TY - JOUR
AU - Berg, Elena, C.
AB - Abstract Recent studies suggest that many bird species are able to vary the sex ratio of their young. Among cooperative breeders, in which adult helpers aid the genetic parents in the rearing of young, two models have been invoked to explain this variation. According to the local resource competition hypothesis, parents should bias offspring sex ratios toward the dispersing sex in order to minimize competition for local resources. In contrast, the local resource enhancement (or “production of helpers”) hypothesis states that parents should overproduce the nondispersing sex if the presence of relatives enhances reproductive success. I examined these models in a Costa Rican population of White-throated Magpie-Jays (Calocitta formosa), a cooperatively breeding corvid with female helpers. Using DNA microsatellite analysis, I sexed 135 offspring from 38 broods and 14 groups over 3 years. I tested for variation in offspring sex ratio at the population level and as a function of social group, helper number, breeding female, and season. Unlike studies of the Seychelles Warbler (Acrocephalus sechellensis), one of the few other avian species with primarily female helpers, I found no evidence for systematic sex-ratio bias supporting either hypothesis. This suggests that female-biased helping is not a sufficient condition for the evolution of offspring sex-ratio biasing. Estudio del Sesgo en el Cociente de Sexos en Calocitta formosa, una Reproductora Cooperativa con Ayudantes Hembras Resumen. Estudios recientes sugieren que muchas especies de aves pueden hacer variar el cociente de sexos de sus crías. Se han utilizado dos modelos teóricos para explicar esta variación en las aves que se reproducen en forma cooperativa, en las cuales los adultos ayudan a los padres genéticos con el cuidado de sus crías. Según la hipótesis de competencia por recursos locales, los padres deben sesgar el cociente de sexos de su prole en favor del sexo que se dispersa con el fin de minimizar la competencia por los recursos locales. Por el contrario, según la hipótesis de incremento de recursos locales (o “producción de ayudantes”), los padres deben sobreproducir el sexo que no se dispersa si la presencia de parientes favorece el éxito reproductivo. Yo estudié estos modelos en una población costarricense de urracas (Calocitta formosa), un córvido de reproducción cooperativa con ayudantes hembras. Utilicé análisis de ADN microsatelital para averiguar el sexo de 135 crías provenientes de 38 nidadas y 14 grupos a lo largo de un período de tres años. Documenté las variaciones en el cociente de sexos de las crías a nivel poblacional y como función del grupo social, la cantidad de ayudantes, la hembra reproductiva y la estación del año. A diferencia de lo encontrado para el caso de Acrocephalus sechellensis, una de las pocas especies de aves con ayudantes principalmente hembras, no encontré indicios de sesgo sistemático en el cociente de sexos que avalara ninguna de las dos hipótesis. Esto sugiere que la ayuda por parte de las hembras no constituye una condición que determine la evolución de un sesgo en el cociente de sexos de las crías. Introduction Recent studies suggest that many birds vary the primary sex ratio of their broods (Hardy 2002, Hasselquist and Kempenaers 2002). Two specific models have been developed to explain patterns of offspring sex-ratio biasing in species with sex-biased dispersal: the local resource competition model and the local resource enhancement model. According to the local resource competition hypothesis, parents should produce offspring sex ratios that minimize competition for local resources (Hamilton 1967, Clark 1978, Clutton-Brock 1986) by biasing production toward the dispersing sex. However, under local resource enhancement parents should overproduce the philopatric sex whenever the presence of additional relatives increases the reproductive output of the natal group (Clark 1978, Gowaty and Lennartz 1985, Emlen et al. 1986, Lessells and Avery 1987). For species that show clear biases in offspring sex ratio, these two models provide a framework for investigating the evolution of alternative reproductive strategies. First proposed by Gowaty and Lennartz (1985), the “production-of-helpers” hypothesis is a special case of local resource enhancement that applies specifically to cooperative breeders (Clutton-Brock 1986, Emlen et al. 1986, Lessells and Avery 1987, Koenig and Walters 1999). Cooperative breeding, the social system in which adult individuals aid genetic parents in the rearing of young, occurs frequently in birds (Brown 1987, Stacey and Koenig 1990). Helpers contribute to breeding efforts in a variety of ways, including nest building, provisioning of incubating individuals, nest defense, and brood care. The production-of-helpers model assumes that (1) helpers significantly enhance parental fitness, and (2) helpers are primarily of one sex. Under conditions where additional helpers would increase the reproductive output of the group, parents should overproduce the helping sex. Evidence for this model has been found in several species, including Red-cockaded