Behavioral Ecology Advance Access published October 5, 2010

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1 Behavioral Ecology Advance Access published October 5, 2010 Behavioral Ecology doi: /beheco/arq156 Forum: Ideas Behavioral consistency and the resolution of sexual conflict over parental investment Nick J. Royle, Wiebke Schuett, and Sasha R.X. Dall Centre for Ecology and Conservation, Biosciences, College of Life and Environmental Sciences, University of Exeter, Cornwall Campus, Penryn, Cornwall, TR10 9EZ, UK Behavioral plasticity or flexibility is expected to be a key determinant of reproductive success because natural selection should favor individuals that adjust their investment in reproduction in response to variability in their environment, their own state, or other factors, such as the behavior or condition of their partner (Roff 2002). There is, however, increasing evidence for inflexibility of behavior, that is, consistent individual differences in behavior across contexts, in nonhuman animals (e.g., Dall et al. 2004; Sih, Bell, and Johnson 2004; Sih, Bell, Johnson, and Ziemba 2004; Dingemanse and Réale 2005; Smith and Blumstein 2008). It has recently been suggested that these consistent individual differences in behavior may be advantageous because they contribute to consistent individual differences in productivity (Biro and Stamps 2008), there are benefits to specialization (e.g., individuals benefit from adjusting their behavior to expected future fitness returns; Wolf et al. 2007), or there are social benefits of predictability (e.g., Dall et al. 2004; McNamara et al. 2009). However, flexibility might be expected to be more important than inflexibility for organisms that provide costly parental care because there are often conflicts over patterns of investment between the sexes (Hartley and Royle 2007), the resolution of which requires each parent to respond to the behavior of the other (Parker et al. 2002), especially in species with biparental care. Although rare compared with other forms of care across the animal kingdom, biparental care is common among birds, some families of fishes (e.g., cichlids), primates, and some subfamilies of insects (e.g., burying beetles) (Clutton-Brock 1991). Costs of reproduction mean that there are conflicts of interest between collaborating parents over the provision of parental investment (PI) (Parker et al. 2002). Consequently, the response of an individual to such sexual conflict should be closely tied to the behavior of its partner in biparental species (Wright and Cuthill 1990), for example, if the male reduces his investment, then the female may adjust hers in response. As a result, levels of PI provided to the current brood, and therefore offspring fitness, may be reduced (Royle et al. 2002). The outcome of the conflict, and therefore the relative investment provided by males and females to their offspring, is dependent on the form of the provisioning rules used by the parents (Parker et al. 2002). Negotiation models, based on flexible negotiation of effort in real time, predict high responsiveness of individuals to a change in effort by their partners (e.g., McNamara et al. 1999; Johnstone and Hinde 2006). Sealed bid models, on the other hand, assume that individuals should be insensitive to changes in effort by their partner (e.g., Parker 1985). Here, individuals commit to a certain level of care at the outset that is independent of partner effort, although it may be modified by variation in environmental resource availability or brood Ó The Author Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please journals.permissions@oxfordjournals.org size (Schwagmeyer and Mock 2003). The process by which selection maintains biparental care, despite underlying conflicts over the provision of costly care, is therefore determined by how parents respond to changes in each other s effort. There is considerable empirical evidence for both flexibility of effort (negotiation) and inflexibility (sealed bids) (reviewed in Sanz et al. 2000; Schwagmeyer and Mock 2003; Harrison et al. 2009). Why is there such variation in the flexibility of provisioning behavior in species with biparental care? The key to answering this question, and therefore how sexual conflict is resolved, may depend on the reliability of indicators of male parental ability and/or quality (and, conversely, female parental ability and/or quality). If offspring fitness is strongly dependent on male PI and males vary in their parental contributions (e.g., Wright and Cuthill 1990; Royle et al. 2006), then selection is expected to favor a degree of female choice for male provisioning behavior (Schwagmeyer and Mock 2003). At the time of pairing, males have no offspring with which to demonstrate their parental skills, so females must use indirect yet reliable and predictable indicator traits to assess the potential of their mates (e.g., Buchanan and Catchpole 2000; Candolin 2000). One potentially reliable indicator