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The Perception Component of Social Recognition Ann. Zool. Fennici 41: 729–745 ISSN 0003-455X Helsinki 20 December 2004 © Finnish Zoological and Botanical Publishing Board 2004 Recognition systems and biological organization: The perception component of social recognition Jill M. Mateo Committee on Human Development, 5730 S. Woodlawn Avenue, University of Chicago, Chicago, IL 60637, USA (e-mail: [email protected]) Received 30 Apr. 2004, revised version received 12 Sep. 2004, accepted 12 June 2004 Mateo, J. M. 2004: Recognition systems and biological organization: The perception component of social recognition. — Ann. Zool. Fennici 41: 729–745. Recognition of conspecifics is necessary for differential treatment of individuals in a variety of social contexts, such as territory establishment and defense, dominance hier- archies, reciprocal altruism, mate choice, parent–offspring interactions and nepotistic contexts, to name a few. Here I first review various categories of perceptual mecha- nisms of social discrimination, focusing largely on the extensive literature on the per- ception component of kin recognition, although the ideas presented here can and have been used for analyses of recognition at many levels of social organization. I then dis- cuss a range of recognition mechanisms observed in a model species, Belding’s ground squirrels, and how socio-ecological factors influence the development and expression of each mechanism. Finally, I address several theoretical and empirical controversies in the kin-recognition literature which pertain to the perceptual component of recogni- tion, as well as areas in need of additional investigation. Introduction of cognitive processing or awareness) whereby animals become familiar with conspecifics and An understanding of recognition systems can later remember them and treat them accordingly, be important for explaining interspecific vari- based on the nature of those previous interac- ation in population cycles, nepotistic patterns, tions. Recognition can also be based on cues of dispersal and inbreeding avoidance (Charnov those individuals, on inanimate objects, or on & Finerty 1980, Blaustein et al. 1987, Hepper other proxies for identity such as spatial location. 1991a, Pusey & Wolf 1996, Sherman et al. While social recognition of individuals is not 1997), particularly in group-living species with required for kin selection, mate choice, tolerance on-going social interactions. Recognition abili- of neighbors or parental care, it can facilitate ties would be expected when animals interact appropriate behavior in these contexts and favor repeatedly over time and when discrimination behaviors directed toward particular individu- among multiple familiar individuals is benefi- als. From a functional perspective, the benefits cial, such as with nepotism, reciprocal altru- of social recognition are clear, yet the processes ism and dominance hierarchies (Hamilton 1964, underlying it can be quite complex. Trivers 1971). I define social recognition as a Kin recognition is an internal process of cognitive process (without implying any level assessing genetic relatedness that can be inferred 730 Mateo • ANN. ZOOL. FENNICI Vol. 41 through kin discrimination, the observable, dif- all are actually mechanisms for recognizing ferential treatment of conspecifics based on cues kin (as versus perceptual abilities serving some that correlate with relatedness. Recognition at other purpose), and whether distinctions between most levels of social organization (but not all; see mechanisms are largely conceptual rather than “Context-based recognition”, below) involves biologically relevant, as described below. Before three components: the expression of unique phe- proceeding, I note that these mechanisms are not notypic cues, or labels (also referred to as the mutually exclusive or necessarily exhaustive, ‘production’ component), the perception of these and that an individual can use several mecha- labels and their degree of correspondence with nisms depending on the recognition context. a “recognition template”, and the action taken by the animal (the ‘evaluator’) as a function of the perceived similarity between its template Context-based recognition and an encountered phenotype (or ‘cue-bearer’; Beecher 1982, Holmes & Sherman 1982, Reeve Similar to Barnard’s (1990) “discrimination by 1989, Gamboa et al. 1991, Sherman et al. 1997, non-conspecific cues”, I group together several Liebert & Starks 2004, Tsutsui 2004). Expression modes of discrimination which are based on and perception components comprise the mecha- contextual cues rather than cues borne by indi- nism of recognition, both of which are necessary viduals themselves. Previously I have focused for discrimination of conspecifics before the on spatial cues alone (Mateo 2002, 2003), but action component can be expressed, resulting recent studies suggest a need for an expansion of in differential treatment of conspecifics (e.g., this category. nepotism, mate choice, avoidance, cooperation). First, animals may be recognized indirectly However, social discrimination — of kin, neigh- based on spatial cues, with individuals encoun- bors, mates, allies, competitors, etc. — is not an tered in a particular area (e.g., nest or burrow) inevitable result of social recognition. treated as kin regardless of true relatedness (e.g., Thus recognition labels and perceptual abili- mother–offspring recognition via natal bur- ties provide proximate or mechanistic explana- rows; Holmes & Sherman 1982). During the tions for social recognition, whereas the action last two decades this mechanism has received component provides a functional or adaptive scant empirical attention, in part because some explanation for recognition because it involves (e.g., Barnard 1990; reviewed in Tang-Martinez behaviors with fitness costs or benefits (such as 2001) have suggested it is not a true, direct form agonism or avoidance of inbreeding). However, of kin recognition, since animals are responding it is important to note that natural selection (and to locations rather than phenotypes of individu- perhaps sexual selection) can operate independ- als. However, spatial cues may correlate reliably ently on each component of recognition, such with relatedness, as when females lay their eggs that if kin labels and perceptual abilities have not or give birth in a nest to which other individuals both evolved, differential treatment of individu- do not have access, and when communal nesting als cannot be selected regardless of how favora- and brood parasitism do not occur. Thus when ble it might be (Hamilton 1964; see also Holmes parents return to the nest, they by default invest & Mateo 2006). exclusively in their own offspring. Likewise, those young will only encounter their parents in that location, and so treating any adult found Mechanisms of kin recognition there as kin would be accurate. For example, bank swallow (Riparia riparia) parents use a The evolution of kin-selected behaviors of course spatially based mechanism to recognize their requires the evolution of mechanisms that make young confined to the nest and later switch recognition of kin possible (Hamilton 1964; see to a familiarity-based mechanism (described Table 1). Several mechanisms for the perception below) just before young fledge (Beecher et al. component of recognition have been described, 1981). Male black-tailed prairie dogs (Cynomys although there is disagreement about whether ludovicianus) appear to treat young-of-the-year ANN. ZOOL. FENNICI Vol. 41 • Perception component of kin-recognition mechanisms 731 differentially depending on whether young are Before young leave the nest and begin inter- encountered in an area where the male copulated acting with other conspecifics, spatially based (Hoogland 1995). recognition is an accurate and adaptive mecha- Table 1. Perceptual mechanisms of social recognition. Mechanism Contexts Type of cues Advantages Disadvantages Context- Spatial Kin (and only Location (nest, Family cues do Risk of mis- based cues kin) are reliably burrow, territory) not need to be identifying encountered in a learned non-kin particular area encountered in familiar location as kin Mating Social partner has Evaluator’s Directed parental Cuckolded access no opportunity to memory of investment in parent may mate with others exclusive offspring even if invest in mating with young do not non-kin target’s parent produce kin labels Cohort Young in a Age of Paternal half- Recognition sharing cohort sired by evaluator and siblings mistakes if one or a few target recognized many males adults without need successfully sire for production young or perception of kin labels Recognition Precise Cue-bearer’s 3 components Risk of treating alleles recognition phenotypic of recognition non-kin with without learning traits can evolve shared trait family traits together as kin Prior Short-lived, little Cue-bearer’s Can recognize May not be association overlap of phenotypic familiar kin able to generations, traits matched regardless of discriminate few social against location among familiar interactions; exemplars in individuals; little fitness evaluator’s cannot benefit for template recognize recognizing previously unfamiliar kin unfamiliar kin Phenotype Fitness benefits Cue-bearer’s Can recognize Liberal matching for recognizing phenotypic previously matching classes of traits matched unfamiliar kin algorithm may unfamiliar kin; to prototype lead to multiple mating derived from acceptance of by males creates referents in non-kin or unfamiliar evaluator’s rejection of kin paternal
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