Sibling Symbiosis in Nestling Birds

Gonzaga: Once more, brothers in arms. Bertoldo: I’ll live and die so. Philip Massinger, Maid of Honor (1632) If the title of this perspective were “Sibling rivalry in nestling birds,” readers could hardly be faulted for expecting a traversal of well- trodden ground. We have come to think of conflict among avian nestlings as natural and to some extent inevitable, which is a long way from the traditional view of families as harmonious social units. It is de rigueur to state that the theory of kin selection opened our eyes to the once-surprising possibility that the closest of relatives may benefit at one another’s expense. The Cain-and-Abel battles of Black Eagles (Aquila verreauxi) and other large predatory birds, which had been described as “an inexplicable example of apparent biological waste” (Brown et al. 1977), became potentially explicable as extreme forms of sibling competition in cases where close relatives were also close rivals for limited food and tight space. We learned that nestling egrets, boobies, and ospreys fight to secure food, with sometimes fatal consequences; that nestling bee-eaters can use a modified egg-tooth to slash nestmates; and that kestrels and owls sometimes cannibalize kin. These and many more spectacular examples of sibling rivalry were chronicled in Mock and Parker’s (1997) masterful Evolution of Sibling Rivalry, which provided a comprehensive overview of theory and data bearing on conflict within families, especially conflict among siblings. Birds were featured prominently in the book, and dramas within the nest captured widespread interest both within and outside ornithology. Mock and Parker left little doubt that siblings within a nest are often important, and sometimes lethal, competitors for food and space. This focus on conflict is an understandable reflection of changing notions of the family and, in particular, revision of the earlier, somewhat romantic notion that close kin must live harmoniously because of their shared genetic interests. But have we gone too far? If one uses the scientific literature to gauge relative interest in sibling relations, it is clear that the pendulum has swung sharply to the side of conflict, competition, and rivalry. A recent (November 2006) search of the Web of Science revealed 334 citations for the keywords “nestling conflict” or “nestling competition,” and only 11 for “nestling cooperation” or “nestling mutualism.” Though I doubt that any serious worker has forgotten that cooperation is also expected among close kin, I suspect that many find conflict a more compelling topic of study than cooperation. Here, to help pull the pendulum back from the pole of conflict among siblings, I will focus on the social benefits that accrue to nestlings during life within a brood. In fact, the conflict-cooperation duality is a bit too narrow for my present purposes, and in its place I will borrow from the language of population ecology to refer to symbiosis (Wilson 1975), not among different species, but among siblings. There is a trio of potential symbiotic interactions (Table 1): parasitism, where one benefits and another suffers (as in siblicide); mutualism, where both parties benefit (as when two individuals cooperate to resist a predator); and commensalism, where one benefits and the other neither gains nor loses (as when one individual sits in the shade of another). Schematic description of different forms of sibling symbioses in structured families of nestling birds. Though it is more likely that core offspring will benefit (as shown here) from sibling parasitism or commensalism, marginal offspring could potentially benefit from these forms of symbiosis Schematic description of different forms of sibling symbioses in structured families of nestling birds. Though it is more likely that core offspring will benefit (as shown here) from sibling parasitism or commensalism, marginal offspring could potentially benefit from these forms of symbiosis The term “brothers in arms” made its first appearance in English literature in Philip Massinger’s 17th-century play Maid of Honor. Though it refers to the camaraderie of two Knights of Malta taking up arms in military service, “brothers in arms” seems appropriate for describing alliances that form among siblings during life in the nest. Though propinquity can make siblings rivals for food or space, it can also make them (1) close allies in battles with parents over the level of parental investment and (2) partners in producing and distributing thermal resources within the nest. It is these symbiotic interactions that I will focus on below. I will mention only briefly the now-familiar benefits of indirect fitness derived from the success of siblings (i.e., if siblings survive and thrive, which results in more descendents, because of an individual’s actions, an inclusive fitness benefit accrues to the latter; Hamilton 1964), because these are well studied and widely understood. And I will not directly address the intriguing issue of multilevel selection within families, whereby broods potentially become targets of selection, because that topic has been ably addressed by Wilson and Clark (2002). My purpose is to examine the forces that push siblings toward increased generosity as opposed to selfishness, and much of what follows, curiously, revolves around parentally imposed competitive asymmetries among contemporary offspring. These occur when parents impose phenotypic handicaps on certain of their progeny and not on others; resulting differences in egg size, hormonal