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Perspectives: Hamilton'S Legacy: Mechanisms of Kin Recognition in Humans ethologyinternational journal of behavioural biology Ethology CURRENT ISSUES – PERSPECTIVES AND REVIEWS Perspectives: Hamilton’s Legacy: Mechanisms of Kin Recognition in Humans Jill M. Mateo Department of Comparative Human Development, Institute for Mind and Biology, The University of Chicago, Chicago, IL, USA (Invited Review) Correspondence Abstract Jill M. Mateo, Department of Comparative Human Development & Institute for Mind and The behavior literature is replete with examples of individuals exhibiting Biology, The University of Chicago, 940 East costly acts that benefit someone else. These examples troubled Darwin so 57th Street, Chicago, IL 60637, USA. much so that he thought they would be fatal to his theory of natural selec- E-mail: [email protected] tion. A century later, W. D. Hamilton refined that theory by showing, quantitatively, that such acts could be favored if the individuals involved Received: October 18, 2014 were relatives. His theory of inclusive fitness is generally considered one Initial acceptance: November 18, 2014 of the greatest theoretical advances in evolution since Darwin’s time. Less Final acceptance: December 26, 2014 appreciated from Hamilton’s 1964 paper is the hypothesis that mecha- (M. Hauber) nisms favoring accurate kin recognition will also be selected. Here, I doi: 10.1111/eth.12358 review those recognition mechanisms and survey the literature on human kin recognition. Although not often considered, humans both produce Keywords: kin recognition, humans, cues to kinship that vary with genetic relatedness and have perceptual Hamilton, inclusive fitness, discrimination abilities to detect these cues in others and assess that relatedness. The potential functions of these abilities are discussed. Importantly, gaps in our understanding of the development and use of recognition mecha- nisms are noted. perception of like genes in other individuals, at the Introduction minimum, genes should affect ‘(1) some perceptible Fifty years ago, W. D. Hamilton not only made the feature of the organism, (2) the perception of that fea- most significant refinement to Darwin’s theory of nat- ture, and (3) the social response consequent upon ural selection with his concept of inclusive fitness what was perceived’ (Hamilton 1964b; p. 25). Today, (Hamilton 1964a), but also predicted the evolution of an understanding of kin recognition involves three mechanisms to facilitate the accurate recognition of components: the production of unique phenotypic kin (Hamilton 1964b). He posited that if one ‘could cues, or ‘labels’, the perception of these labels and their learn to recognize those of his neighbors who were degree of correspondence with a ‘recognition template’ really close relatives and could devote his beneficial (these components are the mechanism of recognition), actions to them alone an advantage to inclusive fitness and the action taken by an animal as a function of the would at once appear’ (Hamilton 1964b, p. 21). Kin similarity between its template and an encountered recognition is an unobservable internal process of phenotype (Beecher 1982; Sherman & Holmes 1985; assessing genetic relatedness that is inferred by kin dis- Reeve 1989; Gamboa et al. 1991; Mateo 2003, 2004). crimination, the observable differential treatment of In this essay, honoring the 50th anniversary of Hamil- conspecifics based on cues that vary with relatedness. ton’s theory of inclusive fitness and mechanisms of kin Hamilton posited that if relationships persist, weak recognition, I discuss these processes in humans, selection could favor the evolution of discrimination, briefly summarize behaviors that influence inclusive even among distant kin. He added that although it fitness and then survey the literature on mechanisms may seem improbable that genes could cause the leading to kin-differentiated behaviors. Ethology 121 (2015) 419–427 © 2015 Blackwell Verlag GmbH 419 Kin-Recognition Mechanisms in Humans J. M. Mateo Recognition can be based on prior association, as households than are genetic kin (Daly & Wilson 1980, organisms learn the labels of related individuals 1982a), demonstrating clear fitness differentials as a during early development (e.g., siblings) and later dis- function of relatedness. Adoption occurs more fre- criminate these familiar individuals from unfamiliar quently among close kin (r = 0.125–0.25) than more ones, or, organisms can learn their own phenotypes distant kin (r ≤ 0.0625); such acts may constrain and/or those of their familiar kin and later compare or future reproduction by the adopting parent (Silk match the phenotypes of unknown individuals to this 1980). People leave a larger proportion of their estate learned template (phenotype matching). Both mecha- to their