Benefits of dominance for behaviour and reproduction in primates

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/237021942 Benefits of dominance for behaviour and reproduction in primates ARTICLE in AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY · JANUARY 2012 Impact Factor: 2.38 READS 87 4 AUTHORS, INCLUDING: Bonaventura Majolo Julia Lehmann 61 PUBLICATIONS 576 CITATIONS 61 PUBLICATIONS 2,340 CITATIONS University of Lincoln SEE PROFILE University of Roehampton SEE PROFILE Gabriele Schino Italian National Research Council 95 PUBLICATIONS 2,549 CITATIONS SEE PROFILE Available from: Julia Lehmann Retrieved on: 04 February 2016 American Journal of Physical Anthropology Journal Copy of e-mail Notification American Journal of Physical Anthropology Published by John Wiley & Sons, Inc. Dear Author, Your article page proofs for American Journal of Physical Anthropology are ready for review. John Wiley & Sons has made this article available to you online for faster, more efficient editing. 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Schino3 AQ1 1 School of Psychology, University of Lincoln, Brayford Pool, Lincoln LN6 7TS, UK Centre for Research in Evolutionary Anthropology, University of Roehampton, London, UK 3 Istituto di Scienze e Tecnologie della Cognizione, Consiglio Nazionale delle Ricerche, Rome, Italy 4 Dipartimento di Biologia Animale e dell’Uomo, Università La Sapienza, Rome, Italy 2 KEY WORDS dominance; feeding success; fecundity; mating; meta-analysis; phylogeny; rank; reproductive success ABSTRACT Dominance hierarchies are thought to provide various fitness-related benefits to dominant individuals (e.g., preferential access to food or mating partners). Remarkably, however, different studies on this topic have produced contradictory results, with some showing strong positive association between rank and fitness (i.e., dominants gain benefits over subordinates), others weak associations, and some others even revealing negative associations. Here, we investigate dominance-related benefits across primate species while controlling for phylogenetic effects. We extracted data from 94 published studies, representing 25 primate species (2 lemur species, 4 New World monkeys, 16 Old World monkeys, and 3 apes), to assess how dominance affects life-history and behavior. We used standard and phyloge- In group-living primates, the outcome of agonistic interactions between group members often determines an individual’s dominance position within the group. Animals strive to obtain high dominance ranks as dominance may give various fitness-related benefits (e.g., Pusey and Packer, 1997; Silk, 2007), such as preferential access to food (Whitten, 1983; Isbell et al., 1999) or mating partners (Alberts et al., 2006), and ultimately greater reproductive success (Ostner et al., 2008; Rodriguez-Llanes et al., 2009). Although dominance hierarchies, with their associated benefits and costs for dominant/subordinate individuals, are a key aspect of primate societies (Wrangham, 1980; van Schaik, 1983; Isbell, 1991; Sterck et al., 1997), very few studies have attempted to concurrently analyze the various possible benefits of dominance in a species or population (e.g., Alberts et al., 2006). Most studies have focused on just one benefit of dominance, one sex and/or on a single genus (for a review see: Cowlishaw and Dunbar, 1991; Ellis 1995; Rodriguez-Llanes et al., 2009), and results across different studies are often inconsistent and little consensus exists as to the actual benefits obtained from high rank (see below). Thus, investigating the different dominance-related benefits across primate species is valuable, as this can help determine to what extent the benefits of being dominant are consistent across different behavioral and reproductive parameters. In addition, such an approach can shed light on how selective pressures impact life history variables and social behavior. Therefore, our aim was to analyze the benefits that dominance can give in terms of feeding, mating and reproductive success in male and female primates. When addressing this topic, two important aspects have to be considered. First, analyses run across primate C 2012 V netic meta-analyses to analyze the benefits of dominance in primates. Dominant females had higher infant survival to first year, although we found no significant effect of dominance on female feeding success. Results for female fecundity differed between the two meta-analytical approaches, with no effect of dominance on female fecundity after controlling for phylogeny. Dominant males had a higher fecundity and mating success than subordinate males. Finally, the benefits of dominance for female fecundity were stronger in species with a longer lifespan. Our study supports the view that dominance hierarchies are a key aspect of primate societies as they indeed provide a number of fitness-related benefits to individuals. V 2012 Wiley Am J Phys Anthropol 000:000–000, 2012. C Periodicals, Inc. species need to be corrected for potential phylogenetic biases (Nunn and Barton, 2001) as phylogeny can modulate the benefits of dominance and because data available in the primate literature are often biased in favor of more frequently studied taxa (e.g., Macaca). Second, various differences, gaps and inconsistencies across populations and species exist in the studies that have investigated the benefits of dominance in primates. Such differences can be due to the high degree of within-species variability (e.g., Henzi and Barrett, 2003), in terms of ecology, competitive regime, group size or mating patterns. Within-species variability can affect the benefits dominant animals gain over subordinate individuals (Chapman and Rothman, 2009). For example, variability in female estrous synchrony between troops or breeding seasons can result in different opportunities for dominant males to monopolize females (Ostner et al., 2008). Similarly, a greater frequency of copulations by dominant males does not always result in a higher reproductive success (Itoigawa et al., 1992; Paul et al., 1993; but see Alberts et al., 2006), possibly because of effective Additional Supporting Information may be found in the online version of this article. *Correspondence to: Bonaventura Majolo, School of Psychology, University of Lincoln, Brayford Pool, Lincoln LN6 7TS, UK. E-mail: bmajolo@lincoln.ac.uk Received 18 May 2011; accepted 8 January 2012 DOI 10.1002/ajpa.22031 Published online in Wiley Online Library (wileyonlinelibrary.com). WILEY PERIODICALS, INC. ID: nareshrao Date: 21/1/12 Time: 10:09 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012 NOTE TO AUTHORS: This will be your only chance to review this proof. Once an article appears online, even as an EarlyView article, no additional corrections will be made. J_ID: ZC0 Customer A_ID: 2011-00139.R3 Cadmus Art: AJPA22031 Date: 21-JANUARY-12 2 Stage: I Page: 2 B. MAJOLO ET AL. counter-strategies by subordinate males (e.g., sneaky copulations) that may limit the benefits of dominance (Berard et al., 1993; Setchell, 2008). Moreover, discrepancies between studies on the same species may also be due to differences in observational setting (e.g., opportunities for sneaky copulations by subordinates in captivity may be low in comparison to the wild due to the small size of the enclosure), methodology, and/or sample size (either in terms of number of individuals studied or duration of the study). For example, in separate studies on captive rhesus macaques (Macaca mulatta), Duvall et al. (1976) found a negative relationship between dominance and number of offspring sired (dominant males had lower paternity) in their 1-year study on eight males, whereas Smith (1993) found the opposite result on 32 males in a 15-year period. Therefore, in order to effectively analyze the benefits of dominance across primates, it is necessary not only to control for the effect of phylogeny but also to take into account intraspecific variation due to within-species variation or to differences across studies in study setting, duration, or sample size (Chapman and Rothman, 2009). Here we present the first study that addresses both of these points, using a metaanalytical approach through which we assess the cumulative fitness-related and sexspecific benefits of dominance across primates, while at the same time taking phylogeny into account. We also analyzed whether the benefits of dominance are modulated by a series of other life-history variables: body weight, lifespan, age at sexual maturity, and interbirth interval. We analyzed the effect of adult body weight on feeding success as body weight determines daily energetic requirements and can thus modulate differences in feeding success among individuals of different rank positions (Whitten, 1983; Isbell et al., 1999). Therefore, we predict that the benefits of dominance would be stronger in species with a larger body weight. When analyzing mating success and reproductive success (i.e., fecundity and infant survival to first year) we considered, as modulator variables, body size, life span and age at sexual maturity for males or females, as well as interbirth interval for females, because these variables can affect reproductive success independently of dominance between species and/or between individuals of different rank (e.g., Kappeler and Pereira, 2002; Clutton-Brock, 2009). We predict that the reproductive benefits of dominance would be more evident in species with a longer lifespan, with a shorter interbirth interval or in those who reach sexual maturity earlier (Altmann and Alberts, 2003). METHODS Data collection We used PrimateLit, available online at http://primatelit.library.wisc.edu, to review the primatological literature for studies testing the benefits of dominance. This database contains all published studies on primates since 1940. Our data collection was restricted to the period from 1940 to March 2009. We also reviewed various books on primates as an additional source of data. To be included in our dataset, a study had to contain a test (or a table with the raw data per individual) on the relationship between rank and one or more of the following variables: mating success (N of copulations), fecundity (N infants produced), infant survival to first year, and feeding success. As a measure of feeding success we consid- ered together rate of food intake (N of items eaten per hour), rate of energy intake (amount of calories ingested per hour), or time spent feeding (defined as picking up or gnawing a food item), as no sufficient studies were available to test these variables independently from one another. Studies on  4 animals were discarded as this figure is too small for the calculation of the estimated variance of an effect size (Hedges and Olkin, 1985; Gates, 2002). We also considered the following variables that were later discarded from analyses due to the small number of studies available (N  6): adult survival, age at first birth, foraging effort, and % of body