of male ability is his personality or behavioral phenotype (Figure 1). Individuals often behave in a consistent manner in different contexts (e.g., foraging and mating behaviors) that are analogous to personality traits (Bell 2007). More specifically, personality variation can be characterized by 2 related components: Individuals differ in the level of their behavioral expression (interindividual variation or behavioral type, e.g., some individuals may be more aggressive than others), and second, individuals will differ in the consistency of the expression of their behavior over time, contexts, and/or situations (sensu Sih, Bell, and Johnson 2004; Dingemanse et al. 2010; intraindividual variation or behavioral consistency; see Figure 1 for further details). In the context of parental care, individuals may, for example, differ in the amount of PI they provide (e.g., the total number of feeds provided to offspring over the whole nestling period; behavioral type) and the consistency with which that PI is provided over time (e.g., variation in the number of feeds provided on consecutive days). Individuals that show consistent effort in the context of provisioning behavior, for example, may also be consistent in other contexts (e.g., effort during courtship). Thus, behavioral consistency can also imply a strong correlation between behavior during parenting and courtship (Sih and Bell 2008). BEHAVIORAL CONSISTENCY OF INDIVIDUALS A SIGNAL OF COMMITMENT? Credible promises and threats Behavioral consistency may provide social benefits to individuals (McNamara and Houston 2002; Dall et al. 2004; McNamara et al. 2009). For example, in the context of parental care, a promise to cooperate can stimulate a partner to cooperate if the promise is reliable (Dall et al. 2004). Conversely, an individual may threaten to desert a brood, which may force their partner to respond by increasing their relative investment if the threat is reliably based on the body condition of the

2 2 Behavioral Ecology Figure 1 Characteristics of personality (adapted from Schuett et al. 2010). Animal personality (also known as coping style or temperament) is defined by 2 main characteristics: Individuals differ in the level of their behavioral expression (inter-individual variation) and second, at least some individuals must be consistent in their behavior over time, contexts, and/or situations (sensu Sih, Bell, and Johnson 2004; intraindividual consistency). This can be expressed in terms of norms of reaction, with each line in Figure 1 representing a different individual. In both Figure 1a,b, the individuals differ in the mean level of behavioral expression (different elevations), but in Figure 1a, the individuals are highly consistent in behavior, whereas in Figure 1b, the individuals are highly inconsistent in behavior (i.e., individuals in Figure 1a have different slopes to individuals in Figure 1b). In Figure 1c, both individuals are inconsistent in behavior (slopes not equal to 0) but differ from one another in both the mean level of behavioral expression and the slope (i.e., differ in intraindividual consistency). The key point is that consistent individuals are predictable in behavior, whereas inconsistent individuals are not (i.e., the sign and the magnitude of the slopes are not predictable over time or across contexts). This means that within a population, some individuals express a behavior of interest (e.g., exploration, aggression, risktaking) more (Figure 1a) or less(figure 1b,c) consistently than other individuals across contexts, even though the rank order of different individuals may remain the same (Figure 1b). threatening individual (Barta et al. 2002; Wiebe 2010). Such credible promises or threats can signal the future behavior or intentions of individuals (McNamara and Houston 2002) and could, in combination with sexual selection, lead to both the evolution and the maintenance of consistent individual differences in behavior (interindividual variation with intraindividual stability: personality; Schuett et al. 2010). Threats or promises are credible if individuals commit themselves to a particular course of action even if it later becomes disadvantageous to do so (McNamara and Houston 2002; Dall et al. 2004). Frequency-dependent selection maintains a range of trait values within a population, with natural variation in behavior among individuals providing the necessary selection pressure to exacerbate variation (McNamara et al. 2009). Variation in behavioral consistency among individuals can be maintained if individuals monitor each other s cooperative tendencies at a cost (McNamara et al. 2009; e.g., a cost of detecting behavioral consistency during mate choice). When some individuals show social sensitivity basing actions on prior behavior of other individuals at a cost to themselves - selection favors variability in consistency, which in turn favors individuals that show social sensitivity (McNamara et al. 2009). Socially sensitive individuals