close kin than to distant kin or non-kin nisms involve comparisons between phenotypes and (Smith et al. 1987; Judge & Hrdy 1992; see also Kal- templates, but prior association leads to recognition of barczyk-Steclik & Nicinska 2012 for data on financial familiar individuals only, whereas phenotype match- transfers to parents as a function of relatedness). ing, through generalization from templates, permits Genetic fathers also invest more in their children than ‘recognition’ of unfamiliar kin (Holmes & Sherman do stepfathers (e.g., Anderson et al. 1999). Differen- 1982; Sherman et al. 1997; Tang-Martinez 2001; tial financial investments may not be costly to the Mateo 2004). This distinction is important when con- parents, certainly not after death, but can have long- sidering kin-directed behaviors such as nepotism or lasting effects on the offspring, particularly when inbreeding avoidance, because phenotype matching young. Although helping behaviors (e.g., with hous- allows more refined discrimination among kin classes ing, finances, health) are more likely to be recipro- than does prior association. Note that some species cated among friends, close kin help each other more can utilize both recognition mechanisms (and others) often than distant kin, and larger acts of helping are depending on the age of kin and the context (Mateo more likely to come from kin (e.g., Essock-Vitale & 2008). Finally, phenotype matching would be difficult McGuire 1985; see also Korchmaros 2006). These if production cues do not vary predictably with kin- helping behaviors are not costly in fitness terms and ship, but such cues could be used reliably for recogni- may only have short-term benefits, but demonstrate tion when prior association correlates with that even when the stakes are low, individuals pay relatedness, such as for parent–offspring recognition. attention to kinship and behave differentially. Kin-recognition abilities have been studied most How do humans assess genetic relatedness? Con- broadly in rodents (reviewed in Mateo 2003), ventionally, we know who our kin are because we although several species in other taxa have been ele- grow up with them or our parents inform us (e.g., Lie- gantly studied (birds: Beecher 1988; insects: Getz berman et al. 2007), and the established kinship ter- 1991; Gamboa 1996; Waldman 1991; anurans: Blau- minology of each culture can provide additional stein & Waldman 1992; Pfennig et al. 1999; primates: indicators of relatedness (e.g., Fox 1967). Barring Kazem & Widdig 2013; Pfefferle et al. 2014). Most errors or intentional withholding of information (e.g., empirical studies of kin-recognition mechanisms have in cases of adoption), this is a reliable mechanism. focused on visual and olfactory discrimination of con- Indeed, sharing a parent and growing up together are specifics (see below), but relatedness potentially could excellent cues to relatedness, at least for close kin be assessed through other modalities, such as vibra- (Lieberman et al. 2007). However, humans are capa- tional signaling (e.g., Randall 1993; O’Connell-Ro- ble of using several perceptual modalities and physio- dwell et al. 2007), behavioral cues (e.g., Michener logical cues to discriminate among familiar kin and to 1973; Boncoraglio et al. 2009), or vocalizations (e.g., discriminate among unfamiliar kin and non-kin. Rendall et al. 1996; Insley 2001; Briefer et al. 2012; Akcay et al. 2013). It is important to note that there Visual Modality of Kin Recognition may be multiple, overlapping modalities indicating kinship (e.g., Coleman 2009). Given the reliance of humans on visual cues (indeed, According to Hamilton’s theory of inclusive fitness, there are neural areas that specifically respond to costly behaviors can evolve when the benefit (b)to faces; see below), facial resemblance might be the recipient, devalued by the coefficient of relation- expected to serve as indicators of kinship. Recognition ship (r), is greater than the cost (c) to the actor (rb>c). of offspring would be especially important for appro- Here, benefits and costs are measured in terms of fit- priate allocation of parental investment. Mothers can ness effects (Hamilton 1964a). Among humans, there recognize photographs of their infants within 33 h of are many examples of kin-biased behaviors, although birth, and strangers can match photographs of moth- not all involve costly behaviors. For example, spouses ers to their infants, suggesting a physical resemblance and step children are more likely to be killed in among kin (Porter et al. 1984). Because the mothers 420 Ethology 121 (2015) 419–427 © 2015 Blackwell Verlag GmbH J. M. Mateo Kin-Recognition Mechanisms in Humans had direct contact with their infants (X = 4.7 h), their among other methodological differences. For exam- recognition could
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