fat. From each suitable study we extracted data on sample size (N of individuals studied), study setting (captivity, provisioned free-ranging, or wild), sex of the study animals, duration of the study (in months), group size and its composition. The dataset for this study comprised 94 published studies on 25 primate species (2 lemur species, 4 New World monkeys, 16 Old World monkeys, and 3 apes; Table 1). Species-specific values for the modulator variables were extracted from four published studies (Harvey et al., 1987; Rowe, 1996; Smith and Jungers, 1997; Kappeler and Pereira, 2002; Table 2). Statistical analyses We used meta-analytical techniques to take into account differences across studies in sample size and study setting, and the nonindependence of data from different species due to their common ancestry. Meta-analysis represents a powerful tool to determine the consistency of a biological phenomenon across taxa and to control for between-study variation (Hedges and Olkin, 1985). It relies on the calculation of an effect size, a standardized measure of the magnitude of the effect of an independent variable on a dependent variable and its weighted average across a range of studies that have addressed the same general question. As such, metaanalysis provides a more reliable estimate of the overall effect of a given explanatory variable on a biological phenomenon than any individual study. Meta-analytical techniques are also used to investigate the sources of variation in effect sizes (Hedges and Olkin, 1985; Sterne et al., 2001; Gates, 2002). We used Pearson correlation coefficients as effect size of the relationship between rank and fitness-related benefits (namely, feeding success, mating success, fecundity, and infant survival to first year). Correlation coefficients were transformed by the Fisher transformation to z values and inserted as such into analyses (Gates, 2002). We used the two meta-analytical approaches currently available: standard and phylogenetic meta-analysis. The use of two meta-analytical techniques was considered necessary to take advantage of their respective strengths and to control for their limitations. In particular, standard meta-analysis allowed us to consider each study as a separate data point (Hedges and Olkin, 1985). This is beneficial because fine-tuned analyses can be run on factors that can vary dramatically across groups and populations of the same species (e.g., group size; Majolo et al., 2008). However, standard meta-analysis does not take phylogenetic effects into account when calculating weighted average effects sizes, so the analyses are at risk of being biased in favor of more frequently studied taxa (here Macaca and Papio). Hence, the results obtained may not be safely generalized to other taxonomic levels (e.g., the entire Primate Order). Furthermore, when American Journal of Physical Anthropology ID: nareshrao Date: 21/1/12 Time: 10:09 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012 T1 T2 J_ID: ZC0 Customer A_ID: 2011-00139.R3 Cadmus Art: AJPA22031 Date: 21-JANUARY-12 Stage: I Page: 3 3 BENEFITS OF DOMINANCE TABLE 1. Details of the species and of the Pearson correlation coefficients (averaged per species and per variable) used in the standard and phylogenetic meta-analysis Pearson correlation coefficients Females Feeding success Species Cebus apella Cebus capucinus Cebus nigrivittatus Cercocebus torquatus Chlorocebusaethiops Erythrocebuspatas Gorilla gorilla Lemur catta Leontopithecusrosalia Macaca arctoides Macaca fascicularis Macaca fuscata Macaca mulatta Macaca nemestrina Macaca radiata Macaca sylvanus Mandrillus sphinx Microcebusmurinus Pan paniscus Pan troglodytes Papio anubis Papio cynocephalus Papio hamadryas Papio ursinus Semnopithecus entellus Males Infant survival to first year Fecundity Mating success Fecundity 0.84 20.24 0.02 0.47 0.20 0.09 0.31 0.15 0.24 0.66 0.02 20.57 20.54 0.72 0.79 20.68 0.52 0.58 0.15 0.79 0.002 20.04 0.13 0.12 20.10 0.50 0.39 0.05 0.25 0.36 0.73 0.75 0.59 0.28 0.84 0.74 0.41 0.13 0.16 0.33 20.30 0.14 0.24 0.43 20.04 0.39 0.22 0.84 0.57 0.49 0.23 0.65 0.47 0.36 0.32 20.46 0.14 0.84 0.80 0.72 0.73 0.85 0.93 Reference* 1 2, 3 4 5, 6 7–10 10 11 12, 13 14 15 16–18 19–34 35–49 50 51, 52 53–59 60, 61 62 63, 64 65–73 74–83 84–89 90 91 92–94 Note that we did not have sufficient data to analyze female mating success and male feeding success or male infant survival to first year of age (*See Supporting Information for the full details of the references used). TABLE 2. Summary and description of the modulator variables used to analyze the effect of species ecology and social structure on the relations between rank and our four dependent variables (feeding success, fecundity, infant survival, mating success) Variable name Female/male body weight Female age at sexual maturity Interbirth interval Male/female lifespan Variable type Source Continuous (Kg) Continuous (months) Continuous (months) Continuous (months) a,b b,c b,c d,b a Smith and Jungers, 1997. Harvey et al., 1987. c Kappeler and Pereira, 2002. d Rowe, 1996. b investigating sources of variation across species in effect sizes, standard meta-analysis does not control for the effect of phylogenetic relatedness (Hedges and Olkin, 1985). Therefore, we also used phylogenetic meta-analysis, a statistical tool recently developed by Adams (2008). This analytical tool combines phylogenetic methods with standard meta-analysis, allowing us to incorporate evolutionary history in the analysis. One