Portal de Periódicos da CAPES

Behavioural Ecology: Promiscuous Fathers Sire Young that Recognize True Family

2006; Elsevier BV; Volume: 16; Issue: 18 Linguagem: Inglês

10.1016/j.cub.2006.08.036

1879-0445

Márk E. Hauber, Rebecca J. Safran,

Evolutionary Game Theory and Cooperation

Most theories of kin selection assume that animals are able to distinguish relatives from non-relatives. This is especially difficult in situations where mixed parentage precludes that relatedness is recognised by familiarity. Recent work shows that, within the same brood, young bluegill sunfish that are fathered by cuckolders — but not those sired by parental males — pick out their relatives using self-referent phenotype matching and not familiarity. Most theories of kin selection assume that animals are able to distinguish relatives from non-relatives. This is especially difficult in situations where mixed parentage precludes that relatedness is recognised by familiarity. Recent work shows that, within the same brood, young bluegill sunfish that are fathered by cuckolders — but not those sired by parental males — pick out their relatives using self-referent phenotype matching and not familiarity. The theory of kin selection revolutionised our understanding of animal sociality by demonstrating that an individual can gain genetic benefits by helping both its own progeny and/or a non-descendent kin [1Hamilton W.D. The genetical evolution of social behaviour - I & II.J. Theor. Biol. 1964; 7 (1–16 and 17–52)Google Scholar]. Accordingly, individuals can increase their inclusive fitness disproportionally, as by helping relatives they pass more copies of their own genes on to the next generation. But can individuals recognise kin that they had not met before? A new study by Hain and Neff [2Hain T.J.A. Neff B.D. Promiscuity drives self-referent kin recognition.Curr. Biol. 2006; 16: 1807-1811Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar] in this issue of Current Biology demonstrates that young bluegill sunfish (Lepomis macrochirus) seek out the company of unfamiliar relatives using chemical cues, despite having grown up in an unpredictable mix of mostly non-kin and some kin of varying relatedness. At the evolutionary level of analysis, kin selection theory predicts that cooperation among relatives has discernable evolutionary benefits [1Hamilton W.D. The genetical evolution of social behaviour - I & II.J. Theor. Biol. 1964; 7 (1–16 and 17–52)Google Scholar]. However, kin selection theory does not provide a predictive framework of when and how individuals should recognise relatives [3Sherman P.W. Reeve H.K. Pfennig D.W. Recognition systems.in: Krebs J.R. Davies N.B. Behavioural Ecology. Fourth edition. Blackwell Science, Malden, MA1997: 69-98Google Scholar]. Research into kin recognition systems, instead, has traditionally focused on understanding the rules and cues that govern the function and development of social affiliation. Konrad Lorenz's classic study [4Lorenz K. Der Kumpan in der Umwelt des Vogels.J. Ornithol. 1935; 83 (289–413): 137-213Crossref Scopus (464) Google Scholar] on filial imprinting is still an important motivation for recent studies on the development of social preferences, such as the establishment of social referents and extrapolation towards more general recognition templates for mate preferences of zebra finches (Taeniopygia guttata), published in Current Biology earlier this year [5ten Cate C. Verzijden M.N. Etman E. Sexual imprinting can induce sexual preferences for exaggerated parental traits.Curr. Biol. 2006; 16: 1128-1132Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar]. Familiarity appears to be a reliable social recognition cue in many species, including birds with ‘helpers at the nest’ [6Sharp S.P. McGowan A. Wood M.J. Hatchwell B.J. Learned kin recognition cues in a social bird.Nature. 2005; 434: 1127-1130Crossref PubMed Scopus (184) Google Scholar], where uncertainty about relatedness to parents and siblings is typically low [7Quinn J.S. Woolfenden G.E. Fitzpatrick J.W. White B.N. Multi-locus DNA fingerprinting supports genetic monogamy in Florida scrub-jays.Behav. Ecol. Sociobiol. 1999; 45: 1-10Crossref Scopus (64) Google Scholar]. But many social behaviours occur among strangers, suggesting that there must be mechanisms to recognise kinship beyond familiarity. In general, individuals can discriminate between relatives and non-relatives using two separate recognition mechanisms: direct recognition involves the discrimination of individuals based on phenotypic traits that reflect the underlying genetic similarity [8Hauber M.E. Sherman P.W. Self-referent phenotype matching: theoretical considerations and empirical evidence.Trends Neurosci. 