Christina Riehl,Joshua B. LaPergola
Inclusive fitness explains behavioral diversity in a social bird
Inclusive fitness explains behavioral diversity in a social bird

In 1964, William Hamilton proposed an elegant explanation for how interactions between genetic relatives could affect selection on competitive and cooperative traits (1). The logic underlying Hamilton’s premise was simple: Since identical gene copies are shared by parents and offspring as well as by more distant relatives, selection should favor traits and behaviors that increase the lifetime reproductive success of individuals (their “direct” fitness) as well as of their family members (their “indirect” fitness). The general predictions of this thesis, which came to be known as kin selection, have been robustly supported over the past 60 y. Despite occasional challenges, kin selection remains a central tenet of evolutionary biology (2). It set the intellectual agenda for modern behavioral ecology, inspiring research on phenomena ranging from eusociality to siblicide to sperm competition—and beyond (3). However, dissecting the relative importance of direct and indirect fitness remains a major challenge, particularly in field studies seeking to understand the evolution of complex cooperative societies. Researchers still disagree about how such fitness components should be defined and measured, and the basic data needed to do this are notoriously difficult to collect in wild populations. In this issue, a new paper by Koenig et al. (4) provides a road map for measuring direct and indirect fitness components in the acorn woodpecker (Melanerpes formicivorus), a long-lived bird that can breed either alone or in social groups. This study not only sheds light on the evolution of a fascinating and unusual breeding system, it provides a new method and a proof-of-principle test for future researchers attempting to understand the selective pressures shaping sociality. Acorn woodpeckers are noisy, gregarious birds, with boldly patterned black-and-white plumage and bright yellow eyes that give them a slightly clownish appearance. Although their range extends from the Pacific Northwest to northern Colombia, most of our knowledge of their reproductive biology comes from the population at Hastings Reservation in central California, where Walt Koenig, Eric Walters, Joey Haydock, and their colleagues have studied them continuously since 1974 (5). As their name suggests, acorn woodpeckers are highly dependent on oak trees: At Hastings and in other nonmigratory populations, they store acorns in individually drilled holes in specialized storage trees, called granaries, that may harbor thousands of acorns that provide critical food during periods of resource scarcity (6). Acorn woodpeckers breed either as single pairs or in cooperative groups that include between 3 and 15 individuals. Each group excavates a single nesting cavity in a tree that serves as the communal nursery and defends a territory that contains additional roosting cavities and one or more granary trees. The simplest groups contain a breeding pair and one or more nonbreeding “helpers,” who are typically offspring of the breeding pair who have remained with their parents to assist in rearing younger siblings. Other groups contain more than one breeding male or female. These can exist in a variety of configurations, including one male sharing a nest with two or more laying females and siring all of their offspring; one female mating with two or more males and laying a single clutch of mixed paternity; or groups with multiple males and multiple females, all of whom contribute offspring to the clutch (5). This type of cooperative polygamy is rare in birds, but the interactions between cobreeding adults—who must coordinate their reproduction and parental care while competing for reproduction in the mixed clutch—provide rich opportunities to explore the costs and benefits of social nesting. Some of these costs are obvious. Female acorn woodpeckers fight with each other over reproduction, often destroying each other’s eggs by removing them from the nest cavity and eating them. This friction arises over competition for reproduction in the nest, driven by the difficulties in incubating and caring for an enlarged clutch of eggs. As a consequence, females tend to raise fewer of their own offspring per clutch when they share reproduction than when they are the sole layer (4, 5). Males suffer similar reductions since they must share paternity of a limited number of eggs with their fellow male group-mates. Indirect fitness benefits, though, could partially or completely recoup these direct fitness costs since group members are nearly always close relatives of their same-sex cobreeders. Males who share reproduction are typically either brothers (who sometimes disperse from their natal nest in fraternal coalitions) or father-and-son pairs (in situations where an unrelated female is available for the son to mate with). Similarly, cobreeding females are typically sisters, or mothers and daughters. Furthermore, cooperative nesting has been linked to additional direct fitness benefits that are not reflected in clutch size, such as increased adult lifespan and earlier age at first reproduction (7). It is possible, therefore, that the total “inclusive” fitness benefits of cooperative polygamy—the sum of both direct and indirect fitness components—outweigh the costs. If so, the lifetime fitness of a cooperative nester might equal or exceed that of a bird nesting singly. Alternatively, cooperative polygamy might result in a net fitness loss, such that single nesting is an optimal strategy and cooperation is a “best of a bad job,” employed only by birds who are unable to breed alone. Quantifying these fitness payoffs is key to understanding how a diversity of breeding strategies can stably coexist in a single population. Koenig et al. (4) used 30 y of meticulously collected field data on over 500 acorn woodpeckers to document individual survival, reproductive output, and breeding strategy. Doing this in long-lived