are expected to only choose trustworthy individuals (i.e., individuals with high behavioral consistency), so this leads to selection for more consistent behavior in the population because this reduces the probability of pairing with an untrustworthy individual (and suffering reduced fitness prospects as a result of exploitation by the untrustworthy individual). The increased consistency of behavior results in a reduction in social sensitivity (because it is costly and the majority of individuals are trustworthy), which favors a subsequent increase in untrustworthy individuals, as they will have a greater fitness payoff in a population largely composed of trustworthy individuals. This favors social sensitivity, which then selects for trustworthiness, and so on. Such dynamic feedback results in the maintenance of combinations of extreme personalities and social sensitivity at evolutionary stable strategy frequencies (Dall et al. 2004). Sexual conflict and behavioral consistency In the context of the provision of costly biparental care, behavioral consistency could be an important indicator of an individual s willingness to provide PI that may help resolve sexual conflicts over care. Behavioral consistency can be selected via female choice if there are benefits to females of predictable male behavior (Schuett et al. 2010). Females may monitor behavioral consistency indirectly through observing males engaging in risky behaviors (e.g., in the context of foraging or social interactions) or directly through behavior during courtship (e.g., how persistent and/or responsive they are in display or aspects of their courtship song). If both male and female are consistent in behavior, as advertised (i.e., they are both trustworthy), then there should be little uncertainty over the relative amount of investment each is willing to commit, so that, if individuals are of similar quality (and can therefore afford similar amounts of investment), reproductive success will be increased accordingly (sensu Royle et al. 2002). On the other hand, if individuals within a pair differ in their level of behavioral consistency (e.g., in trustworthiness), exploitation of the behaviorally consistent individual is expected (or vice versa). If, for example, there is female sensory bias for male predictability (Schuett et al. 2010), which is expected to evolve if there is mate choice based on a male indicator trait that is correlated with male provisioning behavior (Wolf et al. 1998), then untrustworthy males may reduce their investment, leaving females to do more work. This may lead to the evolution of counter strategies ( credible threats ; Dall et al. 2004), such as the strategic reduction of body reserves by females to reduce the possibility of male desertion (e.g., Barta et al. 2002; McNamara and Houston 2002). Conversely, male predictability can be exploited by females if females are behaviorally inconsistent (untrustworthy). Predictability may be particularly advantageous if there are benefits to signaling intent to commit investment. Preemptive

3 Forum: Ideas 3 commitment (making the opening move in a sequential game) can be profitable when conflicts of interest are only slight, as the responding individual cannot punish its partner without also damaging its own interests (Hirshleifer 2001). This is because, when conflicts of interests are slight, the current and future interests of both partners are closely aligned so, for example, a large reduction in PI in response to a low level of initial investment from its partner will result in a reduction in fitness for both individuals. Signaling the intent to commit investment benefits both partners but particularly the individual making the opening move as it is more likely to achieve its ideal level of investment. In contrast, when conflicts of interest are high, the responding individual is expected to behave in a way that is damaging to its partner, so whatever the first move, (s)he will be vulnerable to a countermove (Hirshleifer 2001). In these circumstances, it is vital to have the last, not the first, move. A good example of a species in which having the last move is vital is provided by the penduline tit Remiz pendulinus, which is a small Eurasian passerine with uniparental care that, unusually, can be either the male or the female parent. Either sex can desert the other during incubation, and often, this is achieved simultaneously so that the nest is abandoned by both parents (female desertion: 18%, male desertion: 48%, and both desertion: 34%; Persson and Öhrström 1989). The large well-insulated nest provides the potential for uniparental incubation as the eggs cool slowly, and this gives even single parents time to forage during incubation (Hoi et al. 1996). However, females are still at a disadvantage because internal fertilization of eggs means that they have to attend the nest until the last egg is laid, whereas males could desert as soon as all eggs are fertilized, usually 24 h before laying. Males