Woodpeckers (Picoides borealis; Gowaty and Lennartz 1985) and Green Woodhoopoes (Phoeniculus purpureus; Ligon and Ligon 1990). Predicting the direction of sex allocation in cooperative breeders can be difficult, since both local resource competition and enhancement may be acting at the same time (Komdeur et al. 1997, Koenig and Walters 1999, Hasselquist and Kempenaers 2002). The optima for different breeders may vary with territory quality, helper number, or mate quality, and these individual optima may not result in biases at the population level (Pen and Weissing 2000, Cockburn et al. 2002, Komdeur and Pen 2002). One of the best examples of this interplay between local resource competition and enhancement is in the Seychelles Warbler (Acrocephalus sechellensis), a cooperative breeder with female helpers (Komdeur 1996, Komdeur et al. 1997, 2002). Breeding pairs on high quality territories with fewer than two helpers produce 87% daughters (local resource enhancement), while pairs on low quality territories produce only 23% daughters, regardless of helper number (local resource competition; Komdeur et al. 1997). The aim of this study is to test the local resource enhancement (production-of-helpers) and local resource competition hypotheses in a Costa Rican population of White-throated Magpie-Jays (Calocitta formosa), a cooperatively breeding corvid. The magpie-jay is an ideal candidate for this type of analysis, because (1) helping increases the reproductive success of parents (Langen and Vehrencamp 1999), and (2) there are clear sex biases in helping behavior (88–93% are females; Langen 1996, ECB, unpubl. data). In most cooperatively breeding birds, male offspring remain as helpers-at-the-nest, while female young tend to disperse earlier and breed independently (Greenwood 1980). In the White- throated Magpie-Jay and Seychelles Warbler, the opposite is true. The White-throated Magpie-Jay system provides an excellent opportunity to test whether the predictions of the two models are met consistently in species with atypical sex biases in dispersal and helping. If so, patterns of sex biasing in White-throated Magpie-Jays should be similar to those in the Seychelles Warbler. If local resource enhancement is driving the differential production of sons and daughters in the magpie-jay, population-level offspring sex ratios should be biased toward females, the helping sex. In contrast, if resource competition is driving this variation, sex ratios should be biased toward males, the dispersing sex. Finally, if the two mechanisms are operating in tandem, as in the Seychelles Warbler, the direction of sex-ratio biasing should depend on the resources available to each breeding female. Females should produce male-biased broods in the dry season, when food is limited (local resource competition), and female-biased broods in the wet season, when high-energy food sources are abundant (local resource enhancement). It follows that females should produce the helping sex (daughters) on high quality territories and the dispersing sex (sons) on low quality territories. In this study, it was not feasible to measure territory quality directly. However, previous studies of the magpie-jay showed that the number of successful nests per year increased with helper number (Langen and Vehrencamp 1999) and group size (Langen and Vehrencamp 1998). While the causal links between group size and territory quality are not well established, Langen and Vehrencamp (1998) did find that magpie-jay group size was positively correlated with the number of acacias (a preferred dry-season food) within a group's territory. One might therefore predict a negative relationship between group size (a proxy for resource availability) and sex ratio (proportion of males in clutch). Methods Study Site and Field Procedures Field research was conducted in the Santa Rosa sector of the Guanacaste Conservation Area in Guanacaste, Costa Rica (10°50′N, 85°37′W), where studies on the White-throated Magpie-Jay have been conducted intermittently since 1980. Habitat consists of a mix of pasture, woody vegetation, and secondary woodland and dry forest. Population density of magpie-jays in this area is high (approximately 0.3 jays per ha, Langen and Vehrencamp 1998), with jays defending year- round territories averaging 18.7 ha in size (range 10.6 to 30.5 ha; Langen 1996). Territories consist of both open pasture (for breeding) and forest (for foraging). The breeding season is over 6 months long (January–July), spanning both dry (December–May) and wet (May–December) seasons. Each group makes multiple nest attempts within each season (Innes 1992, Langen 1994, 1996, Langen and Vehrencamp 1998), allowing for extensive data collection on nesting behavior and reproductive success. Data on offspring sex ratios were collected between June 1999 and July 2002. DNA samples were collected from nestlings or embryos. Due to extremely high egg predation levels, few nestlings were available. Predators such as white-faced capuchins (Cebus capucinus), Collared Forest Falcons (Micrastur semitorquatus), spiny-tailed iguanas (Ctenosaura similis), and variegated squirrels (Sciurus