titre, immune-system complement, or birth-hatching asynchrony render some offspring “more equal” than others (Lack 1947, Magrath 1990, Williams 1994, Schwabl et al. 1997, Forbes and Glassey 2000, Royle et al. 2003, Groothuis et al. 2005). Proximity is a key feature of family living from which opportunities for social symbiosis arise. But not all individuals are equally capable of deriving benefits, and some are more likely to pay costs. Asymmetries of power exist among family members, most obviously between parents and offspring but also among contemporary siblings, where age, developmental, physiological, and size differences place individuals on unequal footing. Parentally imposed handicaps divide contemporary siblings into castes of privileged “core” offspring that enjoy superior prospects for growth and survival and disadvantaged “marginal” offspring that suffer reduced growth and elevated mortality (Mock and Forbes 1995, Forbes et al. 1997, Mock and Parker 1997, Forbes 2005). This phenotypic division underpins the concept of the “structured family,” which is useful for examining the dynamics of avian families (Fig. 1). Parents with a structured brood face a more complex parental investment decision, particularly where older, stronger core offspring have partial or complete control over allocation of resources (Parker et al. 1989, Forbes 1993). In such cases, parents must work through core siblings to influence resource-allocation among their progeny, particularly allocation to junior marginal siblings (Fig. 1). By diverting a smaller or greater share of parentally delivered resources to marginal offspring, core offspring can potentially manage their “investment” in siblings to their own benefit, by mechanisms I will explore below. Schematic view of asymmetric sibling rivalry and parent-offspring conflict in a family with a structured brood. The relative strength of familial interactions is approximated by line width. Both parent-offspring and sibling relations are affected when the brood is structured into stronger core and weaker marginal siblings. Empirical work shows that core siblings have stronger effects on marginal siblings than vice versa. And when core siblings affect how food is allocated within the brood, parents must work through the core brood to affect food allocation to marginal offspring In altricial birds, nestlings rely on their parents to provide critical resources such as food and warmth. Theory predicts that parents and offspring should disagree over the preferred level of parental investment (Trivers 1974, Mock and Parker 1997; but see Evans et al. 1995 for an exemplary empirical demonstration of parent-offspring cooperation). Offspring demands are generally expected to exceed the parental optima, and communication between parents and offspring plays a key role in setting the level of investment for which nestling begging has proved to be a model (review in Wright and Leonard 2002). Contemporary theory views nestling begging as an evolutionary game among parents and offspring, with two key parental decisions, which the offspring can influence: how much to invest in current as compared with future broods, and how to allocate this investment among contemporary progeny (e.g., Parker et al. 1989, Godfray 1991, Rodríguez-Gironés et al. 2001, Royle et al. 2004). Offspring begging potentially affects both these parental decisions. Begging involves a dual system of vocal and visual cues, and the emerging view is that there is at least a partial functional separation of the vocal and visual elements of begging. Conspicuous visual displays—neck-stretching, gaping, wing-flapping, jostling—appear to be more important to within-brood allocation of parentally delivered food, and vocal cues more important in determining the overall level of brood provisioning (Muller and Smith 1978, Bengtsson and Ryden 1983, Leonard and Horn 2001, Glassey and Forbes 2002, Leonard et al. 2003), though vocal cues can also affect within-brood allocations (Price and Ydenberg 1995, Kilner et al. 1999, Leonard and Horn 2001, Sacchi et al. 2002). Wilson and Clark (2002) made the intriguing suggestion that selection for the design of signals for use within parent-offspring cooperation may simultaneously reflect individual competition and group- level cooperation. Competitive handicaps are expected to affect the outcome of begging games, and a robust theoretical prediction is that competitively inferior marginal siblings will need to beg harder to gain what is ultimately a lesser reward (Parker et al. 1989, 2002; Rodríguez-Gironés et al. 2001). This prediction has been empirically confirmed (Lotem 1998a, Cotton et al. 1999, Rodríguez-Gironés et al. 2002, Smiseth and Amundsen 2002). Moreover, if begging is subdivided into functionally separate components—one that influences provisioning and one that affects within-brood allocation—then theory further predicts that core siblings should allow their marginal nestmates to shoulder the burden of soliciting food from parents and exploit the efforts of their juniors (Rodríguez-Gironés et al. 2002). Effectively, core siblings parasitize the effort of marginal siblings. An interesting possibility arises. If vocal begging intensity governs parental delivery rate, then older, stronger siblings may benefit from the continued presence of hungry, loud runts. These marginal nestlings may, in fact, be ideal companions for larger core siblings, inducing parents to bring more food though unable to compete for it effectively. Such a mechanism could hold, even if the share of food that core siblings