The Society for Integrative and Comparative Biology
Bateman's Principle in Cooperatively Breeding Vertebrates: The Effects of Non-breeding Alloparents on Variability in Female and Male Reproductive Success1
1 Ecology, Evolution, and Behaviour, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand
2 Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, California 94720-3160
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The sex-specific slopes of Bateman's gradients have important implications for understanding animal mating systems, including patterns of sexual selection and reproductive competition. Intersexual differences in the fitness benefits derived from mating with multiple partners are expected to yield distinct patterns of reproductive success for males and females, with variance in direct fitness predicted to be greater among males. These analyses assume that typically all adults are reproductive and that failure to produce offspring is non-adaptive. Among some species of cooperatively breeding birds and mammals, however, non-breeding adult alloparents are common and may comprise the majority of individuals in social groups. The presence of a large number of non-breeding adults, particularly when coupled with greater social suppression of reproduction among females, may alter the relative variance in direct fitness between the sexes, thereby generating an apparent contradiction to Bateman's Paradigm. To explore quantitatively the effects of non-breeding alloparents on variance in reproductive success, we used genetic estimates of parentage and reproductive success drawn from the literature to calculate the relative variability in direct fitness for females and males in alloparental and "other" societies of birds and mammals. Our analyses indicate that in mammals and, to a lesser extent, in birds, variability in direct fitness is greater among females in species characterized by the presence of non-breeding alloparents. These data suggest that social interactions, including social suppression of reproduction, are powerful determinants of individual direct fitness that may modify sex-specific patterns of reproductive variance from those described by Bateman.
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INTRODUCTION |
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Sexual selection acts through differences in reproductive success (Darwin, 1871
; Andersson, 1994). Individuals whose phenotypes render them better able to attract or to compete for access to members of the opposite sex are expected to produce more offspring. As a result, the traits that make those individuals successful at acquiring reproductive partners will tend to increase in frequency in subsequent generations. Concomitantly, individuals who are better able to recognize and to select appropriate partners should out-reproduce those who are less discriminating, leading to an increased frequency of the traits associated with the choice of high-quality mates. The strength of selection on traits associated with intrasexual competition or intersexual choice is expected to increase as the differences in reproductive success among same-sex conspecifics increase. Thus, the intensity of sexual selection should be directly related to the variance in direct fitness among members of each sex (Arnold, 1994; Webster et al., 1995; Wade and Shuster, 2002).
A seminal, quantitative test of this statement was provided by Bateman (1948) in his now classic studies of mating behavior in Drosophila. Specifically, data from Bateman's fifth and sixth experiments (his Fig. 1b; 1948) indicate that while male reproductive success increases more or less linearly as a function of the number of mates, female reproductive success is not affected by the addition of second or subsequent mates. These findings have profound implications for sexual selection theory. Perhaps most importantly, Bateman's data suggest that while traits associated with the acquisition of multiple mating partners will be strongly selected for among males, the same will not be true for females since females do not accrue additional fitness benefits by mating with multiple males. As a direct corollary, variance in reproductive success is also expected to be greater among males, since enhanced competition for access to partners will result in a greater range of reproductive outcomes (e.g., highly successful versus unsuccessful) for members of this sex. The application of these predictions to other taxa has had a profound effect on the study of animal mating systems and "Bateman's Paradigm" has come to be widely accepted by behavioral ecologists as the basis for the typically greater elaboration of sexually dimorphic traits among males, rather than females (Tang-Martinez, 2000).
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A fundamental but often unstated assumption of this paradigm is that all adults in the population of interest are reproductively active (Bateman, 1948
; Webster et al., 1995; Woolfenden et al., 2002). Although some individuals may fail to produce offspring, these failures are not adaptive and represent a fitness loss imposed by biotic (e.g., predators, diseases) or abiotic (e.g., wind, flooding) environmental conditions (Koenig and Albano, 1986). In some cooperatively breeding species, however, non-breeding appears to be an adaptive trait that enhances the fitness of individuals that forego producing offspring and instead assist the reproductive efforts of others (Sherman et al., 1995). Social suppression of reproduction is a salient feature of these societies that is maintained by natural selection (Solomon and French, 1997; Koenig and Dickinson, 2004). Reproductive skew (Johnstone, 2000; Kokko, 2003) within such cooperatively breeding groups may substantially affect patterns of direct fitness, including estimates of variance in reproductive success. In particular, if reproductive suppression tends to be more extreme among females, this aspect of social structure may lead to apparent exceptions to Bateman's classic relationships between sex, variance in reproductive success, and the relative strength sexual selection. Here, we explore the effects of social suppression of breeding on patterns of male and female reproductive success. Using data drawn from the literature on cooperatively breeding birds and mammals, we compare estimates of the relative variability (range of fitness values) in female and male reproductive success for species in which (1) all adults are presumed to be reproductively active and (2) a demographically predictable subset of adults are socially suppressed non-breeders. Comparisons of these estimates suggest that socially imposed differences in breeding status have important implications for patterns of reproductive competition in animals, including the relative variance in reproductive success between the sexes. We discuss these findings within the context of Bateman's Paradigm and use the results of our comparative analyses to predict how the relative intensity of sexual selection may differ in species with social suppression of reproduction.