will often desert as soon as the first egg is laid, but females have evolved behaviors to counteract this. During laying, females cover their eggs and behave aggressively toward males around the nest (Valera et al. 1997), which reduces the ability of males to determine when laying has started, and increases the females chances of successfully deserting first. Experimental removal of males during laying induces females to stop the covering behavior, strongly suggesting that it has evolved in direct response to male desertion risk (Valera et al. 1997). Reactive commitments in response to another individual (i.e., social sensitivity) take the form of credible threats and/or promises (Hirshleifer 2001). Under conditions of low-to-moderate sexual conflict over PI, as might occur in species with broadly symmetrical biparental care (e.g., zebra finches Taeniopygia guttata), for example, preemptively signaling commitment via behavioral consistency (low intraindividual variation in behavior) could provide males with an advantage in determining the outcome of the conflict over investment. In these circumstances, it will be in the female s best interests to be of similar behavioral consistency to the male (i.e., equally trustworthy), so she is less likely to be exploited by the male. The trustworthiness of the female should also, in turn, increase the probability of the male committing a greater amount of investment, alleviating the conflict of interests accordingly. Behavioral consistency and provisioning rules So how does behavioral consistency for traits not directly involved in the provision of parental care translate to behavioral consistency in parental care? The most plausible suggestion, given the high likely costs of complex and flexible decision making, is that animals use computationally simple decision rules that perform well across a range of circumstances (McNamara et al. 2009), although there may also be direct selection for signaling intent using simple rules if going first pays (see above; Hirshleifer 2001). In the context of parental care, these simple decision rules relate to the provisioning of offspring and are important determinants of the amount of PI realized at conflict resolution (Parker 1985; McNamara et al. 1999; Parker et al. 2002). If behavioral consistency for traits not directly related to parental care (e.g., exploratory or aggressive behavior) is closely correlated with consistency during parental care (i.e., it is a behavioral syndrome; sensu Sih and Bell 2008), then we would expect, for example, individuals with highly consistent exploratory behavior to also show highly consistent patterns of parental effort. The different models of provisioning behavior can be distinguished accordingly: High consistency of effort and no response to a change in partner effort signal a sealed bid response rule (e.g., Parker 1985); but high consistency of effort and a facultative response to a change in partner effort (i.e., social sensitivity) signal negotiation based on information asymmetry (Johnstone and Hinde 2006) as this predicts a positive relationship between the consistency of individual effort and the strength of compensation to changes in partner effort. In contrast, in standard negotiation models (e.g., McNamara et al. 1999), where individuals negotiate effort in real time because they encounter partners that vary in quality, which cannot be assessed accurately prior to pairing, a low consistency of effort combined with a facultative response to a change in partner effort (i.e., social sensitivity) is predicted. Personality and provisioning rules So what then is the expected relationship between personality and provisioning rules (Table 1)? Individuals with highly consistent behavior over time and/or across contexts (i.e., low intraindividual variation in behavior; Figure 1) are expected to utilize either information asymmetry negotiation or sealed bid provisioning response rules, depending on whether they are, respectively, responsive, or unresponsive to short-term changes in partner effort. In contrast, individuals that are less consistent in behavior (i.e., high intraindividual variation in behavior; Figure 1) are expected to negotiate resources or utilize a sealed bid strategy, depending on whether they are, respectively, responsive, or unresponsive to short-term changes in partner effort. Behavioral combinations of individuals and reproductive success Success in biparental care depends on coordination of activities (Johnstone and Hinde 2006), so the behavioral combinations of the personalities of collaborating males and females are also important. Few studies have looked at the relationship between personality and parental care (Schuett et al. 2010), but of those that have, most have shown a positive benefit of assortative mating with respect to behavioral phenotype (e.g., Budaev et al. 1999; Dingemanse et al. 2004; Both et al. 2005; Sinn et al. 2006; Spoon et al. 2006; Schuett W, Dall SRX, Royle NJ, unpublished data; although not always, see van Oers et al. 2008), and behavioral consistency (Schuett W, Table 1 The expected relationship between personality and models for the resolution of sexual conflict Consistent? Responsive? Yes Yes Information asymmetry Sealed bid No Standard negotiation Sealed bid No

