Behavioral Ecology Advance Access originally published online on August 25, 2004
Behavioral Ecology 2005 16(1):274-279; doi:10.1093/beheco/arh153
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Maternal condition and offspring sex ratio in polygynous ungulates: a case study of bighorn sheep
a Département de biologie, Université de Sherbrooke, Sherbrooke, Québec J1K 2R1, Canada, b Unité Mixte de Recherche 5558, Biométrie et Biologie Evolutive, Université Lyon 1, 69622 Villeurbanne cedex, France, and c Alberta Department of Sustainable Development, Fish and Wildlife Division, Suite 201, 800 Railway Avenue, Canmore, Alberta T1W 1P1, Canada
Address correspondence to M. Festa-Bianchet. E-mail: marco.festa-bianchet{at}usherbrooke.ca.
Received 7 January 2003; revised 10 June 2004; accepted 9 July 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The Trivers and Willard model (TWM) predicts that for sexually dimorphic polygynous mammals, mothers able to provide a high level of care should bias offspring sex ratio in favor of sons. Contradictory results of empirical studies, however, suggest that selective pressures for adaptive offspring sex ratio vary with species and environmental conditions. We report the results of a 29-year study of marked bighorn sheep (Ovis canadensis) in a population that underwent wide changes in density and where most females were weighed each year. Lamb sex ratio was independent of absolute ewe mass and yearly deviations from individual or population average mass, but there was a nonsignificant trend towards fewer males being born at high population density. Bighorn sheep satisfy all the assumptions of the TWM but not its prediction: lamb sex ratio is independent of maternal ability to provide care. Recent hypotheses to explain the lack of relationship between maternal condition and offspring sex in ungulates are unlikely to apply to bighorn sheep. We suggest that the TWM may only apply when social rank strongly affects the ability to provide maternal care. Those circumstances are likely to occur for only a few species and within a narrow range of environmental conditions.
Key words: bighorn sheep, habitat quality, sex ratio, social rank, Trivers and Willard model, ungulates.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Trivers and Willard (1973)
proposed a model of adaptive offspring sex ratio variation when parental fitness returns differ according to offspring sex. Their model makes three assumptions: (1) that offspring phenotypic quality at weaning is correlated with maternal phenotypic quality, (2) that offspring quality at weaning is correlated with quality when adult, and (3) that adult quality affects the reproductive success of one sex more than that of the other. For polygynous and sexually dimorphic mammals, such as most ungulates (Alexander et al., 1979), the model predicts that high quality mothers should produce more sons, while low quality mothers should produce more daughters. Empirical results, however, are inconsistent, both across (Hewison and Gaillard, 1999; Pélabon et al., 1995) and within (Hewison et al., 1999) species, possibly because the model was often tested in species that do not meet its assumptions (Hewison et al., 1999) or because adaptive sex ratio variation is also affected by many environmental factors that were ignored in the formulation of the original hypothesis (Kruuk et al., 1999).
The "advantaged daughter hypothesis," based on a theoretical basis similar to the Trivers and Willard model (TWM), leads to the opposite prediction for the sex ratio produced by ungulate mothers (Hewison and Gaillard, 1999; Hiraiwa-Hasegawa, 1993; Simpson and Simpson, 1982). According to this hypothesis, mothers able to provide a high level of care should invest more in daughters than in sons if maternal care can affect the fitness of daughters more strongly than the fitness of sons, for example through inheritance of social rank (see also Leimar [1996] for an extension of this hypothesis). Another hypothesis, based on local resource competition (LRC), was first proposed at the population scale (Clark, 1978). At the individual level (Silk, 1983), it predicts that female mammals in poor condition would benefit from producing males, because males are more likely to disperse than females and therefore adult sons are less likely than adult daughters to compete with their mother for local resources. Some studies of ungulates have provided support for the LRC hypothesis (Caley and Nudds, 1987).
Because a similar theoretical basis predicts sex ratio biases in opposite directions with subtle changes in the assumptions, any significant deviation from parity can be interpreted a posteriori as support for one of these theories. Significant results are easier to publish, and the rarity of replication leads to an important publication bias in many areas of ecology (Csada et al., 1996; Palmer, 2000). A publication bias is particularly likely in sex ratio studies, because both the mechanisms and the potential adaptive significance of this phenomenon are largely unknown (Clutton-Brock, 1985; Festa-Bianchet, 1996; Krackow, 1995). Before concluding that adaptive variation in sex ratio is widespread in mammals, one should consider the reliability of each study, including its sample size (Palmer, 2000), its duration, and most of all to what extent the study species meets the assumptions of the model being tested (Hewison et al., 1999).