Bateman's curves, variance in reproductive success, and intersexual differences in sexual selection
One of the primary implications of Bateman's (1948) research is the expectation that the intensity of sexual selection should be greater among males than among females. This finding is consistent with predictions derived from anisogamy and intersexual differences in gametic investment, both of which suggest that females will be a limiting resource over which males should compete for reproductive opportunities (Parker, 1970). Underlying Bateman's empirical conclusion were data from Drosophila indicating that variance in individual reproductive success is greater for males, which Bateman (1948, p. 362) identified as "a sign of intra-masculine selection." Extrapolating from this statement, the relative variance in reproductive success for males versus females can be used as an indicator of expected intersexual differences in the intensity of sexual selection (Wade, 1979). This assertion is logically appealing because, as the variance in reproductive success increases, the magnitude of the fitness differences between unsuccessful and highly successful individuals should increase, thereby providing greater opportunity for selection to act on the phenotypic traits associated with mating and fertilization success (Wade and Arnold, 1980). For those studies of vertebrates that have quantified sexual selection for male and female conspecifics (e.g., Payne and Payne, 1977; Jones et al., 2001, 2002; Woolfenden et al., 2002; Strausberger and Ashley, 2003), the intensity of this selection is typically greater for males, except for classically sex-role reversed species (dusky pipefish Syngnathus floridae: Jones et al., 2000; wattled jacanas Jacana jacana: Emlen and Wrege, 2004). More generally, the well-established pattern that sexually dimorphic (i.e., potentially sexually selected) traits tend to be more elaborate among males is generally viewed as support for the prediction that sexual selection is more intense for members of this sex (Reeve and Pfennig, 2003).
At least two factors underlie the tendency for variance in reproductive success to be greater among males. One is the greater range of fitness values achieved by males, which results directly from the positive correlation between number of mates and individual fitness (our Fig. 1a). Bateman clearly recognized the importance of this relationship, which he described as "the cause of intra-masculine selection (1948, p. 362)." Indeed, plotting reproductive success against number of mates provides a particularly direct measure of variability in male reproductive success and, hence, the potential for sexual selection to act. As a result, the relative intensity of sexual selection may be better captured by Bateman-type curves than by standard statistical estimates of the variance in individual reproductive success. Specifically, Bateman curves have greater explanatory power than other statistical estimators because the former incorporate both mechanisms that underlie variation in overall reproductive success: mating success (number of mates) and reproductive output (number of offspring).
A second factor contributing to the greater relative variance in male reproductive success is the typically larger proportion of individuals of this sex that achieve no direct fitness (Fig. 1b). This component of variance in reproductive success was not explicitly addressed by Bateman because the slopes of Bateman-type curves do not change as the number of individuals that fail to reproduce (i.e., achieve zero direct fitness) increases. Nevertheless, published data from free-living birds and mammals indicate that the proportion of individuals that fail to reproduce is typically greater for males (Clutton-Brock, 1991), suggesting that non-breeders may be an important determinant of variance in direct fitness. Failure to produce offspring, however, is not limited to males and, if species or situations could be identified in which non-breeding is more prevalent among females, analyses of these systems may provide powerful insights into the effects of variance in reproductive success on the nature and strength of sexual selection.
Cooperative breeding and social suppression of reproduction
Studies of cooperatively breeding vertebrates represent a potentially important opportunity to explore the effects of variance in reproductive success on patterns of sexual selection. Numerous species of birds and mammals have been identified as cooperative breeders, meaning that adults live in groups, within which individuals contribute to the care of offspring that are not their own (Solomon and French, 1997; Koenig and Dickinson, 2004). Although cooperative breeders are behaviorally, ecologically, and phylogenetically diverse, these species are typically divided into two general types of cooperative societies: plural breeders and singular breeders (Brown, 1987). In plural (communally) breeding societies, all adult group members are reproductively active and alloparental care (i.e., care of non-offspring young) is typically performed by individuals with offspring of their own. In contrast, in singular breeding societies, production of offspring is typically limited to a single male and female per group who are assisted by a variable number of non-breeding adult alloparents ("helpers at the nest"). These categories are not absolute and populations or even social groups of conspecifics may shift breeding systems (i.e., singular, plural, or non-cooperative) between or, in some cases, within years (e.g., white-fronted bee-eaters Merops bullockoides: Emlen and Wrege, 1992; long-tailed tits Aegithalos caudatus: McGowan et al., 2003; carrion crows Corvus corone: Baglione et al., 2002; house mice Mus musculus, yellow bellied marmots Marmota flaviventris, and voles Microtus spp.: Solomon and French, 1997). Nevertheless, these designations are widely used as descriptors in the literature on cooperative breeding and, for many species, appear to represent reliable indicators of social and reproductive behavior.