4 4 Behavioral Ecology Dall SRX, Royle NJ, unpublished data). In addition, recent studies have demonstrated that individuals prefer mates of similar quality to themselves (Holveck and Riebel 2009), which is likely to be closely related to personality if risk-taking behavior is linked to resource acquisition ability (Sih and Bell 2008), and that females prefer behavior-compatible males (i.e., similar in exploratory tendency; Schuett W, Godin J-DJ, Dall SRX, unpublished data). The combined results of these studies show that females actively choose males with similar personality traits to themselves and that there are reproductive benefits of doing so. Division of labor, sexual conflict, and personality The examples discussed up to this point have mainly considered sexual conflicts over the provision of investment in species with similar sex roles. However, in many species with biparental care, males and females have strong division of labor between the sexes (e.g., Itzkowitz et al. 2001; Walling et al. 2008; Wiebe 2008). Conflicts can be intensified if there are sex differences in reproductive roles (Lessells 1999), so it might be expected that the relationship between personality and sexual conflict will differ depending on how much sexual division of labor there is between species. Distinct sex roles in the division of care in biparental species are associated with alternative reproductive tactics in the least constrained sex (Clutton-Brock 1991). In most altricial species of birds, for example, males have reduced investment in incubation effort, and it has been suggested that this increases the amount of effort that can be put into alternative mating opportunities (e.g., extrapair copulations or polygyny; Wiebe 2008), thereby intensifying conflicts over PI. However, partner removal and handicapping experiments show that there is considerable flexibility and overlap in how the sexes partition PI in many species with distinct sex roles (e.g., Itzkowitz et al. 2001; Rauter and Moore 2004; Smiseth et al. 2005; Suzuki and Nagano 2009; Wiebe 2010). For example, in the Northern Flicker Colaptes auratus, a species of woodpecker with reversed sex roles and facultative polyandry, the male provides the majority of the PI during incubation (Wiebe 2008), but both males and females either compensated fully in response to handicapping of their partner during incubation or abandoned the breeding attempt (Wiebe 2010). Females had a greater tendency to abandon the brood following handicapping, consistent with their greater alternative reproductive opportunities compared with males (Wiebe 2010). Full compensation indicated that Northern Flickers did not follow sealed bid rules for determining incubation effort (Wiebe 2010). In Nicrophorus (burying) beetles, which also have welldifferentiated sex roles during parental care, with females providing most of the direct care of offspring (Walling et al. 2008), females showed no change in care when males were removed, but single males showed partial compensation (Rauter and Moore 2004; Smiseth et al. 2005; Suzuki and Nagano 2009). In addition, males were more variable than females in the amount of care they provided (Walling et al. 2008). Although these results are likely to be primarily due to females being unable to respond by working harder when males are removed because they are already working at or close to maximal capacity, the larger variation in male behavior compared with females provides the potential for females to chose males based on an indicator of their parental care ability, such as personality. CONCLUSIONS AND FUTURE PROSPECTS The partial compensatory response shown by Nicrophorus beetles is also typical of the response to a change in partner effort by species of bird with biparental care (Harrison et al. 2009). In contrast to burying beetles, however, females tend to be more responsive than males to changes in parental effort by their partner. In addition, females tend not to respond differently to manipulations that affected the attractiveness of their partners, indicating that females are more responsive to indicators of PI in males rather than good genes (Harrison et al. 2009). This meta-analysis supports recent models that predict males will be selected to reliably advertise their qualities as parents in species where male parental care affects offspring fitness (as in species with biparental care) and males vary in quality (Kelly and Alonzo 2009). However, the reliability of male advertisement as an indicator of male care may be reduced if allocation of effort to future reproduction is included in the models (Kelly and Alonzo 2009), suggesting that potential indicators of male