Trivers and Willard (1973) chose the caribou (Rangifer tarandus) to illustrate their influential paper, and ungulates appear to be ideal candidates to test their model (Hewison and Gaillard, 1999; Sheldon and West, 2004). Only four species of ungulates, however, are known to meet the three assumptions of the TWM (Hewison and Gaillard, 1999): bighorn sheep, red deer (Cervus elaphus), reindeer/caribou, and fallow deer (Dama dama). Despite weak adult sexual dimorphism, feral horses (Equus caballus) may also be a good model to test the TWM (Cameron et al., 1999; Cameron and Linklater, 2000), although it is not clear whether or not mare condition has a different effect on foal reproductive success according to offspring sex. Recently, it has been suggested that feral domestic sheep (Ovis aries) also satisfy the TWM assumptions, although there is no relationship between maternal mass and offspring sex ratio (Lindström et al., 2002).
In bighorn sheep, sons receive more maternal care (Festa-Bianchet et al., 1996; Hogg et al., 1992) and have higher fitness costs than daughters; compared to ewes that wean daughters, ewes that wean sons have higher macroparasite counts (Festa-Bianchet, 1989), later subsequent oestrus (Hogg et al., 1992), and lower subsequent weaning success (Bérubé et al., 1996). Mass at weaning is more strongly correlated with adult mass for males than for females (Festa-Bianchet et al., 2000). Male reproductive success appears more strongly affected than female reproductive success by phenotypic characteristics such as horn and body size (Coltman et al., 2002). Finally, in most bighorn sheep populations, including the Ram Mountain population in the current study, litter size is fixed at one, which avoids additional complications in interpreting the TWM predictions (Williams, 1979). Although this species seems an ideal candidate, the TWM's prediction of a relationship between maternal condition and lamb sex ratio remains untested.
In red deer, dominant hinds produce a male-biased offspring sex ratio, but only at low population density (Kruuk et al., 1999). Dominant hinds are likely high quality mothers because they have higher reproductive success than subordinates (Clutton-Brock et al., 1986). Dominance as calculated in the red deer study, however, is cohort-specific and fixed for a hind's lifetime; therefore, it cannot reflect yearly changes in an individual's ability to provide maternal care.
The TWM specifically predicts that a mother should bias offspring sex ratio according to her condition at conception, but very few studies have compared yearly changes in individual maternal condition to offspring sex ratio in ungulates (Cameron et al., 1999). In our study, yearly recaptures of ewes (Festa-Bianchet et al., 1996) allowed us to measure annual condition based on year-to-year changes in individual mass, a variable strongly correlated with individual quality and reproductive potential in this species (Bérubé et al., 1999; Festa-Bianchet, 1998; Gaillard et al., 2000). To test whether individual characteristics and environmental factors affect sex ratio variation, one requires data on many individuals monitored under contrasting environmental conditions (Kruuk et al., 1999). Our 29-year study of marked, known-age and known-mass bighorn sheep is in a unique position for such a test. Population density more than tripled during our study, providing clear evidence of resource limitation at high density (Bérubé et al., 1996; Festa-Bianchet et al., 1998; Jorgenson et al., 1993; Portier et al., 1998). Kruuk et al. (1999) reported a strong effect of density on sex ratio patterns at both the population and individual levels, with poor habitat quality leading to fewer male fetuses being carried to term.
We thus tested (1) whether or not changes in population density affected offspring sex ratio at the population level in bighorn sheep and (2) whether the sex of lambs produced by individual ewes changed according to their body condition. Our null hypotheses were that population density and ewe body condition did not affect lamb sex.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and population
Data were collected from 1972 to 2000 at Ram Mountain, Alberta, Canada (52° N, 115° W). The bighorn sheep range extends over approximately 38 km2 of alpine and subalpine habitat at 1082 m to 2173 m asl. Each year, sheep are captured from late May to September in a corral trap baited with salt. Each ewe's individual rate of mass gain was used to adjust her mass to 15 September, about two months before conception. Between 1972 and 2000, 235 adult females were weighed, including 151 aged between 6 and 10 years. Ewes included in our analyses were weighed at least twice during the summer, but most were weighed 3–4 times. Festa-Bianchet et al. (1996)
report more details on capture frequencies and mass adjustments. Maternal condition about 2 months before conception is a reliable measure of condition at conception because most ewes complete summer mass accumulation by mid-August (Festa-Bianchet et al., 1996), partly because by then the quality of available forage has declined (Festa-Bianchet, 1988b). By mid-September, lambs have almost stopped suckling (Festa-Bianchet, 1988a). A recent meta-analysis claimed that the relationship between maternal condition and offspring sex tends to be stronger when maternal quality is assessed before conception than after it (Sheldon and West, 2004).