One of the most distinctive features of singular-breeding societies is the restriction of direct reproduction to only a subset of group members (Wilson, 1975; Brown, 1987; Sherman et al., 1995). Numerous studies have examined the proximate mechanisms underlying reproductive suppression in cooperatively breeding animals (Faulkes et al., 1990; Creel et al., 1992; Emlen and Wrege, 1992; Saltzman et al., 1996; Brown and Vleck, 1998). Regardless of the specific mechanisms of suppression employed, however, available data indicate that in both mammals and birds, the reproductive differences between breeding and non-breeding group mates are socially induced, meaning that all individuals retain the physiological ability to reproduce and can become breeders when social conditions are appropriate (Brown, 1987; Sherman et al., 1995). As a result, non-breeding alloparental birds and mammals are potential breeders whose direct fitness should be considered when examining patterns of offspring production and variance in reproductive success for singular breeding cooperative societies. Because these animals should add a substantial number of zeros to estimates of individual direct fitness, inclusion of non-breeders may significantly affect estimates of the variance in reproductive success.
Direct fitness and variance in reproductive success in cooperatively breeding groups
The distinct reproductive structures of plural versus singular breeding groups of vertebrates should produce markedly different distributions of direct fitness in these two types of cooperatively breeding societies. Because typically all members of plural-breeding groups produce offspring, patterns of annual reproductive success are expected to be roughly normal in distribution (Fig. 2a). In particular, non-breeders are expected to comprise a relatively small proportion of individuals whose failure to reproduce reflects stochastic environmental or phenotypic effects. In singular breeding groups, however, socially suppressed non-breeders represent at least one-third of the individuals in a group (2 breeders and 
1 alloparent) and, in some species, may comprise the majority of animals that live together and cooperate to rear young (e.g., >90% in many naked mole-rat Heterocephalus glaber colonies: Reeve et al., 1990). As a result, annual direct fitness for singular breeders is expected to be bimodal in distribution (Fig. 2b), with one peak representing breeding animals and the other representing non-breeding alloparents. As the proportion of non-breeders increases, socially-suppressed individuals that fail to produce offspring are expected to have an increasingly substantial impact on overall patterns of direct fitness, including the variance in reproductive success among members of the same sex.
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The presence of a substantial number of non-breeding adults may impact variance in direct fitness in at least two ways. First, as long as the mean number of young produced by a group remains constant, increasing the number of non-breeders in a group should increase the spread of data points for individual direct fitness around that mean, leading to increased variance in fitness. Although it may seem paradoxical that decreasing the number of breeders results in the same mean group fitness, singular breeding and reproductive skew within social groups are thought to arise due to competition among group mates for resources critical to reproduction (Johnstone, 2000
). If total reproduction by a group is resource-limited, partitioning fitness among one or many members of the same sex may not affect the number of young produced by the group, with the result that mean direct fitness will remain constant.
Second, increased variation in group size due to the variable presence of non-breeding helpers may affect patterns of reproductive success within each sex. If larger groups are able to monopolize disproportionately more resources, this may increase the among-group range of fitness values achieved (i.e., group augmentation: Kokko et al., 2001) and, in turn, the variance in direct fitness among members of each sex. These mechanisms are not mutually exclusive, but determining which affects patterns of direct fitness in singular-breeding species is beyond the scope of our current analysis. Instead, our goal is simply to determine whether the relative variance in reproductive success in singular breeding species differs predictably from that in other vertebrate societies.