PI, such as behavioral consistency, will be more reliable when sexual conflict is less intense (i.e., future fitness returns are closely aligned within a pair). Therefore, if, as we have suggested here, behavioral consistency provides a good indicator of the willingness of males of males to provide PI, we predict that individuals will differ more in their behavioral consistencies in species with symmetrical biparental care (i.e., lower conflicts of interest over provision of PI) compared with those with more skewed biparental care or uniparental care (i.e., higher conflicts of interest). Furthermore, we predict that provisioning rules will be related to personality (i.e., behavioral consistency in parental care will be correlated with consistency in other contexts, e.g., courtship behavior) and that breeding pairs where the individuals are similar in behavioral consistency to one another (all else being equal, i.e., for a given level of parental quality) will have higher reproductive success than if the pairs are dissimilar to one another. These predictions can be tested by quantifying the behavioral consistency of individuals in breeding pairs (Schuett et al. 2010) and quantifying the provisioning rules (e.g.,using handicapping and playback experiments, e.g., Hinde and Kilner 2007) and comparing the reproductive fitness of pairs in relation to their similarity in behavioral consistency. In addition, more work needs to be done to investigate and quantify the relationship between behavioral consistency and mate choice (Schuett et al. 2010). Although there is information available on interspecific variation in provisioning rules for species with biparental care (Sanz et al. 2000; Schwagmeyer and Mock 2003; Harrison et al. 2009), there is little information available on interspecific variation in behavioral consistency (Schuett et al. 2010). More importantly, there is currently little known about intraspecific variation in behavioral consistency (Dingemanse et al. 2010; though see Schuett W, Dall SRX, Royle NJ, unpublished data), especially during provisioning (though see Nakagawa et al. 2007), and nothing is known about how consistency in behavior in the context of parental care correlates with consistency of behavior in other contexts (e.g., exploratory behavior, aggression, or courtship). Addressing these issues will be fundamental to testing the ideas proposed in this paper. The ideas presented in this paper could also be incorporated relatively easily into formal models of sexual conflict. For example, Johnstone and Hinde (2006) demonstrate that if there is an asymmetry in uncertainty about brood need between parents, the parent with least uncertainty (most information) should compensate more for shortcomings in its partner s effort and thereby end up doing most of the provisioning to the brood. From a personality perspective, this result suggests that males may have strong incentives to signal their condition to mates by maintaining a consistent level of risk-taking across contexts in the lead up to pairing and breeding (presuming that the costs of doing so handicap their abilities to be

5 Forum: Ideas 5 consistent: Schuett et al. 2010). This is because, if a female knows a male s condition, then variation in his parental effort provides exclusive information about brood need (Johnstone and Hinde 2006). Furthermore, Johnstone and Hinde (2006) show that even when both parents are equally uncertain about brood need, the more certain they are about each other s condition during provisioning, the better parents they are the more overall investment the brood receives. This again suggests a selective advantage to both parties to being consistent in their foraging and exploratory behavior with few conflicts of interest (e.g., when outside options are limited for both sexes). Thus, it is possible to explore the impact of behavioral consistency (and hence predictability) on evolutionary stable outcomes of negotiation over parental effort. Such outcomes will predict the relative brood rearing success of, and the costs in terms of future reproduction to individuals in, different parental consistency pairings, thereby specifying the conditions under which personality may be selected for as a means of resolving conflicts over PI. FUNDING European Social Fund studentship to W.S. Some of the ideas for this paper were conceived when N.J.R. was in receipt of Natural Environment Research Council fellowship NE/ C002199/1. Thanks to Mike Cant and 2 anonymous reviewers for helpful comments on earlier drafts of the paper. Key words: behavioral syndromes, credible threats and promises, parental care, personality, sexual conflict, sexual selection, temperament. Address correspondence to N.J. Royle. n.j.royle@exeter.ac.uk Received 27 March 2010; revised 4 August 2010; accepted 2 September REFERENCES Barta Z, Houston AI, McNamara JM, Szekely T Sexual conflict about parental care: the role of reserves. 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