limitation of phylogenetic meta-analysis, however, is that it requires a single effect size per species and variable, because phylogenetic distances between species are used as covariates in the analysis. Thus, data from multiple populations within a species cannot easily be accommodated. This means that when multiple studies are addressing the same phenomenon (e.g., the effect of dominance on mating success), data have to be combined per species. In doing so, important information on within-species behav- ioral flexibility can be lost. In fact, the average figure per species may not be representative of any real population or group. Primate phylogeny was based on the 10ktrees primate phylogeny version 2 (using a consensus tree and the phylogram branch option; Arnold et al., 2010), accessible at: http://10ktrees.fas.harvard.edu. This online resource applies the recent advances in Bayesian phylogenetics to resolve uncertain nodes and provides phylogenetic relationships and branch length for 230 primate species. For both standard and phylogenetic meta-analysis, we ran a series of general linear models to test the effect of duration of the study (in months), study setting (i.e., captivity, provisioned or wild), and group size on our effect sizes. We found no significant effect of these three factors (analyses not shown here for brevity). Therefore, we excluded duration of the study, study setting, and group size from the subsequent analyses. We first ran a general effects standard meta-analysis on the complete dataset (i.e., including data on both males and females and on all the four test variables) to test for the overall effect that dominance may have on fitness-related benefits in primates. We then used standard and phylogenetic meta-analysis to test, in females and/or males, the relationship between rank and feeding success, mating success, fecundity, and infant survival to first year. Standard meta-analysis was run on the effect size calculated for each single study and thus the N values reported below refer to the number of studies available for each variable. For the phylogenetic meta-analysis, we first had to calculate one effect size per species. When we only had one study for a species and variable (e.g., a single study analyzing the relationship between American Journal of Physical Anthropology ID: nareshrao Date: 21/1/12 Time: 10:09 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012 J_ID: ZC0 Customer A_ID: 2011-00139.R3 Cadmus Art: AJPA22031 Date: 21-JANUARY-12 4 Stage: I Page: 4 B. MAJOLO ET AL. Fig. 1. Forest plot showing the effect size (dots) and confidence intervals (horizontal lines) of the studies used for this metaanalysis for males and females (solid lines: females; dotted lines: males). The distribution of effect sizes indicates a sex difference. Each line represents one study (N 5 136). mating success and dominance in male Microcebus murinus), we calculated the effect size for this study directly and entered this species-value in the phylogenetic metaanalysis. However, when we had 2 studies per species and variable we run a meta-analysis for each species/variable for which we had multiple data to obtain a weighted average effect size per species and variable. Sample sizes were averaged across studies from the same species. In the phylogenetic meta-analysis N values refer to the number of species available. Standard meta-analysis was run in Stata (version 10.1; StataCorp LP, College Station, TX, USA) while phylogenetic meta-analysis was run using R version 2.13.2 (R Development Core Team, 2010). We used meta-regressions (Sharp, 1998) to test whether the relationship between rank and our measures of fitness-related benefits (i.e., the effect size of the relationship between rank and, respectively, feeding success, mating success, fecundity, and infant survival to first year) was affected by a series of modulator variables (Table 2). Modulator variables were entered all together in the meta-regressions. For the standard meta-analysis, we present the weighted average effect size, its 95% confidence intervals, sample size, z and P value. For the phylogenetic meta-analysis we present the cumulative effect size, its standard error, sample size, and permutated P value, derived from randomization (Adams, 2008), thus, no test statistic is provided along with the P-values. A positive effect size indicates a positive relationship between dominance and a dependent variable that is, dominant individuals would have greater fecundity, infant survival, mating or feeding success than subordinates. Publication bias (i.e., the tendency for studies with significant results to be more likely to be published than those with nonsignificant results) is a potential problem for meta-analysis. To control for this we ran, for each variable, an Egger test for publication bias (Egger et al., 1997). The Egger test consists of a regression of the normalized effect estimates (i.e., effect estimate divided by its standard error) against their precision (i.e., reciprocal number of the standard error of the estimate) as a measure of the symmetry of the effect sizes. A nonsignificant result of the Egger test indicates that no evidence of publication bias is apparent in the dataset. RESULTS Because of small sample size, we could not analyze the effect of dominance on female mating success (N of studies 5 4) nor, in males, the relationship between rank and feeding success (N 5 3) or infant survival (N 5 0). None of the Egger test for publication