Ewes were marked with visual collars and lambs with ear tags. Lamb sex was determined at first capture, for lambs aged from 1 week to 3 months. All ewes have been marked since 1976. Over 80% of the lambs were caught in most years, and 686 lambs were weighed between 1972 and 2000. We assumed that sex ratio at capture reflected sex ratio at birth; neonatal mortality (deduced for ewes that lactated but were not seen with a lamb) averaged about 19%, and we have no evidence that it was sex-biased (Bérubé et al., 1996). Lamb and yearling survival is not sex-biased (Jorgenson et al., 1997; Portier et al., 1998). We used the number of adult ewes in June to measure population density, because adult rams use different foraging ranges than those used by adult ewes and juveniles (Geist and Petocz, 1977). The number of adult females has been used to measure population density by other studies of sexually dimorphic polygynous ungulates (Côté and Festa-Bianchet, 2001; Kruuk et al., 1999).
Indices of maternal condition
Earlier research revealed that ewe age affected body mass, fertility, and, for very old ewes, lamb sex ratio (Bérubé et al., 1996; Festa-Bianchet et al., 1996; Gallant et al., 2001). Here we focus on mass and body condition of ewes aged 6–10 years, whose mass is mostly unaffected by age (Festa-Bianchet et al., 1996). Including ewes aged 4 to 14 years (therefore excluding the oldest and youngest reproducing ewes) led to similar results to those presented here. Trivers and Willard made no predictions about how maternal age may affect offspring sex ratio (Hewison et al., 2002), and the use of maternal age as a proxy for condition is problematic (Sheldon and West, 2004).
We used three different measures of ewe quality :
- First, we measured proportion by which each ewe each year deviated from her average mid-September mass at 6–10 years. Changes in absolute body mass from year to year for adult ewes are correlated with differences in reproductive potential (Festa-Bianchet, 1998). Therefore, this first measure tested whether ewes produced more sons in years they were in better condition compared to their individual long-term average (n = 165 ewes-year and 78 different ewes, with an average of 3.7 [range 2–5] measurements of mid-September mass per ewe). This comparison provides a direct test of the TWM.
- The second measure of ewe quality was the difference between each ewe's mass and the average mid-September mass of adult females that year, which provided a measure of a ewe's quality relative to other females each year (n = 172 ewes-year and 83 different ewes). Because measures (1) and (2) were correlated (F = 25,88, df = 165, r2 = .14, p < .001), they could not be included in the same analysis.
- Finally, we compared the average mid-September mass of each ewe at 6–10 years of age with her offspring sex ratio during those years (n = 95 ewes). We performed a separate analysis for this global measure, in which each ewe was considered only once.
To test whether lamb sex ratio varied according to reproductive effort the previous year, we used three levels of increasing energetic cost for the mother (Bérubé et al., 1996): no lamb weaned, weaned a female, and weaned a male. The category ‘no lamb weaned’ included 15 ewe-years of no apparent gestation, 55 of neonatal lamb mortality, and 19 lambs that died during summer, mostly before one month of age. Thus, our sample was insufficient to divide this category into further sub-classes of reproductive effort.
Statistical analyses
Individual ewes were included one to five times in the analysis of the effects of yearly body mass variation and of relative quality on the probability of producing a son. We therefore fitted individual ewe identity as a random effect in a generalized linear model (Schall, 1991). We compared the deviance of the general model (including a measure of condition, previous reproduction, individual, and the interaction between the measure of condition and previous reproduction) with the deviance of the additive model: the difference between models is distributed as a 
2 with degrees of freedom equal to the difference in degrees of freedom between the two models compared. Because the interaction was not significant, we then tested the main factors by successively withdrawing each of the two terms.
The effect of average maternal mass between 6 and 10 years old on lamb sex ratio was analyzed with a logistic regression of the proportion of sons produced by each ewe at 6–10 years of age. A similar analysis was performed to study the relationship between cohort sex ratio and population density. All statistical analyses used R software (R Development Core Team, 2003).
We paid special attention to nonsignificant results by considering the effect size in addition to p-values. We did not run a posteriori power analyses because such retrospective analyses are meaningless (Hoenig and Heisey, 2001). Instead, we used the information provided by confidence intervals as recommended by several authors (Di Stefano, 2004; Johnson, 1999; Steidl et al., 1997).