Several lines of evidence suggest that, at least among mammals, the distinction between breeders and non-breeders is more extreme for females than males. First, behavioral observations and molecular genetic analyses indicate that, within singular-breeding groups of mammals, a smaller proportion of females produce offspring; although reproduction by "non-breeding" alloparents is not common, this phenomenon appears to be more prevalent among males (e.g., dwarf mongooses Helogale parvula: Keane et al., 1994; naked mole-rats: Reeve et al., 1990; common marmosets Callithrix jacchus Nievergelt et al., 2000). Second, the mechanisms used to suppress reproduction by alloparents tend to be more extreme among females, meaning that even within species, cessation of reproduction among females occurs earlier in the series of events leading to offspring production than it does among males (e.g., dwarf mongooses Helogale parvula: Creel et al., 1992; naked mole-rats: Bennet and Faulkes, 2000; common marmosets: Saltzman et al., 1997; Baker et al., 1999; but not in Damaraland mole-rats Cryptomys damarensis: Clarke et al., 2001). Finally, competition to become a breeder may be more severe among females, as evidenced by more overt and prolonged aggression among females when a breeding slot becomes available (e.g., eusocial mole-rats: Reeve, 1992; Clarke and Faulkes, 2001; marmosets: Lazaro-Perea et al., 2000).
Collectively, these observations led us to examine whether, in singular-breeding mammals, variance in reproductive success is greater among females than among males. The implications of this prediction for the relative intensity of sexual selection on females versus males in singular breeding societies are clear, yet we could find no prior discussion of this topic within the context of Bateman's Paradigm. At the same time, we wondered whether a similar tendency toward greater variance in female reproductive success would be evident among singular breeding birds. Singular breeding in both taxa is defined using the same behavioral criteria and the social structures of many singular-breeding avian groups suggest that females are more likely to be excluded from breeding than are helper males (Emlen and Wrege, 1992). Specifically, even though the sex ratio of alloparents in many singular-breeding avian species is male biased, alloparental males may, under some circumstances (e.g., establishment of a new breeding female) achieve some direct fitness by either mating with the single reproductive female in the group or mating outside the group (Rabenold et al., 1990; Mulder et al., 1994). In contrast, in the absence of conspecific brood parasitism (Yom-Tov et al., 2001), reproduction by females (irrespective of the sires of their progeny) is limited to egg-laying by the few individuals who achieve breeding status within social groups. As a result, in singular breeding birds, the proportion of animals that are socially excluded from breeding may be greater for females, leading to greater variance in direct fitness among members of this sex, despite the prevalence of male alloparents. Consequently, comparative studies of these taxa provide an important opportunity to assess the general (i.e., cross-taxon) importance of singular breeding as a determinant of relative variance in reproductive success and, potentially, intersexual differences in the intensity of sexual selection.
Testing hypotheses regarding singular breeding in the context of Bateman's Paradigm
Our contribution to this symposium examined intersexual differences in variance in reproductive success for singular breeding societies of vertebrates. Specifically, our goal was to determine whether singular breeding and the occurrence of non-breeding adults are associated with patterns of relative variance in reproductive success that differ from those predicted by Bateman's Paradigm. As the preceding discussion implies, relatively little attention has been paid to the potential impact of non-breeding alloparents on patterns of sexual selection in cooperatively breeding societies. To explore this issue quantitatively, we use species-level data drawn from the literature on cooperatively breeding birds and mammals to compare patterns of reproductive success across different breeding systems.
Building upon the above discussion of Bateman's gradients and their implications for sexual selection, we use standardized measures of the range of fitness values for same-sex individuals rather than formal estimates of variance in direct fitness to assess relative variability in male and female reproductive success (Clutton-Brock and Vincent, 1991; Emlen and Wrege, 2004). These analyses are used to test the hypotheses that (1) singular breeding is associated with greater relative variability in female reproductive success and (2) patterns of relative variability in reproductive success are similar for singular breeding mammals and birds. The implications of these data for patterns of sexual selection in singular breeding and other vertebrate societies are important in light of the reevaluation of Bateman's Paradigm that formed the basis for the symposium. We anticipate that comparisons of singular-breeding versus other vertebrate societies will yield significant new insights into Bateman's (1948) classic analyses of intersexual differences in mating success, variance in reproductive success, and the intensity of sexual selection.
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METHODS |
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Compilation of the data set
Data were obtained from published accounts of male and female reproductive success in birds and mammals. Because observations of mating behavior do not always provide reliable indicators of direct fitness (Hughes, 1998
; Snow and Parker, 1998; Avise, 2004), we focused on species for which molecular estimates of parentage and reproductive success were available. Moreover, only species for which we encountered data on individual reproductive success were considered; data on parentage were not sufficient if they did not include estimates of either the total number or the proportion of young produced per individual or per reproductive category (i.e., breeder versus non-breeder). We also included species in which non-molecular estimates of reproductive success were subsequently confirmed by genetic methods (e.g., monogamy of breeding pairs in Florida Scrubjays Aphelocoma coerulescens: Quinn et al., 1999) In an effort to be inclusive and unbiased in our compilation of data, we searched citation databases for papers on reproductive success and direct fitness in avian and mammalian species; given the disproportionate attention that behavioral biologists have paid to cooperatively breeding vertebrates, however, it is likely that singular breeders are better represented in our data set than are other vertebrate societies. Although we did not restrict the time frame over which reproductive data were collected, the vast majority of studies that we surveyed provided estimates of annual direct fitness only. As a result, this was the measure of fitness used in our comparisons of variation in male and female reproductive success.