variegatoides) were abundant, and egg and nestling predation levels reached 100% during the second and third years of the study. Therefore, I obtained most of my DNA samples from embryos following nest failure. To do this, I removed eggs from selected nests 3–4 days after the onset of incubation and replaced them with the same number of decoy eggs made from oven-baked Sculpey® modeling clay (Chenille Kraft, Gurnee, Illinois). Decoys were similar to real eggs in size, shape, and color, and behavioral observations during 2001 indicated that females readily accepted and incubated these decoys. In only one case did a female abandon her nest after I replaced her eggs with decoys. Waiting 3–4 days allowed females to settle into their incubation routines, minimizing the disturbance of egg replacement. The real eggs were artificially incubated in a Lyon Turnex-7 incubator (Lyon Electric Company, Chula Vista, California), an electric temperature- and humidity-controlled incubator with a built-in egg turning function. Temperature was maintained at 37.8°C, and relative humidity at 51% (28.9°C wet-bulb). These are the standard conditions used to incubate parrot eggs, which are similar in size and development (Hagen 2001). During 2001 and 2002 I artificially incubated 1–2 (and in one case three) clutches of eggs per female. Due to the inaccessible location of some nests (up to 20 m high, often on spindly branches), it was not possible to collect multiple clutches from all females. Once the eggs were exchanged, the nest was monitored approximately every other day using a mirror attached to an extension pole. If the nest succeeded (i.e., the decoy eggs remained in the nest and were incubated by the female), I returned the real eggs and removed the decoys once the nestlings began to pip out (about 20 days). I then waited until the nestlings were 10 days old before accessing the nest again to bleed and band the chicks. If predation was detected in a field nest (i.e., the decoy eggs disappeared), I treated the nest attempt as a failure and allowed the birds to renest. Evidence of teeth marks on discarded eggs suggested that nest predators such as monkeys and squirrels were responsible. In these cases, I removed that clutch of real eggs from the incubator, killed the embryos by cervical dislocation, and took brain and liver tissue samples for DNA analysis. Tissue samples were diced finely and stored in a DMSO salt solution (25 mM EDTA at pH 8.0, 20% DMSO, NaCl to saturation). I sampled embryos once they were at least a week old to ensure that enough tissue would be available for analysis. Whenever possible, nestlings were banded and blood samples were taken at approximately 10 days of age. Blood samples were taken from the brachial vein of the left wing using wing venipuncture. The area was sterilized using an alcohol swab, and the vein was pricked with a sterile 23-gauge 0.6-mm Monoject® hypodermic needle (Kendall Company, Mansfield, Massachusetts). I collected approximately 150–200 μL of blood from each bird in Fisherbrand micro- hematocrit capillary tubes (Fisher Scientific, Leicestershire, UK) and immediately transferred the blood to Eppendorf tubes filled with Longmire's blood buffer solution (100 mM Tris pH 8.0, 100 mM EDTA, 10 mM NaCl, 0.5% SDS). All samples were stored at 4°C. Adult birds from eight groups were trapped and banded using unique combinations of colored aluminum leg bands. Although magpie-jays have sexually dimorphic and individually distinct plumage patterns, the differences between individuals and sexes are often subtle, and leg bands provide a reliable way to identify individuals. Using leg bands and extensive behavioral observations, I was able to identify all members of the eight core groups and determine each bird's status as helper, breeder, or floater. Sex Determination Using microsatellite analysis, I sexed 135 nestlings and unhatched embryos. With the microsatellite primers P2 and P8, I used the polymerase chain reaction (PCR) to amplify part of the sex-linked CHD gene (CHD-W) in females, and its homologue (CHD-Z) in both sexes (Griffiths et al. 1998). I extracted DNA from blood samples using a Qiagen QIAmp Blood Mini Kit and from tissue samples using a Qiagen DNeasy Tissue Kit (Qiagen Inc., Valencia, California). Tissue samples were washed first in TLE to remove salt traces that might interfere with DNA extraction. After extraction, DNA was quantified to ensure that concentrations of each sample were approximately 20 ng per μL. PCR was carried out in an MJ Research Thermocycler on all samples using the sexing primers P2 and P8, one of which was labeled with fluorescein. PCR was performed in 10 μL reactions with 3 μL template DNA, 0.03 μL Taq DNA polymerase, 1 μL 10× LGL buffer, 0.3 μL 50 mM MgCl2, 1.0 μL 2 mM dNTP, and 0.4 μL each of 10 μM P2 (forward) and P8 (reverse) primers. The PCR profile was as follows: incubation at 94°C for 90 sec; 30 cycles of amplification at 48°C for 45 sec, 72°C for 45 sec, and 94°C for 30 sec; 48°C for 60 sec; and a final extension step at 72°C for 5 min. Electrophoresis of DNA was carried out on 5.5% acrylamide gels copolymerized with 8M urea. Gels were