bias was significant (all slopes \ 0.63, all t \ |1.32|, all P [ 0.21). Therefore, no correction for publication bias was applied. General effects Overall, dominance provides strong fitness-related benefits, with a large average effect size (r 5 0.44, 95%CI 5 0.39 2 0.48, z 5 18.32, N 5 136) that is significantly different from a null effect of zero (P \ 0.001). This effect, however, was stronger in males than in females (b 6 SE 5 0.49 6 0.07, t 5 6.61, N 5 136, P \ 0.001; Fig. 1) and it was affected by the type of benefit considered (i.e., feeding or mating success, fecundity, and infant survival to first year: b 6 SE 5 0.07 6 0.03, t 5 2.13, N 5 136, P \ 0.05; Fig. 2), suggesting that the extent to which dominance provides benefits varies with the type of benefits considered. Therefore, below we ran the analyses independently for females and males and for the different benefits related to dominance, using standard and phylogenetic meta-analysis. American Journal of Physical Anthropology ID: nareshrao Date: 21/1/12 Time: 10:09 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012 F1 F2 J_ID: ZC0 Customer A_ID: 2011-00139.R3 Cadmus Art: AJPA22031 Date: 21-JANUARY-12 Stage: I Page: 5 5 BENEFITS OF DOMINANCE Fig. 2. Forest plot showing the effect size (dots) and confidence intervals (horizontal lines) of the studies used for this metaanalysis for the different response variables (solid lines: feeding success; dotted lines: mating success; dashed line: fecundity; dotted-dashed lines: infant survival to first year). The distribution of effect sizes indicates differences depending on the response variables. Each line represents one study (N 5 136). TABLE 3. Coefficients and significance of the variables considered as possible modulators of the relationship between female fecundity and rank (significant results are in bold) Variable b 6 SE Female body weight Female age at sexual maturity Interbirth interval Female lifespan 20.02 0.02 20.01 0.02 6 6 6 6 Standard meta-analysis t 0.10 0.02 0.02 0.01 Females Feeding success. We found no significant relationship between rank and feeding success in female primates using both standard (r 5 0.09, 95%CI 5 20.01 2 0.27, z 5 0.92, N 5 14, P 5 0.36) and phylogenetic meta-analysis (cumulative effect size 6 SE 5 20.79 6 0.86, N 5 9, P 5 0.96). Similarly, we found no significant effect of female body weight (the only modulator variable tested) on the relationship between rank and feeding success running a meta-regression with both standard metaanalysis (b 6 SE 5 0.06 6 0.04, t 5 1.45, P 5 0.16) and phylogenetic meta-analysis (b 6 SE 5 0.07 6 0.04, P 5 0.27). Fecundity. We found that dominant females had a significantly greater fecundity using standard meta-analysis (r 5 0.19, 95%CI 5 0.09 2 0.29, z 5 3.75, N 5 25, P \ 0.001). Conversely, rank was not significantly related to female fecundity when using phylogenetic meta-analysis (cumulative effect size 6 SE 5 20.17 6 1.41, N 5 14, P 5 0.90). With standard (but not with phylogenetic) meta-analysis we found that the higher fecundity for 22.21 1.56 20.74 2.65 P 0.04 0.14 0.47 0.02 Phylogenetic meta-analysis b 6 SE P 20.02 0.02 20.01 0.07 6 6 6 6 0.02 0.01 0.02 0.02 0.99 0.82 0.54 0.002 dominant females was negatively affected by female body weight (Table 3). With both standard and phylogenetic meta-analysis, the relationship between rank and fecundity was stronger in species with longer lifespans (Table 3). The other modulator variables had no effect on the relationship between rank and female fecundity (Table 3). Infant survival. Dominant females had a higher proportion of infants surviving to their first year of age than subordinates using both standard meta-analysis (r 5 0.20, 95%CI 5 0.13 2 0.27, z 5 5.49, N 5 21, P \ 0.001) and phylogenetic meta-analysis (cumulative effect size 6 SE 5 1.25 6 1.22, N 5 14, P \ 0.05). We found that the relationship between dominance and infant survival to first year was negatively modulated by female lifespan when using standard meta-analysis (Table 4). The other analyses gave nonsignificant results (Table 4). Males Mating success. We found a strong effect size for the relationship between male dominance and mating American Journal of Physical Anthropology ID: nareshrao Date: 21/1/12 Time: 10:09 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012 T3 T4 J_ID: ZC0 Customer A_ID: 2011-00139.R3 Cadmus Art: AJPA22031 Date: 21-JANUARY-12 6 Stage: I Page: 6 B. MAJOLO ET AL. TABLE 4. Coefficients and significance of the variables considered as possible modulators of the relationship between infant survival to first year and rank in females (significant results are in bold) Standard meta-analysis Variable b 6 SE Female body weight Female age at sexual maturity Interbirth interval Female lifespan 20.01 0.02 20.02 20.02 6 6 6 6 0.01 0.01 0.01 0.01 Phylogenetic meta-analysis t P 21.54 2.02 21.26 22.53 0.15 0.07 0.23 0.03 b 6 SE 20.01 0.02 20.02 20.03 6 6 6 6 0.00 0.00 0.01 0.01 P 0.92 0.11 0.75 0.98 TABLE 5. Coefficients and significance of the variables considered as possible modulators of the relationship between rank and, respectively, mating success or fecundity in males Standard meta-analysis Variable Mating success Male body weight Male age at sexual maturity Male lifespan Fecundity Male body weight Male age at sexual maturity Male lifespan T5 Phylogenetic meta-analysis b 6 SE t P b 6 SE P 20.01 6 0.01 0.01 6 0.01 20.00 6 0.02 20.74 0.38 20.13 0.47 0.71 0.90 20.05 6 0.02 0.02 6 0.01 0.00 6 0.01 0.41 0.60 0.41 0.03 