Behavioral Ecology Advance Access originally published online on January 18, 2008
Behavioral Ecology 2008 19(2):456-461; doi:10.1093/beheco/arm150
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Testing the sexy son hypothesis—a research framework for empirical approaches
Institute of Avian Research "Vogelwarte Helgoland," An der Vogelwarte 21, D-26386 Wilhelmshaven, Germany
Address correspondence to T. Huk, who is now at Department of Business Administration, Economics, and Social Sciences, Technische Universität Braunschweig, Rebenring 58A, D-38106 Braunschweig, Germany. E-mail: t.huk{at}tu-braunschweig.de.
Received 21 March 2007; revised 30 November 2007; accepted 3 December 2007.
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INTRODUCTION |
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 TOP INTRODUCTION SSH: CRITICAL AND COMPATIBLE...SSH IN POLYGYNOUS MATING...REVIEW OF EMPIRICAL STUDIESCONCLUSIONSREFERENCES |
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Sexual selection by direct and/or indirect benefits as well as sexual conflict determines the evolution of animal mating systems (e.g., Andersson and Simmons 2006
). In polygynous mating systems, the female preference of apparently useless or deleterious male characteristics can be understood if a correlation between preferred male characteristics and direct benefits for the female exists (see polygyny threshold model, e.g., Orians 1969), such as improved paternal care or territorial quality (e.g., Price et al. 1993; Iwasa and Pomiankowski 1999). This issue is particularly interesting in facultative polygynous mating systems with biparental care because the female's choice of a polygynous male as a mate is most often accompanied by a reduction in paternal care by this mate (for a review, see Ligon 1999). Several studies (e.g., Johnson et al. 1994; Pribil and Searcy 2001; Moreno et al. 2002; but see Both 2002) have observed a reduction in offspring number and/or offspring performance in females mated with a polygynous male, thus raising doubt in the relevancy of the polygyny threshold model (see, e.g., Orians 1969) in these instances. More generally, females of most species do not seem to take any appreciable direct benefits of their mate choice (Kirkpatrick and Ryan 1991; Andersson 1994).
Since the 1970s, indirect benefits are discussed as a possibility to explain female choice (Kirkpatrick and Ryan 1991; Andersson and Simmons 2006). Weatherhead and Robertson (1979) proposed the sexy son hypothesis (SSH) as an additional explanation for the establishment of polygyny. According to this hypothesis, females are assumed to compensate for their direct inferior breeding success by the increased number of descendents produced by their sexy—and therefore polygynous—sons (see Table 1). The idea of focusing on fitness advantages as a result of male attractiveness is similar to the "Fisherian runaway selection process" (see, e.g., Andersson and Simmons 2006). The "good genes" model (see Table 1), that is, the idea of an indirect benefit due to the male's genetic quality, is a second, complementary hypothesis that is discussed as a possibility to explain female choice by indirect benefits (Andersson and Simmons 2006; Charmantier and Sheldon 2006). Both hypothesized mechanisms, SSH and good genes, belong to the same continuum of indirect selection (Kokko et al. 2002; Radwan 2002). SSH as well as good genes postulate that indirect benefits due to male characteristics in a specific species will be similar for all females of this species (see also Table 1). Compatible genes, on the other hand, try to explain intraspecific differences in female mate choice (see Table 1). According to this theory, each individual female tries to enhance its fitness by choosing a male with a genetic pattern that is compatible with its own genetic configuration (e.g., Neff and Pitcher 2005).
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Another approach to understand mating behavior that results in deleterious female reproductive success, such as offspring number or performance, is the idea of sexual conflict (see Table 1; Gavrilets et al. 2001
; Cameron et al. 2003; Arnqvist and Rowe 2005; Andersson and Simmons 2006; Lessells 2006; Parker 2006; Rice et al. 2006). Sexual conflict is driven by the opposed reproductive interests in females and males that result in sexually antagonistic behavior and coevolving adaptations. Whereas the traditional hypotheses of sexual selection, such as the polygyny threshold model and SSH, discuss the importance of direct versus indirect benefits, sexual conflict considers the possibility that polygynous males are not beneficial to females, neither directly nor indirectly. For example, Arnqvist and Kirkpatrick (2005) demonstrated that extrapair copulations, which do not lead to any direct advantages such as additional food resources or shelter, in socially monogamous birds are in line with sexual conflict assumptions as indirect benefits are much smaller than the direct negative selection caused by depressed paternal investment by social males.