run on SA-32 vertical gel rigs from Life Technologies. Banding patterns were resolved using a Molecular Dynamics FluorImager™ 595 (Amersham Biosciences, Piscataway, New Jersey). For both sexes, there was a band at approximately 370 bp that corresponded to the CHD-Z gene. In females only, a second band (corresponding to the CHD-W gene) was present at approximately 390 bp. In cases where band patterns were unresolved or faint, the same PCR product was run again on a different gel. If the sex of the individual was still not clear, a second PCR was carried out on the extracted DNA. In a few cases it was necessary to extract additional DNA and repeat PCR and electrophoresis. Statistical Analyses To test for an overall population bias in sex ratio, I pooled offspring sex-ratio data from 38 clutches and 14 groups. Using SPSS for Windows (SPSS 2001), I performed a chi-square goodness-of-fit test to determine whether overall numbers of males and females differed significantly from 1:1. I created three generalized linear models (GLM) to determine whether there was variation in offspring sex ratios across Julian date, group size, or number of helpers during each breeding attempt. Group size was defined as the number of permanent adult residents within a territory. Number of helpers was the number of jays, aside from the nesting pair, that were observed provisioning either the incubating female or the nestlings. By assigning binomial error, the GLM technique is ideal for analyzing proportional (yes/no) data, which are not normally distributed (Crawley 1993, Wilson and Hardy 2002). Another advantage of this technique is that unlike classical regression or nonparametric statistics, it includes information about sample sizes. In a GLM, a weighted regression is performed, using individual sample sizes as weights. Accounting for sample size differences was crucial in this study, since the total number of offspring sampled varied widely across clutches. Models were built using the program Arc (version 1.04, Cook and Weisberg 2002). To investigate the influence of Julian date (season) on the proportion of sons, I used a GLM with logit link function and binomial error distribution. The unit of measurement was each brood (n = 38). For a well-fitting model, the residual mean deviance (residual deviance/residual df) should be approximately equal to one (and no greater than 1.5; Wilson and Hardy 2002). The null GLM (no explanatory terms other than the intercept) was used to determine whether the data conformed to the binomial distribution. I tested for a significant departure from the binomial distribution by comparing the null deviance against the χ2 distribution with the null degrees of freedom (Crawley 1993). I created a similar GLM to determine whether sex ratios varied with group size (a possible correlate of resource availability). Though group size and helper number are highly correlated, they do contain slightly different information about group dynamics. For this reason, I created a third GLM to test whether sex ratios varied with the number of helpers-at-the-nest during each nest attempt. A smaller dataset was used to build these two models, since information on helper number and group size was available only for eight groups and 32 clutches. Results A total of 135 eggs and nestlings were sampled from 38 clutches, 20 females, and 14 groups; 81% of the samples (n = 109) came from 13 females in eight core study groups. Data were collected from 98 embryos and 37 nestlings. Individual females nested up to eight times a season, and clutch sizes ranged from 2–6 (mean ± SD = 4 ± 0.96). Combining data on nestlings and embryos, there was an equal sex ratio in the study population (68 males and 67 females; Pearson χ21 = 0.01, P = 0.93). Since I sampled some offspring as embryos and others as nestlings, I conducted a second chi-square test to rule out potential sex differences in mortality between those two stages. The number of males and females did not differ from equality among embryos and nestlings (Fisher's Exact Test, P = 0.70). Among embryos, there were 46 females and 49 males, and among nestlings, there were 19 females and 17 males. The results of the first GLM indicated that Julian date was not a significant explanatory variable (Table 1, Fig. 1). The χ2 test of the null model indicated that the data were consistent with a binomial distribution (χ237 = 41.3, P > 0.25). The GLM fit the assumption of no dispersion (residual mean deviance = 1.11). Similarly, the results of the second GLM showed no significant effect of group size on brood sex ratio (Table 1, Fig. 2). The data were consistent with a binomial distribution (χ231 = 33.5, P > 0.25), and the assumption of no dispersion was met (residual mean deviance = 1.08). Finally, the results of the third GLM showed no significant effect of helper number on proportion of male offspring (Table 1, Fig. 2). The data were consistent with a binomial distribution (χ231 = 33.5, P > 0.25), and the assumption of no dispersion was met (residual mean deviance = 1.11). The number of helpers at each nest ranged from 0–5. Table 1. Results of three separate generalized linear models