6 0.03 20.01 6 0.01 20.00 6 0.03 0.84 20.53 20.07 0.41 0.60 0.95 20.02 6 0.02 0.00 6 0.01 0.01 6 0.01 0.71 0.29 0.40 success, i.e., dominant males were found to have a higher copulation frequency than subordinates using both standard (r 5 0.66, 95%CI 5 0.55 2 0.78, z 5 10.94, N 5 50, P \ 0.001) and phylogenetic meta-analysis (cumulative effect size 6 SE 5 1.86 6 1.18, N 5 13, P \ 0.05). We found no significant effect of the modulator variables (Table 5). Fecundity. Dominant males had higher fecundity than subordinates when using standard meta-analysis (r 5 0.71, 95%CI 5 0.48 2 0.95, z 5 6.01, N 5 26, P \ 0.001). This effect became marginally nonsignificant with phylogenetic meta-analysis (cumulative effect size 6 SE 5 1.36 6 0.62, N 5 13, P 5 0.076). We found no significant effect of the modulator variables (Table 5). DISCUSSION Overall, our study supports the view that attaining a dominant position provides various fitness benefits across a variety of species as proposed by socio-ecological models (Wrangham, 1980; van Schaik, 1983; Isbell, 1991; Sterck et al., 1997). In the general standard meta-analysis, we found that rank had a larger effect on male than on female fitness (for a similar result see: Ellis, 1995). This is consistent with sexual selection theory and with the widespread sexual dimorphism in body and canine size observed in primates (Dixon, 1998). Our analysis on the whole dataset further suggests that the benefits conveyed by dominance differ between the two sexes and in relation to the type of benefit. However, this conclusion needs to be supported by further data as we could not always run analyses on the same variable for the two sexes due to lack of data in the literature. The differences observed between the various benefits of dominance analyzed here confirm our claim that testing these benefits independently is key to fully understanding the importance of dominance hierarchies in primates. Rank-related benefits for female primates We found that dominance significantly enhanced female reproductive success in terms of infant survival and fecundity (although phylogenetic meta-analysis did not confirm this latter result; see below for discussion). Indeed, modern socio-ecological models predict that, similar to what is found in males (e.g., Ellis, 1995; Ostner et al., 2008), female primates gain fitness-related benefits by attaining dominant positions. A greater reproductive success for dominant females may be due to various factors, including male mate choice, dominance-related differences in physical conditions or stress reduction (Abbott, 1984; Barton and Whiten, 1993; Kappeler and Pereira, 2002), although we could not test this with our data set. The higher infant survival for dominant females is probably due to the agonistic support infants receive from their dominant mothers which may result in preferential access to food sources and reduced risk of aggression from other group members (e.g., Wolfe, 1984; Kleindorfer and Wasser, 2004). The significant positive effect of dominance on female fecundity disappeared when using phylogenetic metaanalysis, indicating that female fecundity may be positively correlated with rank in some, probably closely related, species (e.g., Whitten, 1983; Saito, 1996) but not in primates in general. Our dataset showed a strong bias in terms of taxa represented in the dataset (i.e., the genera Macaca or Papio were over-represented; see Table 1 and discussion below). Therefore, the contrasting results of the two meta-analyses may be due to the fact that the relationship between female fecundity and rank holds true in some species (e.g., macaques; Rodriguez-Llanes et al., 2009) but not necessarily for all primates. For example, dominance can predict reproductive success in despotic species, such as rhesus or Japanese macaques (e.g., Wolfe, 1984), but not in species with shallower dominance hierarchies such as in colobines (Chapman and Rothman, 2009). Dominance did not have a significant effect on feeding success in females using either of the two meta-analyses. A higher feeding success should in theory translate into American Journal of Physical Anthropology ID: nareshrao Date: 21/1/12 Time: 10:09 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012 J_ID: ZC0 Customer A_ID: 2011-00139.R3 Cadmus Art: AJPA22031 Date: 21-JANUARY-12 Stage: I 7 BENEFITS OF DOMINANCE better physical condition, which is a key element for females to reproduce successfully (Barton and Whiten, 1993; Isbell et al., 1999). As such, our results on feeding and reproductive success (i.e., fecundity and infant survival to first year) are somehow contradictory. As a measure of feeding success we considered together three different variables (i.e., rate of food intake or of energy intake, time spent feeding) as not enough studies were available to independently analyze each of these variables. This combination of three variables, together with the difficultly to make direct comparisons between feeding and reproductive success (as different species were represented in the two analyses), might explain our results. Moreover, individuals have been observed to compensate for a lower feeding success by increasing the time they devote to searching for food (Saito, 1996). If this strategy holds true across primates, we would expect a greater foraging effort in subordinate individuals. Unfortunately, we could not test this hypothesis as we did not find a sufficient number of studies to analyze the relationship between