Because we were interested in examining the effects of non-breeding individuals on the relative variability in male and female reproductive success, we divided the species in our data set into "singular breeders" and "others." Singular-breeding species were identified on the basis of the regular presence of non-breeding alloparents within groups of cooperatively breeding adults; species not exhibiting this characteristic were categorized as "other." Although the latter designation includes a potentially wide array of mating and social systems, this dichotomous classification scheme is appropriate given our emphasis on the effects of non-breeding adults on patterns of reproductive success. Intraspecific variation in the prevalence of non-breeding alloparents is characteristic for some of the species included in our sample (e.g., carrion crows: Baglione et al., 2002), which potentially complicated the assignment of taxa to the two categories of breeding system considered here. In these cases, we relied upon published descriptions of these species as singular or plural breeders (Brown, 1987; Solomon and French, 1997) to determine the placement of these species within our analyses. Whenever possible, we used data on breeding system and direct fitness obtained from the same population of conspecifics; given that most species in our data set have been the subjects of intensive research by specific groups of investigators, behavioral and genetic data were typically coincident.
Estimating relative variability in reproductive success
Published studies of reproductive success did not typically include the raw data necessary to calculate variance in direct fitness using standard statistical estimators (Zar, 1999). Given this analytical challenge and arguments regarding the greater utility of Bateman's gradients for estimating the intensity of sexual selection (Jones et al., 2000, 2002), we used data regarding the range of fitness values achieved by conspecifics of each sex to estimate the relative variability in direct fitness (RV) for females and males (Clutton-Brock and Vincent, 1991). For species in which all individuals reproduce (i.e., "others"), this was done by calculating the difference between the mean and maximum fitness values reported for females (Fig. 2a) and then dividing this number by the comparable statistic for males. For unimodally-distributed data (i.e., the distribution of direct fitness values expected for "other" societies), use of mean and maximum values should capture the range of direct fitness outcomes observed, since the minimum fitness value possible for an individual is zero. This approach does not incorporate the relative density of data points around the mean but, in the context of sexual selection, it is the extreme (maximum) values that are expected to be particularly important since they represent the phenotypes that are likely to be disproportionately under or over represented in future generations (Andersson, 1994).
For singular breeders, this estimator of RV will fail to capture the effect of multiple non-breeders if mean direct fitness for the group is unaffected by the number of alloparents. Consequently, for singular-breeding species, we used the expected bimodality in individual direct fitness to estimate the range of fitness values for members of each sex. Specifically, we calculated the ratio of the mean reproductive success for breeding and non-breeding females (Fig. 2b), and then divided this number by the comparable number for males. Because "non-breeders" in many species achieve a limited degree of direct fitness, this procedure resulted in finite (i.e., non-infinity) ratios for the reproductive success of breeders and non-breeders of the same sex.
For both singular-breeding and other societies, we generated relative estimates of variability in reproductive success, meaning that values for females were standardized by dividing by the comparable value for conspecific males. Consequently, the results of our analyses should not be biased by the somewhat different procedures used to estimate variability in reproductive success for singular breeders and "others." Nevertheless, as a check against this possibility, we also calculated RV for a subset of singular breeders using the procedure outlined above for "other" societies; reanalysis of relative variability in direct fitness was completed for the 4 singular breeding species for which appropriate data were available. Use of this second analytical approach produced no consistent differences in estimated values of RV (paired t(3) = 1.14, P = 0.338; n = 4 species). To further validate our measure of relative variability in direct fitness between the sexes, we calculated both RV and the standardized variance in reproductive success (I) for the subset of 6 species for which appropriate data on direct fitness were available. A Spearman rank correlation indicated a positive relationship between RV and I (rSpearman = 0.83; P = 0.06). Although sample sizes are small, these analyses imply that RV provides a reliable measure of the relative variability in individual direct fitness for males and females.
Because of the heterogeneity of the taxa and the data sources used in our analyses, we used conservative, two-tailed statistical tests to determine if observed values of RV for singular-breeding and other species differed from the expected value of 1.0 (equal variability in male and female reproductive success).