analyzing the effects of Julian date, number of permanent adult residents in group (group size), and number of helpers on brood sex ratio in White-throated Magpie-Jays Open in new tab Table 1. Results of three separate generalized linear models analyzing the effects of Julian date, number of permanent adult residents in group (group size), and number of helpers on brood sex ratio in White-throated Magpie-Jays Open in new tab Figure 1. Open in new tabDownload slide Scatterplot of White-throated Magpie-Jay offspring sex ratio (number of males/number of females) by Julian date of nest initiation. Data limited to eight central groups (32 clutches) and pooled for all years. Each group is represented by a different symbol Figure 1. Open in new tabDownload slide Scatterplot of White-throated Magpie-Jay offspring sex ratio (number of males/number of females) by Julian date of nest initiation. Data limited to eight central groups (32 clutches) and pooled for all years. Each group is represented by a different symbol Figure 2. Open in new tabDownload slide Box plots of White-throated Magpie-Jay brood sex ratio by (A) group size during each nest attempt, and (B) number of helpers per group. Data are from the eight groups for which breeder identities, group size, and number of helpers were known. Dark lines represent median values, boxes represent the middle 50% of the distribution, and whisker bars indicate the highest and lowest values. The number of clutches sampled for each group size or helper number category is listed above median bars Figure 2. Open in new tabDownload slide Box plots of White-throated Magpie-Jay brood sex ratio by (A) group size during each nest attempt, and (B) number of helpers per group. Data are from the eight groups for which breeder identities, group size, and number of helpers were known. Dark lines represent median values, boxes represent the middle 50% of the distribution, and whisker bars indicate the highest and lowest values. The number of clutches sampled for each group size or helper number category is listed above median bars It is possible that group size and helper number were not accurate correlates of territory quality. To address this, I built additional models to establish whether sex ratios differed broadly across social groups or breeding females. These GLMs showed no effect of social group or breeding female identity on brood sex ratios. Also, the number of offspring sampled per clutch ranged widely, from one to six. Since very low sample sizes may lead to artificially skewed sex ratios (e.g., a sample size of one will always result in a sex ratio of either zero or one), I performed additional GLMs where I excluded all clutches for which fewer than three offspring were sampled. Even when analyses were restricted to these larger clutch sizes, there was no evidence that brood sex ratios varied predictably as a function of time, helper number, group size, social group, or female identity. Although not consistent with the hypotheses examined here, sex ratios varied widely across the 38 clutches (Fig. 1, 2). Some groups tended to have female-dominated clutches (e.g., Casona, Oficina, Rosa Maria), while others had male- dominated clutches (e.g., Borrachos, Campground). It is possible that nest sequence within breeding seasons influenced offspring sex ratios. I analyzed multiple nests within a breeding season for five of the 13 females. For three of these females, sex ratios became more female-biased as the season progressed. In other cases, the ratio stayed the same (n = 1) or became more male biased (n = 1). I also assessed how brood sex ratios varied among females across the entire study period (Fig. 3). Sex ratios deviated widely from 1:1, but not in any consistent direction. Figure 3. Open in new tabDownload slide Offspring sex ratios across multiple clutches of seven breeding female White-throated Magpie-Jays. For each female, clutches are numbered in the order in which they were sampled over the 3- year study period. Not all clutches of a given female were sampled. Data shown only for females for which more than one clutch was sampled, and for clutches for which at least three offspring were sampled. Each female is represented by a different line pattern Figure 3. Open in new tabDownload slide Offspring sex ratios across multiple clutches of seven breeding female White-throated Magpie-Jays. For each female, clutches are numbered in the order in which they were sampled over the 3- year study period. Not all clutches of a given female were sampled. Data shown only for females for which more than one clutch was sampled, and for clutches for which at least three offspring were sampled. Each female is represented by a different line pattern Discussion I found no statistical evidence that offspring sex ratios varied consistently as a function of nest initiation date, group size, or number of helpers at the nest. There was considerable sex-ratio variation across clutches, but the hypotheses examined here could not account for this variation. There are several explanations for the observed results. First, it is possible that for magpie-jays, selectively producing