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RESULTS |
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Individual ewes were not significantly more likely to conceive sons in years when they were heavy (mean proportion of males 0.48, 95% CI: 0.37–0.59) than in years when they were lighter than their average adult mass (0.45, 95% CI: 0.34–0.56; Table 1, Model a). Both confidence intervals included 0.50. The effect size (0.03) was positive as predicted by the TWM but was very small and confidence intervals overlapped by 76%. We therefore concluded that sex ratio was independent of ewe body condition. Reproductive status the previous year did not significantly influence lamb sex (means of 0.49, 95% CI: 0.37–0.61; 0.44, 95% CI: 0.31–0.57; and 0.46, 95% CI: 0.32–0.60; for females that weaned no lamb, daughters, and sons, respectively; Table 1, Model a). All confidence intervals included 0.50 and overlapped by 67% or more. The effect was opposite of that predicted by the TWM because sex ratio for females having weaned a son was higher than for females having weaned a daughter. We thus concluded that there was no relationship between previous reproductive status and sex ratio.
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There was a slight trend for ewes to produce more sons between 6 and 10 years of age if their average mass was heavier than the population average (71.5 kg; 0.50, 95% CI: 0.41–0.60, compared to 0.42, 95% CI: 0.31–0.54 for females lighter than the population average; Table 1, Model b, and Figure 1). The confidence intervals, however, overlapped by 45% and both included 0.50. Moreover, when we divided the females into three groups according to body mass (first group: less than 69.83 kg; second group: between 69.83 and 73.90 kg; third group: more than 73.90 kg), the heaviest females tended to produce fewer sons than females of intermediate mass (0.425, 95% CI: 0.31–0.54 vs. 0.576, 95% CI: 0.46–0.69), contrary to the TWM prediction. We thus concluded that female body mass did not influence offspring sex ratio in bighorn sheep.
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Females heavier than the population average in the year of conception did not produce significantly more male offspring (0.47, 95% CI: 0.39–0.55) than females lighter than other females (0.43, 95% CI: 0.24–0.62; Table 1, Model c). Both confidence intervals included 0.50 and overlapped by 100%. We thus concluded that a female's quality relative to the population average did not influence offspring sex ratio in bighorn sheep.
Population density may have influenced cohort sex ratio, as our results were somewhat inconclusive. Lamb sex ratio tended to decrease with increasing density (slope of –0.0056, 95% CI: –0.0119–0.0008, 2 = 2.99, df = 1, p = .08); at high density (>72 ewes), the offspring sex ratio was 0.45 (95% CI: 0.38–0.52) whereas at low density (<72 ewes) it was 0.54 (95% CI: 0.49–0.59), leading to an effect size of 0.09. Although the difference was not significant, the confidence intervals overlapped by only 16%. The overall mean proportion of sons was 0.47 ± 0.039 (SE).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Our results suggest that maternal condition has no detectable influence on offspring sex in bighorn sheep, despite the fact that this species is an ideal candidate to test the predictions of the TWM because it satisfies its assumptions, and despite the quality of our long-term data. We monitored the sex ratio of lambs of individual ewes of known age, body mass, and condition in a population that underwent substantial changes in density. Offspring sex ratio is independent of individual maternal condition in this population, because ewes were not more likely to conceive sons in years when they were heavier than their average multi-year adult mass. However, lamb sex ratio may have varied with population density, possibly because at high population density fewer male fetuses were carried to term, as has been suggested for red deer (Kruuk et al., 1999
), or because more male lambs died neonatally.
The TWM's prediction is not consistently met in ungulate species that satisfy its assumptions (Hewison and Gaillard, 1999). In fallow deer, maternal body mass or maternal body mass changes are not related to offspring sex (Birgersson, 1998). In red deer and reindeer, the relationship between offspring sex ratio and maternal quality is affected by population characteristics (Kojola and Eloranta, 1989; Kruuk et al., 1999; Reimers and Lenvik, 1997). Maternal condition has been reported to affect sex ratio and sex-biased maternal investment in horses, where results also vary among study populations (Cameron et al., 1999; Cameron and Linklater, 2000; Monard et al., 1997). Several factors may explain these inconsistent results both across and within species that meet the TWM assumptions.