rank and foraging effort. The apparent contradictions between different benefits of dominance highlights the importance of analyzing such benefits independently from one another, as attempted in this study. Rank-related benefits for male primates Dominant males were found to have higher mating success and to a lesser extent (as the result of the phylogenetic meta-analysis was marginally nonsignificant), greater fecundity than subordinates. As such our results are in agreement with previous studies on the topic (e.g., Duvall et al., 1976; Alberts et al., 2006; Ostner et al., 2008), including a recent meta-analysis on male reproductive success in macaques (Rodriguez-Llanes et al., 2009). Dominant males can attain increased mating opportunities through winning direct competition with subordinate males, female mate choice, coercion of mating, and/or successful mate guarding (Kutsukake and Nunn, 2006; Ostner et al., 2008; Rodriguez-Llanes et al., 2009). The different results obtained for male fecundity from the standard and phylogenetic meta-analysis indicate that, similar to what we found for female fecundity (see above), dominant males obtain higher paternity in some primate species but not in others. Such differences among species may be due to differences in sperm competition (Dixon, 1998), in female estrous synchrony (Ostner et al., 2008), and/or in the opportunities for sneaky copulations. For example, sneaky copulations may be more frequent in species living in dense forests than in open habitats where visibility is better and in the wild than in small-size enclosures. The scarcity of data on feeding success in males probably reflects the fact that socio-ecological models mainly focus on the effect that food distribution and abundance have on female grouping patterns and reproductive success (Wrangham, 1980; Isbell, 1991; Sterck et al., 1997). Testing the validity of this model for males in the wild is necessary in order to understand if food distribution has a similar effect on reproductive success in males as it does in females. Factors affecting rank-related benefits in primates The importance of lifespan in modulating rank-related differences in mating opportunities and reproduction has Page: 7 been theoretically predicted (e.g., Chapais, 1990). However, few empirical studies have tested this effect (e.g., Bercovitch and Strum, 1993; Altmann and Alberts, 2003) probably due to the long lifespan of many primate species, which makes data collection challenging. Here we found that rank-related benefits for female fecundity were stronger in species with a longer lifespan. One possible explanation is that, in species with a longer lifespan, dominant individuals can maintain their rank position longer and this has a positive effect on their reproductive success. We obtained the opposite result for rank-related effects on infant survival to first year, as this relationship was negatively modulated by lifespan with standard but not phylogenetic meta-analysis. This suggests that the selective pressure for rank-related benefits is stronger in species with a shorter lifespan. Similarly, body size had a negative effect on female fecundity when using standard meta-analysis. Therefore, speciesspecific differences in life history variables do not have consistent effects on the benefits of dominance. The other analyses on the effect of the modulator variables gave non-significant results for either females or males. The steepness of a dominance hierarchy, and thus the power differences between individuals along the hierarchy, may vary significantly across species (Pusey and Packer, 1997). However, the benefits of dominance seem not to be systematically affected by species-specific differences in life history variables, such as interbirth interval and age at sexual maturity. This conclusion is in line with some previous studies that have reported no significant effects of, e.g., female estrous synchrony or study setting (captivity versus wild) on reproductive success (Kutsukake and Nunn, 2006; Rodriguez-Llanes et al., 2009; but see Ostner et al., 2008). It would be interesting to test whether variations in the steepness of the hierarchy are associated to variations in the effect of rank on fitness, so as to assess the functional consequences of variations in tolerance. However, it is often problematic to classify a species along some of the modulator variables (e.g., assign a species-specific value for age at sexual maturity). With the accumulation of data on a larger number of populations, we are learning that primates can be very flexible in their adaptation to local ecological conditions (e.g., Chapman and Rothman, 2009). The within-population variability of life-history parameters, such as age at sexual maturity or interbirth interval, may help subordinates to minimize the drawbacks of their low dominance rank. For example, subordinate individuals might have shorter interbirth intervals as a strategy to maximize their fitness (Setchell, 2008). Because of the observed variance among populations, it can be difficult to assign a species-specific value for these traits. Overall, the main conclusion of our analysis of the factors modulating the effects of rank on fitness is that additional data are necessary before any reasonable synthesis can be attempted. Phylogeny With the exception of female fecundity, we found that the results of the two meta-analytical approaches were largely in agreement, both when addressing the overall effects of