The present study will focus on SSH because SSH as well as the good genes assumption are based on the relative magnitude of direct and indirect effects of mate choice and thus have become relevant to the recent debate of whether sexual conflict can result in sexually antagonistic selection. SSH developed by Weatherhead and Robertson (1979), further called "narrow-sense SSH," refers to mating systems with biparental care. In these mating systems, females mated with a polygynous male normally receive less assistance than females mated with a monogamous male (see, e.g., Ligon 1999) and thus suffer from direct fitness consequences that have to be (over)compensated by their sexy sons. On the other hand, "broad-sense SSH" encompasses polygyny and promiscuous mating systems with and without biparental care. Alatalo (1998) argues that the costs of any additional choice may be so minor that female choice for honestly signaling males, that is good genes, may evolve even if the indirect benefits on offspring quality are small. A similar argument can be given for SSH if mates of attractive males do not suffer any direct fitness consequences.
Since it was first proposed by Weatherhead and Robertson (1979), SSH has been discussed vividly. Several theoretical studies either support (Weatherhead 1994; Kokko et al. 2002; McNamara et al. 2003) or attempt to argue against SSH (e.g., Kirkpatrick 1985; Wagner 1994; Alatalo and Ratti 1995). Recent sophisticated empirical studies dealing with SSH have reached contrasting results (compare Gwinner and Schwabl 2005; Head et al. 2005; Orteiza et al. 2005; Gustafsson and Qvarnström 2006; Huk and Winkel 2006). However, these studies differ in terms of the explicit research questions they ask and thus highlight the importance of questioning precisely what factors should be measured. The aim of the present paper is to shed light on the contrasting empirical results by analyzing the appropriateness of various research questions in empirical tests of SSH and in so doing to differentiate between "critical predictions" and "compatible predictions" (see Table 2). Critical predictions should be studied in future work as they address topics that are at the core of the predictions of SSH. Critical predictions are therefore able to validate or invalidate SSH as a hypothesis explaining female choice. Compatible predictions are aspects that can be discussed in the light of this hypothesis without directly addressing the critical predictions. Thus, compatible predictions only test for "by-product" predictions that can neither validate nor invalidate SSH.
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SSH: CRITICAL AND COMPATIBLE PREDICTIONS |
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TOPINTRODUCTIONSSH: CRITICAL AND COMPATIBLE...SSH IN POLYGYNOUS MATING...REVIEW OF EMPIRICAL STUDIESCONCLUSIONSREFERENCES |
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A major reason for the different conclusions reached by empirical studies dealing with SSH is that they differ both in terms of the variables investigated and of the different treatment factors compared. How best to test SSH empirically? The major emerging critical prediction is that indirect effects, that is, genes delivered by the male, do increase lifetime reproductive success in sons. Therefore, females of attractive males, which in narrow-sense SSH suffer from inferior direct fitness estimates, in the long run achieve the same fitness as females mated with a monogamous male (Weatherhead and Robertson 1979
). This prediction, however, occurs also in the good genes hypothesis (see Andersson and Simmons 2006; Charmantier and Sheldon 2006). According to SSH, it is their sexy sons who are assumed to be responsible for this compensation as they inherit their father's genes which in turn enable them to become polygynous themselves, thus increasing the number of grandchildren produced. SSH therefore predicts that females mated with a polygynous male rear sons that become polygynous themselves. More specifically, the number of polygynous breeding attempts should be higher in sons descending from females mated with a polygamous male than in sons descending from females mated with a monogamous male. Investigation of this prediction would clarify whether the underlying assumption of SSH, that is heritability of attractiveness, is valid. This would be, however, no direct evidence for the compensation of any direct inferior fitness consequences. To test SSH, the aforementioned second critical prediction must also be investigated, that is, a fitness (over)compensation with respect to the number of F1+x descendents.
SSH as well as the good genes hypothesis predict that the number of grand-offspring is similar or higher in females mated with a polygynous male than in females mated with a monogamous male. Whereas a greater number of grand-offspring would be in line with SSH, a lower number would be an argument against this hypothesis. In case of a similar reproductive success, it is rather difficult to distinguish between 1) instances that observed no significant differences in fitness due to the fact that there really were no differences—as proposed by SSH—and 2) empirical studies that failed to detect a difference in the number of grandchildren, although females mated with a polygynous male in fact could not compensate direct inferior reproductive success. In long-lived species with several subsequent breeding events, another important parameter is the consequence of mating behavior for any further breeding success in the future, that is, the risk to suffer from sexually transmitted diseases especially in females mating with polygynous males (see Thrall et al. 2000). SSH studies on long-lived species, therefore, have to investigate not only the number of grandchildren of the actual breeding event but also possible subsequent differences in female longevity or offspring performance in any further breeding attempts (for the possibility of an increase in longevity in polygynously mated females, see also Garamszegi et al. 2004).
However, only few empirical studies have to date focused on these critical predictions. In particular, lifetime reproductive success, measured in terms of the number of grand-offspring produced, has rarely been investigated (see Hunt et al. 2004).