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RESULTS AND DISCUSSION |
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Relative variability in reproductive success versus breeding system
Data on individual direct fitness were obtained from six singular-breeding species of mammals representing three orders and four families (Appendix). Data from an additional six species representing five families and four orders were used in analyses of reproductive success in "other" mammalian societies. For singular-breeding birds, data were obtained from eight species representing six families and two orders (Appendix). For other avian societies, data were analyzed for 13 species representing eight families and six orders. Given the taxonomic diversity of our data set, we did not control statistically for phylogeny (e.g., pair-wise comparisons of sister-taxa or independent contrast analyses; Harvey and Pagel, 1991
) in our comparative analyses of reproductive success. Because singular-breeders were defined on the basis of the shared characteristic of non-breeding alloparents, analyses of these species were potentially more likely to be confounded by phylogenetic relationships than were analyses of other societies. Visual inspection of recent phylogenies for the species in our data set, however, revealed that these taxa represent a minimum of 11 evolutionary origins for singular breeding (mammals: n 5; birds: n 6; Cockburn, 1998; Bennett and Faulkes, 2000; Veron et al., 2004), indicating that our analyses were unlikely to have been influenced by recent shared ancestry among the singular breeders in our data set.
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Among mammals, the relative variability in female and male reproductive success (RV) differed markedly between singular-breeding and other species. Among singular breeders, our measure of variability in reproductive success was greater for females than for males (one-sample t(5) = 3.2, P < 0.019; with expectation of 1.0; Fig. 3). In contrast, among the other mammalian societies examined, variability in direct fitness was greater among males (one-sample t(5) = –4.7, P = 0.0056; Fig. 3). The mean RV value for singular breeders was significantly greater than the mean for the other mammalian species included in our data set (unpaired two-sample t(11) = 5.8, P < 0.001). Thus, our data support the prediction that, in singular-breeding mammal species, variability in direct fitness is greater for females.
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A similar pattern was evident among the avian species included in our analyses. As in mammals, the RV for singular breeding birds indicated that variability in reproductive success was greater among females (one-sample t(7) = 2.1, P = 0.078; with expectation of 1.0; Fig. 3), while the RV for other avian taxa indicated that variability in fitness was greater among males (one-sample t(12) = –3.8, P = 0.0026; Fig. 3). The mean RV value for singular breeders was significantly greater than that for the other avian species in our analyses (unpaired two-sample t(19) = 3.9, P = 0.0010). The difference in RV between singular-breeding and other birds appeared to be less pronounced than the comparable difference between mammalian societies (Fig. 3); this interaction between taxa and breeding systems was significant (F(1,30) = 9.1, P = 0.0051), indicating that the magnitude of the apparent effect of singular breeding on RV varies between birds and mammals.
These findings are striking, particularly given the diverse array of mammals and birds included in our analyses. The species listed in the Appendix represent considerable phylogenetic, behavioral, and life history variation, suggesting that patterns of reproductive success are likely to be influenced by numerous factors in addition to the presence of non-breeding alloparents. We had expected that these other sources of variation would tend to obscure the predicted relationship between breeding structure (singular versus other) and RV. That we found a significant relationship between singular breeding and RV despite these sources of variation suggests that breeding structure—in particular the presence of non-breeding alloparents—has a profound influence on patterns of relative direct fitness in birds and mammals.
Singular breeding vertebrates and Bateman's Paradigm
Our analyses of reproductive success in singular-breeding and other vertebrate societies appear to contradict Bateman's (1948) findings regarding relative patterns of reproductive success in males versus females. In particular, the greater variability in direct fitness for females in singular breeding birds and mammals seems to counter Bateman's (1948) data indicating that reproductive success varies more widely among males. Several factors may have contributed to this outcome. For example, differences in RV between singular and other breeders may reflect biases in estimates of the proportion of individuals in a population that achieve little or no reproductive success (e.g., dispersers, floaters, parasites, or individuals whose [undetected] reproductive attempts failed) (Hauber and Dearborn, 2003). At the same time, assigning genetic parentage to individuals that were not themselves genetically sampled is challenging (Mennil et al., 2003) and may result in underestimation of the number of individuals that fail to reproduce. For these factors to have significantly impacted our findings, however, underestimation of non-breeding would have to have been consistently greater for males in singular breeding societies to bias our results in the predicted direction; given the diverse social, demographic, and dispersal patterns of the species examined, this seems unlikely.