Within species, some authors reported an effect of environmental conditions on sex ratio patterns, in ungulates and in other groups (Kruuk et al., 1999; Van Shaik and Hrdy, 1991). In primates it has been suggested that when local environmental conditions lead to intense female-female competition for resources, the selective pressures for adaptive sex ratio variation may be different from those existing when resources are more readily available (Dittus, 1998; Johnson, 1988; Packer et al., 2000; Van Shaik and Hrdy, 1991). In red deer, Kruuk et al. (1999) showed that the association between a female's social rank and her probability to produce a son disappeared at high density, probably because the higher growth rates of sons resulted in differential fetal loss. They pointed out that all support for the TWM prediction among ungulates had been found in populations below carrying capacity. The Ram Mountain bighorn sheep population more than tripled during our study, showing clear density-dependence in age at primiparity (Jorgenson et al., 1993), mortality of yearling ewes (Jorgenson et al., 1997), horn growth of males (Jorgenson et al., 1998) and lamb winter survival (Portier et al., 1998). Summer food quality was negatively affected by population density (Blanchard et al., 2003). Together, these results suggest that this population was well below carrying capacity during the low-density years of the study.
In feral domestic sheep, Lindström et al. (2002) reported no correlation between offspring sex ratio and maternal mass but showed a weak positive correlation with population density. The authors proposed that the time scale of variation in density and weather conditions might be too short in this highly fluctuating environment to allow mechanisms of sex ratio adjustment to evolve. Both the Ram Mountain bighorn sheep and the Hirta Soay sheep populations underwent wide changes in density, but while density for Soay sheep varied substantially from one year to another, population changes at Ram Mountain developed over decades. Therefore, the explanation for the lack of adaptive sex ratio manipulation proposed for Soay sheep is unlikely to apply to bighorn sheep.
As pointed out by Kruuk et al. (1999), variation in habitat quality is probably far from sufficient to explain the inconsistent results in sex ratio patterns across species. Differences in results may also be due to the different measures of maternal quality that were used. Whereas Kruuk and colleagues considered maternal social rank, studies on Soay and bighorn sheep were based on maternal condition. Sheldon and West (2004) pointed out that studies that employed behavioral measures of dominance supported more strongly the TWM than those based on body condition. We suggest that social organization may affect the role of female condition in producing the offspring sex ratio pattern predicted by the TWM.
Within species where the TWM assumptions are met, the selective pressure for a female to manipulate offspring sex ratio should depend not only on her own ability to provide maternal care, but also on the quality of other females in the population. A mother in good condition could increase her fitness by producing a daughter if most other females in the population were in even better condition and thus likely to produce sons of greater competitive ability. Therefore, the evolution of sex ratio manipulation could involve a physiological mechanism dependent directly on social rank, which, under some conditions, will be a reliable clue to a female's relative potential as a mother (Dittus, 1998; Sheldon and West, 2004). Maternal hormone levels may be involved in determining offspring sex ratio, because they vary according to female rank (Goodwin et al., 1999; James, 1985) and are correlated with litter sex ratio (Flint et al., 1997; James, 1996). Dominant females may have higher fitness than subordinates only if high rank provides better access to some resources (Richards, 1974). The TWM prediction may apply only to species where female social rank directly affects access to resources. Moreover, variance in female condition should be maximized in such species (Clutton-Brock et al., 1997). Across species known to meet the TWM assumptions, those that confirm its prediction (red deer, reindeer, and horses) contrast with species that do not (bighorn and Soay sheep) in their social organization.
In female reindeer and red deer, social rank determines the outcome of interference competition for food (Barrette and Vandal, 1986; Kojola, 1997; Thouless, 1990) and is positively correlated with maternal and offspring mass (Clutton-Brock et al., 1986; Kojola, 1997). Dominant female reindeer lose less mass overwinter than subordinates (Kojola, 1997), and in red deer growth rate declines with increasing population density only for subordinate hinds (Blanc and Theriez, 1998; see also Clutton-Brock et al., 1984). In horses, female rank is also correlated with diet quality and reproductive success (Duncan, 1992). In contrast, dominance does not affect access to food in bighorn ewes (Eccles and Shackleton, 1986; Festa-Bianchet, 1991), a species of low aggressiveness compared to other ungulates (Fournier and Festa-Bianchet, 1995), and female rank is not correlated with mass, activity costs, diet quality (Eccles and Shackleton, 1986), conception date, lamb birth mass or birth date (Hass, 1991), or reproductive success (Festa-Bianchet, 1991). Although we did not measure dominance in ewes at Ram Mountain, we have no reason to believe that it played a stronger role than elsewhere. Soay sheep have a similar social organization to bighorn sheep (Clutton-Brock et al., 1997) and there is no evidence that social rank determines access to resources in that species.