In addition to these critical predictions, further research predictions that encompass the theoretical concept of SSH can be made. These compatible predictions deal with topics that rely on the validity of the critical predictions mentioned above. Females have to be able to detect males that will pass on genes that increase the probability of rearing sons that will become polygynous during their own reproductive phase. Various studies demonstrate that females are able to detect "attractive" males by secondary sexual characteristics such as ornamentation (e.g., Gustafsson et al. 1995; Sheldon et al. 1999; Siitari et al. 2002). As a second compatible prediction, one should expect that females trade mate choice between male attractiveness and pairing status in species with biparental care as pairing status is an indicator of male assistance in these species. Third, if a female mated with a polygynous male rears sexy sons that are able to compensate any direct inferior reproductive success, one might argue that such females could be expected to shift their brood sex ratio toward producing more males than females (Burley 1981). Similarly, one should expect that sons of polygynous (thus attractive) males should exhibit behavior that increases their probability to become polygynous themselves.
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SSH IN POLYGYNOUS MATING SYSTEMS WITH BIPARENTAL CARE |
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TOPINTRODUCTIONSSH: CRITICAL AND COMPATIBLE...SSH IN POLYGYNOUS MATING...REVIEW OF EMPIRICAL STUDIESCONCLUSIONSREFERENCES |
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Especially interesting are female decision opportunities in species with short-term pair-bond, that is, species in which females and males choose their partner at the beginning of the actual reproduction period, in which fitness is mainly attributed to habitat quality, male assistance during the rearing of offspring, and heritable male attractiveness. For convenience, a facultative bigynous mating system is assumed to make female mate choice decisions more explicit. At the beginning of the reproduction period, all males are unmated. Females should therefore select males on the basis of habitat quality and attractiveness; they should primarily select attractive males occupying a superior habitat in order to increase their reproductive success. In the subsequent breeding season, unpaired females have ideally to decide whether 1) to mate with these superior (but already mated) males, thus becoming a secondary female sharing their male with the already existing primary female, or to mate with a still unmated male that is either 2) less attractive or 3) one which occupies a territory of lower quality (but see, e.g., Searcy and Yasukawa 1989
for alternative no-compensation models). In the latter case, these females do not have to share their monogamous mate. In order to test SSH, only females of the categories 1) and 2) should be compared with test SSH. A comparison between 1) and 3), on the other hand, is not appropriate for testing SSH as fitness differences are due to differences in territorial differences. A good system may be, therefore, a facultative polygynous species that does not defend feeding territories, thus making territorial differences less important.
When testing SSH, it is important to analyze the reason for a mate choice decision in favor of a polygamous male. Is the choice based on the attractiveness of the male or is it based on the quality of the male's territory? It should be stressed that in the case of a positive correlation between territorial quality and male attractiveness, it is quite difficult to investigate SSH as it is not possible to distinguish fitness consequences between these 2 confounding factors in the field, that is territorial quality and male attractiveness. In this case, only experimental approaches can solve this problem by controlling territorial quality in the laboratory or by cross fostering of whole or partial broods (see, e.g., Hadfield et al. 2006). If habitat quality and male attractiveness are independent, that is, female choice in the sense of runaway selection, females should select an already mated male for 2 reasons: the already mated male occupies a superior habitat or is more attractive than the unpaired male. As one cannot rule out in most cases that territorial quality and male attractiveness are at least partially correlated, studies focusing on SSH experimental approaches, for example, cross fostering of whole or partial broods between females with different mating status and in territories of different quality, have to be preferred over correlational studies as they allow to break down correlations between territorial quality and male attractiveness.
As regards female perspective in mate choice, 3 categories can, therefore, be distinguished for females breeding in territories of similar quality: females mated with a monogamous male, primary females, and secondary females. As primary females, as a rule, receive more male assistance (Ligon 1999), their direct reproductive success is less affected than that of secondary females. Primary females therefore combine a pattern of relatively high direct male assistance with the supposed indirect benefits due to the genetic constitution of their attractive males (however, it is important not to consider primary females mated with a less attractive male occupying a superior habitat, see above). According to this combination, a comparison of primary females and females mated with a monogamous male should exhibit not only more polygynous sons in primary females but also a significantly higher number of grand-offspring as differences in direct reproductive success should be of minor importance.