offspring of one sex is simply too costly. Indeed, a low-cost physiological mechanism for manipulating offspring sex ratio has yet to be identified in birds (Emlen 1997, Hardy 1997, Sheldon 1998, Krackow 1999). In their study of sex-ratio biasing in raptors, Pen and colleagues (1999) argue that in most cases, even small costs to the mother would outweigh any adaptive benefits. A second possibility is that magpie-jays do indeed control the sex ratio of their offspring, but that biases are so small or variable that statistical analyses could not detect the deviations. The sex ratio of all offspring combined was as close to 1:1 as possible given an odd number of samples. With my sample size of 135, I had the statistical power to detect an effect size larger than 0.25 (Cohen 1988), which is considerably smaller than the effect size of the Seychelles Warbler (>0.50, Komdeur et al. 1997). Finally, it is possible that group size and helper number are not appropriate correlates of territory quality in this species. Within a group, the number of acacia trees per magpie-jay has been shown to be approximately equal across territories (Langen and Vehrencamp 1998). However, though group size may be a good predictor of acacia number, it is not necessarily an accurate indicator of the territory quality differences that affect reproductive success. A more accurate assessment of territory quality would require quantifying territory size and density of key resources and relating those variables to the number of birds within a group. Under what conditions might selection act on females to bias brood sex ratios? According to a genetic model developed by Reiss (1987), due to conflicts of interest between the mother and the sex chromosomes of gametes, the expected fitness of one sex would have to be three times that of the other sex for biasing to be adaptive. Sex chromosomes of gametes from the heterogametic sex (females in birds) should have no genetic interest in sex-ratio distortion, and the gametic autosomes should favor deviations from 1:1 only if fitness differences between the sexes are very large. Such extreme differences in fitness are arguably rare in most species. The Seychelles Warbler is an exception: inclusive fitness benefits for females raising daughters on high quality territories were 9.8 times higher than for females raising sons (Komdeur et al. 2002). Although we cannot directly compare the benefits of raising daughters versus sons in the magpie- jay, it is likely that the inclusive fitness differences are small. According to one study of the White-throated Magpie-Jay, a helper increases a breeder's inclusive fitness, as measured by fledgling production, an equivalent of about one offspring per year (Langen and Vehrencamp 1999). There are several possible reasons why the fitness benefits of sex-ratio biasing might differ between the two species. Seychelles Warblers forage primarily on insects that they glean from vegetation. Insect abundance varies widely among territories and accurately indicates territory quality (Komdeur 1996). In an environment such as this where territory quality is highly heterogeneous, sex-ratio differences are magnified. In contrast, White-throated Magpie-Jays are omnivores, foraging on a diverse array of fruits, insects, and small vertebrates (Langen 1994). Given their highly varied diet, differences in resource availability among magpie-jay territories might be expected to be small, and the advantages of producing highly skewed offspring sex ratios less pronounced. However, results of an ecological study conducted by Langen and Vehrencamp (1998) suggest otherwise. Although magpie-jays are indeed generalists, resource availability varies widely across territories. During the dry season, the jays are highly dependent on the fruits of acacia trees, and groups on territories with a higher density of acacia trees fledged more offspring per successful nest (Langen and Vehrencamp 1998). Group stability might also play a role. Among Seychelles Warblers, group membership is fairly stable across time, breeder turnover is low, and territorial boundaries are maintained over many years. In contrast, within the population of magpie-jays at Santa Rosa, the last two decades have brought increasing rates of breeder turnover, frequent changes in group membership, and a breakdown in territorial boundaries. These changes are likely due to rapidly changing forest structure and concomitant increases in predation in this area (ECB, unpubl. data). Due to widespread social instability within this particular population of magpie-jays, the fitness benefits of producing daughters over sons might not be consistent across breeding attempts or seasons. Despite publication biases against negative results (for reviews see Festa-Bianchet 1996, Palmer 2000), studies that find no evidence for sex-ratio biasing are emerging (Koenig and Dickinson 1996, South and Wright 2002, Westneat et al. 2002, Wheelwright and Seabury 2003). While sex ratios varied considerably across magpie-jay clutches, this variation was not consistent with the predictions of local resource enhancement or competition. Although the