A related issue is the appropriateness of measures of reproductive success based solely upon direct fitness. It is possible that, in social vertebrates, measures of direct fitness are misleading when trying to evaluate the relative variance in reproductive success between females and males. Specifically, intersexual differences in direct fitness may not parallel sex-specific patterns of inclusive fitness (Creel, 1990), with the result that RV provides a biased picture of the actual variation in fitness upon which sexual selection can act. This situation would represent a confound when intrasexual relatedness among group members is greater for females than for males, such that relative variability in inclusive fitness is reduced among members of the former sex. This problem seems most likely to arise during analyses of reproductive success in mammals, given their typically female-biased patterns of natal dispersal and associated tendency to form primarily female kin groups (Greenwood, 1980; Dobson, 1982). Although we cannot exclude this possibility, the regular presence of unrelated female group mates in at least some singular breeding societies (e.g., meerkats Suricata suricatta Clutton-Brock et al., 2000; superb fairy wrens Malurus cyaneus: Dunn et al., 1995; white-browed scrub wrens Sericornis frontalis: Wittingham et al., 1997) suggests that direct fitness benefits are important (Clutton-Brock, 2002) and, thus, represent a relevant measure of the potential for sexual selection in these species.
Assuming that direct fitness is an appropriate measure of the potential for sexual selection in singular-breeding societies, determining whether our findings represent a modification versus a refutation of Bateman's Paradigm depends upon the reasons for greater variability in female reproductive success. Although sex role reversal, in the context of greater parental effort by males than females, is increasingly recognized as an apparent contradiction to this paradigm (Emlen and Wrege, 2004), this explanation does not appear to apply our analyses. In species that exhibit sex role reversal, the fundamental relationship between number of mates and direct fitness is reversed, such that female reproductive success increases more rapidly as a function of number of reproductive partners (Jones et al., 2000). While studies of vertebrate cooperative breeders have not typically explored this issue quantitatively, the singular breeding species in our analyses do not exhibit other behavioral and phenotypic correlates of sex role reversal such as predominately male parental care or greater elaboration of female traits associated with mate attraction, we are led to conclude that sex role reversal does not explain the contrasting patterns of variability in reproductive success for singular-breeding and other societies of vertebrates.
Instead, we suggest that the greater variability in female reproductive success in singular-breeding societies reflects a specialized case of Bateman's Paradigm in which social suppression of reproduction increases the range of direct fitness values achieved by same-sex conspecifics. Several factors may favor greater suppression of reproduction among females. On a mechanistic level, reproduction by same-sex conspecifics may be easier to detect and, hence, to suppress among females (Vehrencamp, 2000; Williams, 2004). Among mammals, sexual activity is often more temporally restricted and more behaviorally or physiologically conspicuous for females (e.g., Faulkes et al., 1990; Saltzman et al., 1996), both of which may facilitate the disruption of reproduction by same-sex competitors. Among birds, the external deposition of large, conspicuous zygotes may facilitate egg removal by females as a means of reducing the reproductive success of same-sex group mates (e.g., Macedo et al., 2001).
At a functional level, the presumably larger per capita cost of offspring production for females may favor greater competition among members of this sex when the resources required for reproduction become limited. This argument derives from the fundamental dichotomy in gamete size that is characteristic of anisogamous species; because the per capita cost of egg production is high relative to that for sperm (Trivers, 1972; but see Tang-Martinez, 2000), the slope of the relationship between per-offspring cost of reproduction and number of offspring produced should be steeper for females. This relationship may be further exaggerated in mammals and birds due to the costs, respectively, of internal gestation or the production of calcified eggs (Vaanraji, 1995; Vezina and Williams, 2002). As a result, limitations on the resources required for reproduction should have a greater impact on the number offspring that a female can produce, which may lead to more severe competition among members of this sex for those resources that are available. This argument is built upon the same fundamental asymmetries in gamete size that underlie Bateman's (1948) work and, hence, increased competition among females in singular-breeding societies should be viewed as a modification, rather than a refutation, of Bateman's Paradigm. More generally, ecological or social conditions may interact with the general relationships identified by Bateman to generate variable patterns of relative reproductive success for females and males.
Comparisons of birds and mammals
Although variability in reproductive success was greater among females in both singular breeding birds and mammals, our analyses revealed that this effect was more pronounced among mammals. One factor that may have contributed to this taxonomic difference is the distinct pattern of natal dispersal in birds versus mammals. Natal dispersal in mammals is typically male biased, with the result that kinship and social structure are often more pronounced among females (Dobson, 1982). In contrast, natal dispersal in birds is generally female-biased, such that singular breeding groups are composed primarily of males (Liberg and von Schantz, 1985; Brown, 1987). Consequently, while reproductive competition among mammalian females is most likely to occur within social groups, reproductive competition among avian females may be more common among individuals vying for access to the same group. Although both contexts may result in the competitive exclusion of individuals from breeding status, the extent of this bias may be less severe among birds if turnover of breeding animals is more frequent among versus within social groups (Daniels and Walters, 2000). Interestingly, the only singular breeding bird in our data set for which RV was <1.0 was the Seychelles Warbler (Acrocephalus sechellensis); unlike the other avian species considered here, alloparental Seychelles Warblers are typically females (Komdeur et al., 1997), suggesting that competition for access to breeding groups may be more extreme among males. Thus, fundamental differences in mammalian versus avian life histories and reproductive strategies may contribute to the smaller difference between RV values for singular and other species of birds. Indeed, given the number of factors that may differentially influence patterns of reproductive success in birds versus mammals, our finding that sexual differences in RV are similar for both taxa (Fig. 3) suggests that the presence of non-breeding alloparents is an important determinant of the variability in reproductive success.