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ACKNOWLEDGEMENTS |
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We thank D. Allainé, D. W. Coltman, S. D. Côté, T. Coulson, J.-Y. Georges, A. J. M. Hewison, A. Loison, A. Mysterud, D. Pontier, E. J. Solberg, N. G. Yoccoz, and two anonymous referees for critical comments and discussion of earlier drafts of the manuscript. The Ram Mountain bighorn sheep research is supported by the Natural Sciences and Engineering Research Council of Canada, Alberta Fish and Wildlife, the Université de Sherbrooke, and the Rocky Mountain Elk Foundation (Canada). P.B. was supported by a scholarship from the French government (allocation de recherche) and by the France-Québec co-supervision program.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Alexander RD, Hoogland JL, Howard RD, Noonan KN, and Sherman PW, 1979. Sexual dimorphism and breeding systems in pinnipeds, ungulates, primates and humans. In: Evolutionary biology and human social behaviour: an anthropological perspective (Chagnon N, Irons W, eds). North Scituate, MA: Duxbury Press; 402–435.
Barrette C, and Vandal D, 1986. Social rank, dominance, antler size, and access to food in snow-bound wild woodland caribou. Behaviour 97:118–146.[CrossRef][Web of Science]
Bérubé CH, Festa-Bianchet M, and Jorgenson JT, 1996. Reproductive costs of sons and daughters in Rocky Mountain bighorn sheep. Behav Ecol 7:60–68.
Bérubé CH, Festa-Bianchet M, and Jorgenson JT, 1999. Individual differences, longevity and reproductive senescence in bighorn ewes. Ecology 80:2555–2565.[CrossRef][Web of Science]
Birgersson B, 1998. Adaptive adjustment of the sex ratio: more data and considerations from a fallow deer population. Behav Ecol 9:404–408.
Blanc F, and Theriez M, 1998. Effects of stocking density on the behaviour and growth of farmed red deer. Appl Anim Behav Sci 56:297–307.[CrossRef][Web of Science]
Blanchard P, Festa-Bianchet M, Gaillard J-M, and Jorgenson JT, 2003. A test of long-term fecal nitrogen monitoring to evaluate nutritional status in bighorn sheep. J Wildlife Manage 67:477–484.[CrossRef]
Caley MJ, and Nudds TD, 1987. Sex-ratio adjustment in Odocoileus: does local resource competition play a role? Am Nat 129:452–457.[CrossRef][Web of Science]
Cameron EZ, and Linklater WL, 2000. Individual mares bias investment in sons and daughters in relation to their condition. Anim Behav 60:359–367.[CrossRef][Web of Science][Medline]
Cameron EZ, Linklater WL, Stafford KJ, and Veltman CJ, 1999. Birth sex ratios relate to mare condition at conception in Kaimanawa horses. Behav Ecol 10:472–475.
Clark AB, 1978. Sex ratio and local ressource competition in a prosimian primate. Science 201:163–165.
Clutton-Brock TH, 1985. Birth sex ratios and the reproductive success of sons and daughters. In: Evolution: essays in honour of John Maynard Smith (Greenwood PJ, Harvey PH, Slatkin M, eds.). Cambridge: Cambridge University Press; 221–236.
Clutton-Brock TH, Albon SD, and Guinness FE, 1986. Great expectations: dominance, breeding success and offspring sex ratio in red deer. Anim Behav 34:460–471.[CrossRef]
Clutton-Brock TH, Guiness FE, and Albon, SD, 1984. Individuals and populations: the effects of social behaviour on population dynamics in deer. Proc R Soc Lond B 82:275–290.
Clutton-Brock TH, Illius AW, Wilson K, Grenfell BT, MacColl ADC, and Albon SD, 1997. Stability and instability in ungulate populations: an empirical analysis. Am Nat 149:195–219.[CrossRef][Web of Science]
Coltman DW, Festa-Bianchet M, Jorgenson JT, and Strobeck C, 2002. Age-dependent sexual selection in bighorn rams. Proc R Soc Lond B 269:165–172.[Medline]
Côté S, and Festa-Bianchet M, 2001. Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 127:230–238.[CrossRef][Web of Science]
Csada RD, James PC, and Espie RHM, 1996. The "file drawer problem" of non-significant results: does it apply to biologial research? Oikos 76:591–593.[CrossRef][Web of Science]
Di Stefano J, 2004. A confidence interval approach to data analysis. Forest Ecol Manage 187:173–183.[CrossRef]
Dittus WPJ, 1998. Birth sex ratio in toque macaques and other mammals: integrating the effects of maternal condition and competition. Behav Ecol Sociobiol 44:149–160.[CrossRef][Web of Science]
Duncan P, 1992. Horses and grasses—the nutritional ecology of equids and their impact on the Camargue. New York: Springer Verlag.