social system of this species is similar to the Seychelles Warbler, patterns of sex-ratio biasing are very different. This discrepancy suggests that the strong biases found in the Seychelles Warbler are not due specifically to its female- biased helping system. It also suggests that selection acting on females must be sufficiently strong for sex control mechanisms to evolve, and that different selection pressures may be acting simultaneously. Acknowledgments I am very grateful to the staff of the Area de Conservación Guanacaste, Costa Rica, for permission to work at Santa Rosa and for years of advice and support. In particular, thanks to R. Blanco and M. Chavarria for administrative help and unfailing enthusiasm for my research. For assistance in the field, thanks to P. Ingram, L. Larsen, T. Lim, C. Schwendener, R. VanBuskirk, A. Perez, H. Guadamuz, and eight volunteers from the UC University Research Expeditions Program. Many thanks to my advisor, J. Eadie, for discussing ideas and providing access to his molecular laboratory. A. Fowler provided helpful advice in the lab. M. Berg translated the abstract into Spanish. Drafts of this manuscript were greatly improved with comments from J. Eadie, T. Langen, P. Sherman, A. Harcourt, A. Bell, H. Berg, and two anonymous reviewers. Special thanks to R. VanBuskirk for his help with statistical analysis and writing style. Financial support for this research was provided by an NSF Dissertation Improvement Grant (no. 0105139), University of California at Davis (UCD) chapter of Phi Beta Kappa, UCD Center for Population Biology, UCD Animal Behavior Graduate Group, UCD Department of Biological Sciences, UCD Sherley Ashton Scholarship, UCD Jastro-Shields Graduate Research Awards, UCD & Humanities Research Awards, Frank M. Chapman Memorial Fund Research Awards, Wilson Ornithological Society Louis Agassiz Fuertes Award, Animal Behavior Society Student Research Grant, and American Ornithologists' Union Blake Award. All field procedures were approved by UC Davis Animal Use and Care Protocol #8934. Literature Cited Brown , J. L. 1987 . Helping and communal breeding in birds. Princeton University Press, Princeton, NJ . WorldCat Clark , A. B. 1978 . Sex ratio control and local resource competition in a prosimian primate. Science 201 : 163 – 165 . Google Scholar Crossref Search ADS PubMed WorldCat Clutton-Brock , T. H. 1986 . Sex ratio variation in birds. Ibis 128 : 317 – 329 . Google Scholar Crossref Search ADS WorldCat Cockburn , A. , S. Legge , and M. C. Double . 2002 . Sex ratios in birds and mammals: can the hypotheses be disentangled?, p. 266–286. In I. Hardy [ed.], Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, UK . WorldCat Cohen , J. 1988 . Statistical power analysis for the behavioral sciences. Lawrence Erlbaum Associates, Hillsdale, NJ . WorldCat Cook , R. D. , and S. Weisberg . [online&rsqb . 2002 . Arc software. Version 1.04. <http://www.stat.umn.edu/arc/software.html> (26 January 2004) . WorldCat Crawley , M. J. 1993 . GLIM for ecologists. Blackwell Scientific Publishing, Oxford, UK . WorldCat Emlen , S. T. 1997 . When mothers prefer daughters over sons. Trends in Ecology & Evolution 12 : 291 – 292 . Google Scholar Crossref Search ADS PubMed WorldCat Emlen , S. T. , J. M. Emlen , and S. A. Levin . 1986 . Sex-ratio selection in species with helpers-at-the- nest. American Naturalist 127 : 1 – 8 . Google Scholar Crossref Search ADS WorldCat Festa-Bianchet , M. 1996 . Offspring sex ratio studies of mammals: does publication depend upon the quality of the research or the direction of the results?. Ecoscience 3 : 42 – 44 . Google Scholar Crossref Search ADS WorldCat Gowaty , P. A. , and M. R. Lennartz . 1985 . Sex ratios of nestling and fledgling Red-cockaded Woodpeckers (Picoides borealis) favor males. American Naturalist 126 : 347 – 353 . Google Scholar Crossref Search ADS WorldCat Greenwood , P. J. 1980 . Mating systems, philopatry, and dispersal in birds and mammals. Animal Behaviour 28 : 1140 – 1162 . Google Scholar Crossref Search ADS WorldCat Griffiths , R. , M. C. Double , K. Orr , and R. J G. Dawson . 1998 . A DNA test to sex most birds. Molecular Ecology 7 : 1071 – 1075 . Google Scholar Crossref Search ADS PubMed WorldCat Hagen , M. [online&rsqb . 2001 . Artificial incubation applied to small numbers of altricial bird eggs. <http://shell.pubnix.net/∼mhagen/docu/tabcon2.html> (26 January 2004) . WorldCat Hamilton , W. D. 1967 . Extraordinary sex ratios. Science 156 : 477 – 488 . Google Scholar Crossref Search ADS PubMed WorldCat Hardy , I. [ed&rsqb . 2002 . Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, UK . WorldCat Hardy , I. C W. 1997 . Possible factors influencing vertebrate sex ratios: an introductory overview. Applied Animal Behaviour Science 51 : 217 – 241 . Google Scholar Crossref Search ADS WorldCat Hasselquist , D. , and B. Kempenaers . 2002 . Parental care and adaptive brood sex ratio manipulation in birds. Philosophical Transactions of the Royal Society of London Series B 357 : 363 – 372 . Google Scholar Crossref Search ADS PubMed WorldCat Innes , K. E. 1992 . The behavioral ecology and sociobiology of the White-throated Magpie-Jay (Calocitta formosa) of northwestern Costa Rica. Ph.D. dissertation, Cornell University, Ithaca, NY . WorldCat Koenig , W. D. , and J. L. Dickinson . 