Implications for sexual selection
Bateman's (1948) work has substantially impacted our understanding of sexual selection (this volume). In particular, his analyses of the relationship between number of mates and individual direct fitness continue to provide a quantitative rationale for the widely accepted assertion that sexual selection is more intense among males (Jones et al., 2002). As a corollary, Bateman (1948) suggested that intersexual differences in the variance in reproductive success could be used as indicators of the relative intensity of sexual selection. We have argued here that estimates of the relative variability in direct fitness provide a potentially more relevant, general indicator of the strength of sexual selection, since it is the extremes of individual direct fitness that are expected to be most subject to selection (Clutton-Brock and Vincent, 1991). Given this argument, what do our findings regarding greater variability in direct fitness for females in singular breeding birds and mammals suggest about the relative intensity of sexual selection in these species?
If variability in reproductive success provides a meaningful measure of the phenotypic extremes upon which selection can act, then we would expect the intensity of sexual selection to be greater in the sex that exhibits greater variability in direct fitness. To the best of our knowledge, no other comparative studies have been conducted that examine quantitatively the intensity of sexual selection acting on females and males in singular breeding birds and mammals. Based upon our analyses, the few data that are available suggest that sexual selection may be particularly intense among females in some species of singular breeding mammals. Sexual dimorphism in body size is frequently interpreted as evidence of sexual selection, particularly in species in which members of the larger sex compete through direct, physical aggression. In some singular breeders (e.g., naked mole-rats, Reeve, 1992: African wild dogs Lycaon pictus, Girman et al., 1997), reproductive females tend to be larger than their male conspecifics, providing potential circumstantial evidence of enhanced sexual selection among females in these species. At the same time, more extreme, elaborate, or effective mechanisms of reproductive suppression among females (common marmosets: Saltzman et al., 1996) may be interpreted as evidence of greater strength of sexual selection (Williams, 1966). Thus, although direct estimates of the relative intensity of sexual selection are required for singular breeding species, both conceptual arguments and empirical evidence suggest that the greater variability in direct fitness for females in these species may be associated with enhanced sexual selection.
Future directions
Our results imply greater strength of sexual selection among females in cooperatively breeding vertebrate societies characterized by non-breeding alloparents. This finding should be considered preliminary, given the limited number of species for which data were available. In addition to increasing the number and phylogenetic diversity (e.g., cooperatively breeding fish: Brouwer et al., 2005; amphibians: Jones et al., 2002) of taxa examined, future treatments of this problem should include more explicit comparisons of (1) closely related species that differ with regard to social system, as well as (2) demographically and ecologically distinct species. Collectively, these analyses can be used to determine more exactly the role that singular breeding plays in shaping relative patterns of male and female direct fitness. At the same time, the relative intensity of sexual selection acting on members of singular-breeding and other societies should be examined directly, rather than estimated from data on variability in direct fitness. Despite the limitations of the current data set, our findings are intriguing and we hope that our exploration of singular-breeding societies within the context of Bateman's paradigm will stimulate further studies of the role that breeding and social systems play in shaping intersexual differences in reproductive success and sexual selection in natural populations of animals.
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ACKNOWLEDGMENTS |
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We thank Zuleyma Tang-Martinez for inviting us to participate in the Bateman Symposium. Financial support for the symposium was provided by the National Science Foundation and SICB. Our research has been funded by grants from the National Science Foundation, NIH: National Institute for Aging, UC Berkeley, the Miller Institute for Basic Research in Science, the Marsden Fund, and the University of Auckland Research Council. This project has benefited from discussions with many colleagues, including the participants of the Bateman symposium and D. Dearborn, J. Dickinson, J. Mateo, P. Sherman, B. Strausberger, A. Suarez, Z. Tang-Martinez, M. Webster, and B. Wolfenden.
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FOOTNOTES |
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1 From the NSF-sponsored Symposium Bateman's Principle: Is It Time for a Re-evaluation? presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5–9 January 2004, at New Orleans, Louisiana, and supported by NSF.
2 E-mail: m.hauber{at}auckland.ac.nz
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SYNOPSISINTRODUCTIONMETHODSRESULTS AND DISCUSSIONReferences |
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