certain sex and plumage color combination in their offspring. This is the first study to our knowledge showing two clearly opposing strategies of sex ratio allocation within the same population, correlated with a plumage trait expressed identically in both males and females.
So far, we have indications that females in matched pairs may allocate their resources in agreement with the SSH, producing a surplus of potentially advantageous pale females and melanic males. Further observations support differential selection on plumage color in the sexes. Pale jaegers started to reproduce, on average, 0.6 years earlier than melanic jaegers (O'Donald, 1983, 1987). Furthermore, melanic males, including first-time breeders and experienced breeders mating with a new female, had an earlier laying date and higher breeding success than pale males in their first year of breeding but not subsequently (O'Donald, 1983, 1987; but see Phillips and Furness, 1998). It has been suggested that this selective advantage in melanic males may partly be offset by the pale jaegers' younger age of first reproduction. Pale females may simply gain a selective advantage over melanic females because of their earlier reproduction. However, we do not know if the relatively small difference in age of first breeding has significant consequences for the lifetime reproductive success of a long-lived species like the parasitic jaeger.
Our results encourage further studies searching for potential selective differences between plumage color morphs in male and female parasitic jaegers. Interestingly, the closely related south polar skua (Catharacta maccormicki) exhibits a similar plumage color polymorphism with strongly sex-related differences in morph frequencies biased toward pale females and dark males (Ainley et al., 1985; Bustnes JO and Janssen K, personal communication). Yet, we are not able to rule out that the observed surplus of pale female and melanic male offspring in matched pairs is the consequence of, and not the reason for, differential resource allocation. Further investigations, including experimental studies, are needed to understand in detail how reproductive differences between pair combinations and selection for certain plumage morphs may affect the offspring sex ratio allocation and reproductive success over a longer period of time. For example, subtle differences in reproductive success have been found among plumage color pair combinations of northern fulmars (Fulmarus glacilis) in Alaska. Pairs including at least one individual of the light morph had lower breeding success than matched dark pairs in 1 out of 6 years, whereas matched dark pairs either skipped more breeding attempts or had lower overwinter survival than light birds (Hatch, 1991).
Assortative mating and the maintenance of the polymorphism
We found a tendency for more matched pale and melanic pairs among parasitic jaegers than expected from random mating. This is in line with other findings that do not allow for clear conclusions whether or not assortative mating occurs in this species. Earlier findings were inconsistent between colonies and years and often depended on the type of analytical approach used (for discussion, see O'Donald, 1987; Phillips and Furness, 1998). The two reproductive strategies suggested in the present study may together explain why no strong assortative mating is expected to occur. On one hand, the proposed opposing selection for pale female and melanic parasitic jaegers alone would likely result in assortative mating because females would thereby maximize the probability of producing either pale or melanic offspring. On the other hand, the higher reproductive success in mixed pairs may compensate for the disadvantage of producing less offspring possessing the advantageous plumage color and sex combination. Alone higher reproduction in mixed pairs would likely lead to disassortative mating. Consequently, both processes may balance each other, partially or completely. Mating in several other polymorphic species appears to be at random, for example, in the northern fulmar (Hatch, 1991) and little shag (Phalacrocorax melanoleucus brevirostris, Dowding and Taylor, 1987), while assortative mating governed by imprinting has been found in the lesser snow goose (Anser caerulescens, Cooke et al., 1976) and common buzzard (Buteo buteo, Krüger et al., 2001). Furthermore, the reproductive strategies found at Slettnes can potentially contribute to the maintenance of the plumage color polymorphism in the parasitic jaeger. The overproduction of pale female and melanic male offspring in matched pairs, independent of being the result of opposing selection for plumage color between sexes or being the consequence of differential sex ratio allocation based on other criteria, could maintain the polymorphism. If mixed pairs have a consistently higher breeding success that translates further into higher fitness compared to matched pairs, the polymorphism would also be maintained. Further work is needed to test these suggestions.
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ACKNOWLEDGEMENTS |
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We thank Hans Källander, Truls Moum, and two anonymous reviewers for helpful discussion and comments on the manuscript. Financial support was provided by the Norwegian Research Council (doctoral scholarship to K.J.) and the German Ornithologists' Society (travel grant to K.J.).
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