2001; 24: 609-616Abstract Full Text Full Text PDF PubMed Scopus (259) Google Scholar]. Familiarity is one such direct recognition mechanism, when it can be assumed that familiar individuals are kin; another direct recognition mechanism is phenotype matching, whereby individuals are categorized as kin according to how well their phenotypic traits match the traits of a memorized or genetically determined recognition template, such as those learned from parents [3Sherman P.W. Reeve H.K. Pfennig D.W. Recognition systems.in: Krebs J.R. Davies N.B. Behavioural Ecology. Fourth edition. Blackwell Science, Malden, MA1997: 69-98Google Scholar]. Unlike familiarity, phenotype matching thus allows individuals to discriminate between kin and non-kin even without prior exposure: kin should reliably resemble the recognition template to a greater extent than non-kin. By contrast, indirect kin recognition involves affiliation with a group of individuals based on location or timing [3Sherman P.W. Reeve H.K. Pfennig D.W. Recognition systems.in: Krebs J.R. Davies N.B. Behavioural Ecology. Fourth edition. Blackwell Science, Malden, MA1997: 69-98Google Scholar, 8Hauber M.E. Sherman P.W. Self-referent phenotype matching: theoretical considerations and empirical evidence.Trends Neurosci. 2001; 24: 609-616Abstract Full Text Full Text PDF PubMed Scopus (259) Google Scholar]. For instance, during the parental feeding visits of eastern phoebes (Sayornis phoebe) to their young nestlings chicks are recognised as progeny based on their age (pre-fledging) and location (inside own nest) [9Kilner R.M. Madden J.R. Hauber M.E. Brood parasitic cowbird nestlings use host young to procure resources.Science. 2004; 305: 877-879Crossref PubMed Scopus (123) Google Scholar]. More recently, behavioural ecologists have begun to study the ontogeny of recognition systems in unpredictable social contexts [10Holmes W.G. Sherman P.W. The ontogeny of kin recognition in two species of ground squirrels.Amer. Zool. 1982; 22: 491-517Google Scholar]. Consider, for instance, how a brood parasite, such as the brown-headed cowbird (Molothrus ater), can recognise its own species when its early social environment consists of only host parents and nestmates that belong to a completely different species [11Göth A. Hauber M.E. Ecological approaches to species recognition in birds through studies of model and non-model species.Ann. Zool. Fenn. 2004; 41: 823-842Google Scholar]. Indirect recognition is not feasible for cowbirds, because typically only a single parasite chick grows up in the host nest. Familiarity with or phenotype matching of foster parents' and nestmates' traits would also misidentify conspecifics. Instead, as Hauber and colleagues [12Hauber M.E. Sherman P.W. Paprika D. Self-referent phenotype matching in a brood parasite: the armpit effect in brown-headed cowbirds (Molothrus ater).Anim. Cognit. 2000; 3: 113-117Crossref Scopus (65) Google Scholar] have shown, young cowbirds inspect their own traits and later associate with individuals who match these self-traits closely, even when the self-traits were experimentally manipulated. This recognition mechanism has been termed ‘the armpit effect’ by Richard Dawkins [13Dawkins R. The Extended Phenotype. W.H. Freeman, San Francisco, CA1982Google Scholar]. Theoretically, such self-referent phenotype matching may be evolutionarily advantageous in a wide range of contexts in which social cues are unreliable for inferring the genetic relatedness of familiar individuals (Box 1). In support of this prediction, self-referencing has been suggested to explain preferred association with relatives in lekking manakins (Manacus manacus) where siblings often hatch alone and are unlikely to interact until maturity, peacocks (Pavo cristatus), whose early social environment includes a mix of relatives and non-relatives, and golden hamsters (Mesocricetus auratus) that had been cross-fostered to unrelated mothers and littermates (reviewed in [8Hauber M.E. Sherman P.W. Self-referent phenotype matching: theoretical considerations and empirical evidence.Trends Neurosci. 2001; 24: 609-616Abstract Full Text Full Text PDF PubMed Scopus (259) Google Scholar]). There is even evidence for self-referencing in plants during competition between vegetatively propagated rootlets from the same original individual [14Gruntman M. Novoplansky A. Physiologically mediated self/non-self discrimination in roots.Proc. Natl. Acad. Sci. USA. 2004; 101: 3863-3867Crossref PubMed Scopus (169) Google Scholar]. In humans, self-referencing is likely to explain how women can discriminate between odour cues from men, with whom they do or do not share specific alleles of the MHC-system [15Jacob S. McClintock M.K. Zelano B. Ober C. Paternally inherited HLA alleles are associated with women's choice of male odor.Nat. Genet. 