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REVIEW OF EMPIRICAL STUDIES |
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TOPINTRODUCTIONSSH: CRITICAL AND COMPATIBLE...SSH IN POLYGYNOUS MATING...REVIEW OF EMPIRICAL STUDIESCONCLUSIONSREFERENCES |
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What have we learned from existing empirical studies? Different empirical studies demonstrated that female mating decisions may be explained by the good genes model of sexual selection. It was demonstrated that attractive males confer disease resistance to their offspring (Barber et al. 2001
) or increase offspring viability (Hasselquist 1998; Byers and Waits 2006; Forsman and Hagman 2006). Whereas good genes may support fitness of sons and/or daughters, SSH predicts fitness advantages in sons only. According to Alatalo and Lundberg (1986), SSH should not apply in the model species Ficedula hypoleuca due to poor phenotypic quality of nestlings of secondary females. In their study, they supported their assumption by estimation of lifetime reproductive success. Contrary, Johnson et al. (1994) concluded that secondary females in the house wren (Troglodytes aedon) may recoup fitness losses in the next generation if male mating success is at least moderately heritable. However, both studies did not measure critical predictions of SSH directly. A review of empirical studies revealed that compatible predictions of SSH were investigated by a rather large variety of studies. The majority of these studies have not been intended to look especially at SSH because compatible predictions of SSH do play a role in other theoretical concepts as well. Although each compatible prediction was supported by empirical results, the pattern is not unequivocal because several studies observed pattern that contradict compatible SSH predictions (see Table 2).
Empirical studies dealing with critical predictions of SSH are rare. These empirical approaches used either birds or insects as model species, whereas studies on other taxa are missing (see, e.g., Barbosa and Magurran 2006). Two correlational studies in the closely related collared flycatcher (Ficedula albicollis) and pied flycatcher (F. hypoleuca) revealed no support for narrow-sense SSH, that is, no compensation of inferior reproductive success via sexy sons (see Table 2; Gustafsson and Qvarnström 2006; Huk and Winkel 2006). However, in the pied flycatcher, this result held true for secondary females, whereas in primary females, that is, females with a relatively weak inferior direct reproductive success, the pattern was compatible with SSH (see Table 2). Recent studies, however, that did not look at the number of grand-offspring came to contrasting results (Both 2002; Garamszegi et al. 2004).
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CONCLUSIONS |
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TOPINTRODUCTIONSSH: CRITICAL AND COMPATIBLE...SSH IN POLYGYNOUS MATING...REVIEW OF EMPIRICAL STUDIESCONCLUSIONSREFERENCES |
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To sum up, it can be concluded that empirical studies dealing with critical predictions to date only partially support SSH; that is, only studies with rather small direct fitness consequences are compatible with critical SSH predictions. Contrary, the demonstration of compensation of considerable lower direct reproductive success via a heritable genetic effect of male attractiveness, and hence male mating status in sons, is not demonstrated until now. Thus, facultative polygyny in biparental species seems to be best explained by sexual conflict. Approaches derived from quantitative genetic models of mate choice came to similar results (Kirkpatrick and Barton 1997
; Charmantier and Sheldon 2006; Hadfield et al. 2006; Qvarnström et al. 2006). Recent studies therefore support the position that inferior direct reproductive success cannot be overcompensated by a "sexy son" effect (e.g., Kirkpatrick 1985). Thus, attractiveness of sexy sons and its resulting fitness advantages seem to be of minor biological effect.
The deception hypothesis, that is, the assumption that males hide their mating status and deceive females into polygyny in polyterritorial species (Alatalo et al. 1982; Temrin and Arak 1989; Ligon 1999), is an alternative no-compensation explanation that fits into sexual conflict assumptions. Slagsvold and Dale (1994) found little support for deception hypothesis while observing pied flycatcher behavior. They instead suggest that female pied flycatchers are able to detect male mating status but sometimes settle with mated males because of cost of searching thus doing "the best of a bad job."
The impact of extrapair copulations for female choice decisions in the light of SSH has already been discussed by Wagner (1994) and Weatherhead (1984). As extrapair copulations allow females to benefit from "sexy genes" of attractive males even if they are not the primary or secondary female, differences between females mated with a monogamous male and primary or secondary females can be assumed to be mitigated. Thus, differences in territorial quality will become more important in these cases, highlighting the importance of comparing only females breeding in habitats of similar quality. A more precise approach would be to genetically detect male paternity (see Andersson and Simmons 2006).
As empirical studies focusing on critical SSH predictions are rare, future research is needed: ideally, the comparison of future fitness consequences between females that choose to be secondary females with the success they would have had if they had been paired with a monogamous male. As this is principally not possible, future research should therefore focus on a comparison of total fitness, that is, number of grand-offspring, between females mated with a monogamous male and primary females as well as between females mated with a monogamous male and secondary females while controlling for possible confounding variables such as timing of reproduction, habitat quality, and frequency of interactions with males. This total fitness measure should also incorporate female and offspring survival. Furthermore, these studies should use genetic proof of paternity as social matings are generally only rather poor measures of the numbers of offspring produced (e.g., Griffith et al. 2002). A fruitful avenue would be experimental approaches such as cross fostering of whole or partial broods (see, e.g., Hadfield et al. 2006) between females with different mating status.
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ACKNOWLEDGEMENTS |
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We thank Ben Sheldon as well as anonymous referees for valuable comments.
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