animals is no trivial task: In fact, the dataset was restricted to birds who hatched prior to 2007, in order to exclude those who might still be alive and reproducing. Statistically, determining the effect of cooperative nesting on lifetime fitness presents a different challenge since a given individual might nest singly in some years but cooperatively in others. Koenig et al. (4) simplified this calculation by using the mean number of cobreeders that an individual had over its lifetime as their measure of cooperative polygamy. The authors then measured the observed direct fitness (offspring produced) of each bird over each year of its life, as well as each individual’s observed indirect fitness (offspring produced by its related cobreeders). Observed inclusive fitness was, therefore, the sum of these two components. Notably, however, the authors also calculated the alternative fitness that each individual would have achieved, had it employed a different breeding strategy—in other words, the counterfactual situation in which a group nester bred singly and its cobreeders had bred without it, or in which a single breeder had instead joined a group. This approach enabled them to compare observed fitness values with alternative scenarios, generating estimates of the net fitness effect of breeding in cooperative groups of varying sizes. This study not only sheds light on the evolution of a fascinating and unusual breeding system, it provides a new method and a proof-of-principle test for future researchers attempting to understand the selective pressures shaping sociality. This method yielded interesting results, highlighting sex-specific differences in the tradeoffs to male and female woodpeckers. Most strikingly, the authors found that males gained no inclusive fitness advantage or disadvantage by cobreeding: Their gains in indirect fitness (achieved by rearing their relatives’ offspring) were canceled out by their reductions in direct fitness. Females, by contrast, achieved higher inclusive fitness by breeding in intermediate-sized groups (two cobreeding females) rather than singly or in large groups, since cobreeding was associated with an earlier age of first reproduction. Previous studies have found that male and female life histories differ in other important respects, including survival, reproductive lifespan, and reproductive skew within cooperative groups (7, 8). Whereas egg destruction by cobreeders ensures that each female contributes approximately the same number of eggs to the shared clutch, cobreeding males typically share parentage unequally, with one male monopolizing the lion’s share of paternity and some “cobreeders” failing to breed at all (8). Understanding why cooperative nesting allows females—but not males—to reproduce earlier than single nesters could prove key to understanding why the inclusive fitness effects of cooperative polygamy differ for the two sexes. Koenig et al.’s (4) results help to explain why male acorn woodpeckers employ such an unusual variety of breeding strategies: Neither single nesting nor cobreeding yields a predictable inclusive fitness advantage, so no “optimal” strategy prevails in the population. The relative frequencies of cooperative polygamy in the Hastings population are consistent with this hypothesis: About 45% of breeding groups contain more than one reproductive male, with the rest containing a single male. For females, however, the results are more perplexing. According to the inclusive fitness calculations in this paper, females should profit from nesting in duos—yet cobreeding is less common than single nesting. Fewer than 25% of breeding groups contain more than one reproductive female, and less than half of females nest with cobreeders (5). Although the authors invoke the physiological costs of egg destruction as a possible explanation for the rarity of female cobreeding, this explanation is not altogether satisfactory: Such costs, if they are high enough to limit cobreeding, should presumably be expressed by reductions in female survival or reproductive output and therefore should have been captured by the methods employed in this paper. A more promising explanation is that females may simply lack close relatives with whom to breed. Whereas males often disperse in coalitions with their brothers or inherit a breeding position in their natal group, females tend to disperse singly and rarely remain with their natal group to breed (5). More research on the factors that prevent females from forming coalitions is needed to understand the mismatch between the relative rarity of female cobreeding and its apparent benefits. Koenig et al.’s (4) method of calculating inclusive fitness considers fitness from the perspective of the individual, not the gene or the genetic lineage. Consequently, it considers only offspring produced by the focal individual (and its kin) in one generation. Such a method has its limitations (9), but it is both practical and intuitively appealing for field researchers, who usually lack the data on demographic structure and multigenerational pedigrees needed for gene-based approaches. Their method also provides a workable solution to the problem that researchers face in quantifying the fitness effects of a behavioral strategy when individuals may employ different strategies across years. Finally, Koenig et al. (4) highlight the value of long-term, open-ended field research on animal populations. When this study began, just a decade after the publication of Hamilton’s key insight, the statistical and molecular tools used to analyze this dataset had not yet been developed. Given the acorn woodpecker’s long lifespan—up to 17 y in the wild—the 50-y span of this study was clearly fundamental to measuring lifetime inclusive fitness. Such detailed pictures of the lives of known individuals are of immeasurable value to evolutionary biologists, but we have only a small number of these studies. Koenig et al.’s (4) results underscore the importance of long-term, individually based studies for our understanding of inclusive fitness in nature.