receive were to decline. A simple example based on the despotic allocation model of Forbes (1993) illustrates the logic of this (Fig. 2). Schematic overview of the relationship between brood size, food share, provisioning, and fitness in nestling birds. The uppermost panels represent a two-chick brood, with a senior sibling (alpha) and a junior sibling (beta). Food is shared according to a dominance hierarchy. The total food offered to the brood and shares to alpha and beta are represented by the pie chart. The direct fitness (f[m]) of alpha in relation to its per-capita food share (m) is shown in the upper left panel. The bottom panels represent a three-chick brood, with alpha, beta, and omega; total provisioning is split three ways, and the share of the pie to alpha now falls from 59% (upper pie chart) to 41% (lower pie chart). But because the overall size of the pie is larger, alpha’s m value increases in the larger brood, and alpha’s f(m) value rises (bottom left panel) The model assumes (1) that food is distributed according to an absolute and linear dominance hierarchy that resembles the food-allocation system of some siblicidal birds and (2) that food is shared in accordance with Hamilton’s Rule. Moreover, Parker et al. (2002) noted that begging scrambles among chicks of unequal competitive ability generate predictions similar to those of hierarchy models when the handicap is large. Here the most senior member of the brood hierarchy controls how much food to take for itself and how much to leave for its junior siblings. Although I do not expect the quantitative mathematics of this stylized system to apply closely to any empirical system, it illustrates the underlying logic. Given the explicit mathematical function used in the original model for the relationship between provisioning (m) and fitness (f[m]), the senior sibling (alpha) should take 59% of all parental provisioning in a brood of two, leaving the remaining 41% for beta. But in a brood of three, the share to alpha falls to 41%, the share to beta is 35%, and the share to the most junior nestling (omega) is 24% (Fig. 2). Does this falling food share mean that alpha is necessarily worse off in a brood of three? Not at all. The direct fitness of alpha need not decline at all if parents simply bring more food to the larger brood, as illustrated in Figure 2. If the pie gets larger, it may not matter that alpha’s share of the pie is smaller. This basic argument was presented in Forbes (1993) to explain why selfish siblings may not profit from brood reduction if parents diminish parental investment as a consequence (see also Rodríguez-Gironés 1996). Study of nestling begging behavior provides a proximate behavioral mechanism for this limit to selfishness: senior siblings may enjoy an increment to their personal fitness (not to mention inclusive fitness) from being in a larger brood if junior nestmates help to secure more parental investment for the entire brood. Recently, dramatic evidence of this effect has been found in studies of brood-parasitic cow- birds. Kilner et al. (2004) demonstrated experimentally that Brown-headed Cowbird (Molothrus ater) nestlings profited from the presence of more food to with both and nestlings than to with only and in when The larger can nestlings by of their larger size and and, as Kilner et al. (2004) exploit the effort of their There is why similar dynamics not in structured families in which larger, stronger core siblings can marginal nestmates in within-brood as and Kilner have could model this but a model is that the is If the begging effort of a marginal sibling the level of parental investment for the current brood, core siblings may benefit directly from the presence of marginal offspring, even though are competitors for Here, I to between in personal fitness to the senior sibling is more than by the gains in indirect in accordance with Hamilton’s and potentially or at least symbioses between siblings, where we expect gains in direct fitness for core offspring. If both the core and marginal siblings their level of provisioning through the begging effort of the the term the core sibling benefits and the fitness of the marginal is the is a in which the begging of the marginal offspring are by an increased food if the core sibling benefits at the of the marginal is the stronger core siblings are to manage the benefits or that accrue to their marginal core siblings ultimately the sibling relationship to parasitism, or Mock and Parker a potential example of sibling in nestling where the presence of a was to a stronger found that parents were likely to broods but not in a that if in the current parents could to and potentially a larger this a of parents the were off their offspring than not at all. in broods of two where core siblings the power of life or over marginal there was a for in the the of all parental Sibling symbiosis on an family that asymmetric sibling rivalry and Glassey The competitive that the core siblings can a greater share of parentally delivered resources siblings are to the role of inferior competitors during their nestling on receive food, more and die more often than core But by to core siblings can marginal siblings are more likely to in the and make or more Given their role of junior in a sibling it seems that marginal offspring that make the of a a possibility that has been little I will such are potentially important in the social benefits that accrue to because affect the fitness for or place for a to be is in where in may reflect 1996). 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