Eccles TR, and Shackleton DM, 1986. Correlates and consequences of social status in females bighorn sheep. Anim Behav 34:1392–1401.[CrossRef]
Festa-Bianchet M, 1988a. Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex. Anim Behav 36:1445–1454.[CrossRef]
Festa-Bianchet M, 1988b. Seasonal range selection in bighorn sheep: conflict between forage quality, forage quantity and predator avoidance. Oecologia 75:580–586.[CrossRef][Web of Science]
Festa-Bianchet M, 1989. Individual differences, parasites and the costs of reproduction for bighorn ewes (Ovis Canadensis). J Anim Ecol 58:785–795.[CrossRef]
Festa-Bianchet M, 1991. The social system of bighorn sheep: grouping patterns, kinship and female dominance rank. Anim Behav 42:71–82.[CrossRef]
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.
Festa-Bianchet M, 1998. Condition-dependent reproductive success in bighorn ewes. Ecol Lett 1:91–94.[CrossRef][Web of Science]
Festa-Bianchet M, Gaillard J-M, and Jorgenson JT, 1998. Mass- and density-dependent reproductive success and reproductive costs in a capital breeder. Am Nat 152:367–379.[CrossRef][Web of Science][Medline]
Festa-Bianchet M, Jorgenson JT, King WJ, Smith KG, and Wishart WD, 1996. The development of sexual dimorphism—seasonal and lifetime mass changes in bighorn sheep. Can J Zool 74:330–342.[CrossRef]
Festa-Bianchet M, Jorgenson JT, and Réale D, 2000. Early development, adult mass and reproductive success in bighorn sheep. Behav Ecol 11:633–639.
Flint APF, Albon SD, and Jafar SI, 1997. Blastocyst development and conceptus sex selection in red deer Cervus elaphus: studies of a free-living population on the Isle of Rum. Gen Comp Endocrinol 106:374–383.[CrossRef][Web of Science][Medline]
Fournier F, and Festa-Bianchet M, 1995. Social dominance in adult female mountain goats. Anim Behav 49:1449–1459.[CrossRef]
Gaillard J-M, Festa-Bianchet M, Delorme D, and Jorgenson JT, 2000. Body mass and individual fitness in female ungulates: bigger is not always better. Proc R Soc Lond B 267:471–477.[Medline]
Gallant BY, Réale D, and Festa-Bianchet M, 2001. Does mass change of primiparous bighorn ewes reflect reproductive effort? Can J Zool 79:312–318.[CrossRef]
Geist V, and Petocz RG, 1977. Bighorn sheep in winter: do rams maximise reproductive fitness by spatial and habitat segregation from ewes? Can J Zool 55:1802–1810.[CrossRef]
Goodwin N, Hayssen V, Deakin DW, and Flint APF, 1999. Influences of social status on ovarian function in farmed red deer (Cervus elaphus). Physiol Behav 65:691–696.[Medline]
Hass CC, 1991. Social status in female Bighorn Sheep (Ovis canadensis): expression, development and reproductive correlates. J Zool 225:509–523.[Web of Science]
Hewison AJM, Andersen R, Gaillard J-M, Linnell JDC, and Delorme D, 1999. Contradictory findings in studies of sex ratio variation in roe deer (Capreolus capreolus). Behav Ecol Sociobiol 45:339–348.[CrossRef][Web of Science]
Hewison AJM, and Gaillard J-M, 1999. Successful sons or advantaged daughters? The Trivers-Willard model and sex-biased maternal investment in ungulates. Trends Ecol Evol 14:229–234.[CrossRef][Medline]
Hewison AJM, Gaillard J-M, Blanchard P, and Festa-Bianchet M, 2002. Maternal age is not a predominant determinant of progeny sex ratio variation in ungulates. Oikos 98:334–339.[CrossRef][Web of Science]
Hiraiwa-Hasegawa M, 1993. Skewed birth sex ratios in Primates: should high-ranking mothers have daughters or sons? Trends Ecol Evol 8:395–400.[CrossRef]
Hoenig JM, and Heisey DM, 2001. The abuse of power: the pervasive fallacy of power calculations for data analysis. Am Stat 55:19–24.[CrossRef]
Hogg JT, Hass CC, and Jenni DA, 1992. Sex-biased maternal expenditure in Rocky Mountain bighorn sheep. Behav Ecol Sociobiol 31:243–251.[Web of Science]
James WH, 1985. Sex ratio, dominance status and maternal hormone levels at the time of conception. J Theor Biol 114:505–510.[Web of Science][Medline]
James WH, 1996. Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels at the time of conception. J Theor Biol 180:271–286.[CrossRef][Web of Science][Medline]