dominance and when analyzing the factors that may modulate these effects. In a study on seed germination in relation to seed size and seed passage through frugivores’ guts, Verdú and Traveset (2004) compared results obtained from standard meta-analysis and American Journal of Physical Anthropology ID: nareshrao Date: 21/1/12 Time: 10:10 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012 J_ID: ZC0 Customer A_ID: 2011-00139.R3 Cadmus Art: AJPA22031 Date: 21-JANUARY-12 8 Stage: I Page: 8 B. MAJOLO ET AL. nonmeta-analytic phylogenetic comparative methods. They found significant differences between the results obtained with the two methods and concluded that standard meta-analysis and phylogenetic methods should be used concurrently. However, the authors recognized that it is difficult to formulate conclusions when the two methods yield conflicting results. Although our results were largely consistent between the two meta-analytical approaches, a key question to answer is what method should preferentially be used in future research. This is particularly relevant because the two meta-analytical approaches have different benefits and drawbacks (see Methods). The choice between the two meta-analytical approaches depends on the research question one tries to address. Phylogenetic meta-analysis is more effective for between-species analyses and to control for potential phylogenetic biases while standard meta-analysis seems better suited to analyze the consistency of an effect within a taxon. One compromise might be to combine the benefits of the two meta-analytical approaches by creating a ‘‘dummy’’ variable where data for the same species but coming from different studies, groups or populations are artificially assigned a low degree of phylogenetic distance below the level of the species (Adams, pers. comm.). This would allow the researcher to run fine-tuned analyses at the group or population level while simultaneously controlling for phylogeny. This option needs to be tested to determine the robustness of phylogenetic meta-analysis to such approach. An alternate possibility would be to assess the actual effect of phylogeny on the dataset by calculating the strength of the phylogenetic signal (Lajeunesse, 2009). This signal could then be used to decide which method to use (assuming that the datasets are the same across methods). However, methods to calculate the strength of the phylogenetic signal in the context of meta-analyses are still at an early stage and alternative methods (e.g., the use of the Akaike Information Criterion to compare standard and phylogenetic meta-analysis) are being explored (Lajeunesse, 2011). Some authors have argued that one should always control for phylogenetic relationships in cross-species analyses (Nunn and Barton, 2001) and indeed, meta-analyses containing strongly uneven numbers of studies per species may be biased due to the effects of other life history variables, such as lifespan or interbirth interval. Here we have shown that the effects of dominance on male and female fecundity appear to differ between species, as there were no significant universal effects after phylogeny was controlled for. Thus, although in some species both sexes may benefit from high rank by increasing their fecundity, the overall significance in the meta-analysis appears to be biased by an overrepresentation of some species in the dataset. CONCLUSIONS This study shows that attaining a dominant position improves individual fitness in male and female primates and that this effect is true across the 13 genera studied here, even after controlling for phylogeny. Although studies of the fitness benefits of dominance have a long history in primatology, quantitative information on the different benefits dominant individuals gain over subordinates is still scanty, particularly with regard to some variables (e.g., male feeding success). Meta-analytical techniques (in particular phylogenetic meta-analysis) provide an important contribution to deepen our under- standing of biological phenomena, even in the face of inconsistencies in findings, sample size and study setting. To fully analyze the benefits of dominance in primates we need data on less-studied species, as the literature on this topic is currently significantly biased in favor of two genera, Macaca and Papio. ACKNOWLEDGMENTS The authors would like to thank Dean Adams, for his help and advice in the use of phylogenetic meta-analysis in R software, and Garry Wilson for useful comments on our manuscript. They thank Dr. Ruff and two anonymous reviewers for very constructive comments on an earlier version of our manuscript. This study complies with the laws on the use of animals for research in Great Britain and Italy. LITERATURE CITED Abbott DH. 1984. Behavioural and physiological suppression of fertility in subordinate marmoset monkeys. Am J Primatol 6:169–186. Adams DC. 2008. Phylogenetic meta-analysis. Evolution 62:567–572. Alberts SC, Buchan JC, Altmann J. 2006. Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72:1177–1196. 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American Journal of Physical Anthropology ID: nareshrao Date: 21/1/12 Time: 10:10 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012 J_ID: ZC0 Customer A_ID: 2011-00139.R3 Cadmus Art: AJPA22031 Date: 21-JANUARY-12 Stage: I Page: 10 AQ1: Please provide the department names for Affiliations 1 and 2. ID: nareshrao Date: 21/1/12 Time: 10:10 Path: N:/3b2/AJPA/Vol00000/120012/APPFile/JW-AJPA120012