1996 . Nestling sex-ratio variation in Western Bluebirds. Auk 113 : 902 – 910 . Google Scholar Crossref Search ADS WorldCat Koenig , W. D. , and J. R. Walters . 1999 . Sex-ratio selection in species with helpers at the nest: the repayment model revisited. American Naturalist 153 : 124 – 130 . Google Scholar Crossref Search ADS PubMed WorldCat Komdeur , J. 1996 . Facultative sex ratio bias in the offspring of Seychelles Warblers. Proceedings of the Royal Society of London Series B 263 : 661 – 666 . Google Scholar Crossref Search ADS WorldCat Komdeur , J. , S. Daan , J. Tinbergen , and C. Mateman . 1997 . Extreme adaptive modification in sex ratio of the Seychelles Warbler's eggs. Nature 385 : 522 – 525 . Google Scholar Crossref Search ADS WorldCat Komdeur , J. M. , J. L. Magrath , and S. Krackow . 2002 . Pre-ovulation control of hatchling sex ratio in the Seychelles Warbler. Proceedings of the Royal Society of London Series B 269 : 1067 – 1072 . Google Scholar Crossref Search ADS PubMed WorldCat Komdeur , J. , and I. Pen . 2002 . Adaptive sex allocation in birds: the complexities of linking theory and practice. Philosophical Transactions of the Royal Society of London Series B 357 : 373 – 380 . Google Scholar Crossref Search ADS PubMed WorldCat Krackow , S. 1999 . Avian sex ratio distortions: the myth of maternal control. Proceedings of the International Ornithological Congress 22 : 425 – 433 . WorldCat Langen , T. A. 1994 . Ecology, learning, and dispersal in the White-throated Magpie-Jay (Calocitta formosa). Ph.D. dissertation, University of California, San Diego, CA . WorldCat Langen , T. A. 1996 . The mating system of the White- throated Magpie-Jay Calocitta formosa and Greenwood's hypothesis for sex-biased dispersal. Ibis 138 : 506 – 513 . Google Scholar Crossref Search ADS WorldCat Langen , T. A. , and S. L. Vehrencamp . 1998 . Ecological factors affecting group and territory size in White-throated Magpie-Jays. Auk 115 : 327 – 339 . Google Scholar Crossref Search ADS WorldCat Langen , T. A. , and S. L. Vehrencamp . 1999 . How White-throated Magpie-Jay helpers contribute during breeding. Auk 116 : 131 – 141 . Google Scholar Crossref Search ADS WorldCat Lessells , C. M. , and M. I. Avery . 1987 . Sex-ratio selection in species with helpers at the nest: some extensions of the repayment model. American Naturalist 129 : 610 – 620 . Google Scholar Crossref Search ADS WorldCat Ligon , J. D. , and S. H. Ligon . 1990 . Female-biased sex ratio at hatching in the Green Woodhoopoe. Auk 107 : 765 – 771 . Google Scholar Crossref Search ADS WorldCat Palmer , A. R. 2000 . Quasireplication and the contract of error: lessons from sex ratios, heritabilities and fluctuating asymmetry. Annual Review of Ecology and Systematics 31 : 441 – 480 . Google Scholar Crossref Search ADS WorldCat Pen , I. , and F. J. Weissing . 2000 . Sex-ratio optimization with helpers at the nest. Proceedings of the Royal Society of London Series B 267 : 539 – 543 . Google Scholar Crossref Search ADS PubMed WorldCat Pen , I. , F. J. Weissing , and S. Daan . 1999 . Seasonal sex ratio trend in the European Kestrel: an evolutionarily stable strategy analysis. American Naturalist 153 : 384 – 397 . Google Scholar Crossref Search ADS PubMed WorldCat Reiss , M. J. 1987 . Evolutionary conflict over the control of offspring sex ratio. Journal of Theoretical Biology 125 : 25 – 40 . Google Scholar Crossref Search ADS PubMed WorldCat Sheldon , B. C. 1998 . Recent studies of avian sex ratios. Heredity 80 : 397 – 402 . Google Scholar Crossref Search ADS WorldCat South , J. M. , and T. F. Wright . 2002 . Nestling sex ratios in the Yellow-naped Amazon: no evidence for adaptive modification. Condor 104 : 437 – 440 . Google Scholar Crossref Search ADS WorldCat SPSS. 2001 . SPSS graduate pack. Version 11.0. SPSS Inc., Chicago . WorldCat Stacey , P. B. , and W. D. Koenig . [eds.&rsqb . 1990 . Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, Cambridge, UK . WorldCat Westneat , D. F. , I. R K. Stewart , E. H. Woeste , J. Gipson , L. Abdulkadir , and J. P. Poston . 2002 . Patterns of sex ratio variation in House Sparrows. Condor 104 : 598 – 609 . Google Scholar Crossref Search ADS WorldCat Wheelwright , N. T. , and R. E. Seabury . 2003 . Fifty: fifty offspring sex ratios in Savannah Sparrows (Passerculus sandwichensis). Auk 120 : 171 – 179 . Google Scholar Crossref Search ADS WorldCat Wilson , K. , and I. Hardy . 2002 . Statistical analysis of sex ratios: an introduction. p. 48–92. In I. Hardy [ed.], Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, UK . WorldCat Author notes ecberg@ucdavis.edu © The Cooper Ornithological Society 2004
TI - A Test of Sex-Ratio Biasing in the White-Throated Magpie-Jay, A Cooperative Breeder with Female Helpers
JF - Condor: Ornithological Applications
DO - 10.1093/condor/106.2.299
DA - 2004-05-01
UR - https://www.deepdyve.com/lp/oxford-university-press/a-test-of-sex-ratio-biasing-in-the-white-throated-magpie-jay-a-ffwz4qXl6K
SP - 299
VL - 106
IS - 2
DP - DeepDyve
ER -