Johnson CN, 1988. Dispersal and the sex-ratio at birth in primates. Nature 332:726–728.[CrossRef][Medline]
Johnson DH, 1999. The insignificance of statistical significance testing. J Wildlife Manage 63:763–772.[CrossRef]
Jorgenson JT, Festa-Bianchet M, Gaillard, J-M, and Wishart WD, 1997. Effects of age, sex, disease and density on survival of bighorn sheep. Ecology 78:1019–1032.[CrossRef][Web of Science]
Jorgenson JT, Festa-Bianchet M, Lucherini M, and Wishart WD, 1993. Effects of body size, population density, and maternal characteristics on age at first reproduction in bighorn ewes. Can J Zool 71:2509–2517.[CrossRef]
Jorgenson JT, Festa-Bianchet M, and Wishart WD, 1998. Effects of population density on horn development in bighorn rams. J Wildlife Manage 62:1011–1020.[CrossRef]
Kojola I, 1997. Behavioural correlates of female social status and birth mass of male and female calves in reindeer. Ethology 103:809–814.[Web of Science]
Kojola I, and Eloranta E, 1989. Influences of maternal body weight, age and parity on sex ratio in semidomesticated reindeer (Rangifer t. tarandus). Evolution 43:1331–1336.[CrossRef][Web of Science]
Krackow S, 1995. Potential mechanisms for sex ratio adjustment in mammals and birds. Biol Rev Camb Phil Soc 70:225–241.[Medline]
Kruuk LEB, Clutton-Brock TH, Albon SD, Pemberton JM, and Guinness FE, 1999. Population density affects sex ratio variation in red deer. Nature 399:459–461.[CrossRef][Medline]
Leimar O, 1996. Life-history analysis of the Trivers and Willard sex-ratio problem. Behav Ecol 7:316–325.
Lindström J, Coulson T, Kruuk L, Forchhammer MC, Coltman DW, and Clutton-Brock TH, 2002. Sex-ratio variation in Soay sheep. Behav Ecol Sociobiol 53:25–30.[CrossRef][Web of Science]
Monard AM, Duncan P, Fritz H, and Feh C, 1997. Variations in the birth sex ratio and neonatal mortality in a natural herd of horses. Behav Ecol Sociobiol 41:243–249.
Packer C, Collins DA, and Eberly LE, 2000. Problems with primate sex ratios. Phil Trans R Soc Lond 355:1627–1635.
Palmer AR, 2000. Quasireplication and the contract of error: lessons from sex ratios, heritabilities and fluctuating asymetry. Ann Rev Ecol Syst 31:441–480.[CrossRef][Web of Science]
Pélabon C, Gaillard J-M, Loison A, and Portier C, 1995. Is sex biased maternal care limited by total maternal expenditure in polygynous ungulates? Behav Ecol Sociobiol 37:311–319.[CrossRef][Web of Science]
Portier C, Festa-Bianchet M, Gaillard J-M, Jorgenson JT, and Yoccoz NG, 1998. Effects of density and weather on survival of bighorn sheep lambs (Ovis canadensis). J Zool Lond 245:271–278.[CrossRef]
R Development Core Team, 2003. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (www.R-project.org.)
Reimers E, and Lenvik D, 1997. Fetal sex ratio in relation to maternal mass and age in reindeer. Can J Zool 75:648–650.
Richards SM, 1974. The concept of dominance and methods of assessment. Anim Behav 22:914–930.[CrossRef]
Schall R, 1991. Estimation in generalized linear models with random effects. Biometrika 78:719–727.
Sheldon BC, and West AC, 2004. Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals. Am Nat 163:40–54.[CrossRef][Medline]
Silk JB, 1983. Local resource competition and facultative adjustment of sex ratios in relation to competitive ability. Am Nat 121:56–66.[CrossRef][Web of Science]
Simpson MJA, and Simpson AE, 1982. Birth sex ratios and social rank in rhesus monkey mothers. Nature 300:440–441.[CrossRef][Medline]
Steidl, RJ, Hayes JP, and Schauber E, 1997. Statistical power analysis in wildlife research. J Wildlife Manage 61:270–279.[CrossRef]
Thouless CR, 1990. Feeding competition between grazing red deer hinds. Anim Behav 40:105–111.[CrossRef]
Trivers RL, and Willard DE, 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92.
Van Shaik CP, and Hrdy SB, 1991. Intensity of local resource competition shapes the relationship between maternal rank and sex ratios at birth in cercopithecine primates. Am Nat 138:1555–1562.[CrossRef]
Williams GC. 1979. The question of adaptive sex ratio in outcrossed vertebrates. Proc R Soc Lond B 205:567–580.[Medline]
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