2002; 30: 175-179Crossref PubMed Scopus (318) Google Scholar]. Self-referencing has also been suggested to govern the paternal decision mechanisms to provide differential care in nesting bluegill sunfish: parental males who have been cuckolded provide less attention to broods than males who sired their full brood [16Neff B.D. Sherman P.W. In vitro fertilization reveals offspring recognition via self-referencing in a fish with paternal care and cuckoldry.Ethol. 2005; 111: 425-438Crossref Scopus (38) Google Scholar].Box 1Social systems that introduce genetic unpredictability between familiar individuals and predict the evolution kin recognition based on self-referent phenotype matching. Modified from [8Hauber M.E. Sherman P.W. Self-referent phenotype matching: theoretical considerations and empirical evidence.Trends Neurosci. 2001; 24: 609-616Abstract Full Text Full Text PDF PubMed Scopus (259) Google Scholar, 10Holmes W.G. Sherman P.W. The ontogeny of kin recognition in two species of ground squirrels.Amer. Zool. 1982; 22: 491-517Google Scholar].Extra-pair copulations and quasi parasitismBroods of full- and half-siblings reared together.Brood parasitismYoung of different relatedness reared together (from relatives, if parasites are kin, to non-relatives, if parasites are non-kin or heterospecifics).Interbrood aggregationYoung from different parents reared together, either through cooperative breeding, adoption/kidnapping or brood amalgamation.Spatial hotspotsKin and non-kin from different broods and generations aggregating for sexual displays (leks) and mate choice. Extra-pair copulations and quasi parasitism Broods of full- and half-siblings reared together. Brood parasitism Young of different relatedness reared together (from relatives, if parasites are kin, to non-relatives, if parasites are non-kin or heterospecifics). Interbrood aggregation Young from different parents reared together, either through cooperative breeding, adoption/kidnapping or brood amalgamation. Spatial hotspots Kin and non-kin from different broods and generations aggregating for sexual displays (leks) and mate choice. Bluegill sunfish have gained scientific fame through their variable breeding system: females do not provide maternal care, instead the males build nests and protect and care for the offspring (Figure 1). During mating, females visit nest-holding males and release eggs [17Gross M.R. Sneakers, satellites and parentals: polymorphic mating strategies in North American sunfishes Z.Tierpsychol. 1982; 60: 1-26Google Scholar]. In addition to these sex-role reversed couples, some male bluegills have developed yet a different mating strategy: cuckolders steal reproductive success from nest-building males by fertilising eggs after release by the female [17Gross M.R. Sneakers, satellites and parentals: polymorphic mating strategies in North American sunfishes Z.Tierpsychol. 1982; 60: 1-26Google Scholar]. Consequently, cuckolders invest more heavily into sperm production and avoid the costs of nestbuilding and paternal care. A consequence of this reproductive strategy is that most broods will be derived from different fathers. As nest-building males also have multiple female partners, the relatedness of a brood of bluegill sunfish in a given nest is highly variable. Only recently have questions about interaction between kin uncertainty and the mechanisms of social recognition systems been described in the context of mate choice, paternal care and kin discrimination [18Neff B.D. Decisions about parental care in response to perceived paternity.Nature. 2003; 422: 716-719Crossref PubMed Scopus (126) Google Scholar]. In particular, genetic analyses revealed that parental blue-gill males and their multiple female partners sire most young in the nest, creating cohorts of full- and half-sibs, while the progeny of any cuckolder are surrounded by mostly unrelated individuals as well as some half and full sibs [2Hain T.J.A. Neff B.D. Promiscuity drives self-referent kin recognition.Curr. Biol. 2006; 16: 1807-1811Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar]. As such, one nest hosts a veritable cocktail of genotypes from several males and females which means that finding your relatives is not an easy task. Still, the effort may have important pay-offs because interactions with kin can lead to increased efficiency in foraging and more rapid growth rates [2Hain T.J.A. Neff B.D. Promiscuity drives self-referent kin recognition.Curr. Biol. 2006; 16: 1807-1811Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar]. In a series of carefully detailed choice tests Hain and Neff [2Hain T.J.A. Neff B.D. Promiscuity drives self-referent kin recognition.Curr. Biol. 2006; 16: 1807-1811Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar] demonstrate that the progeny of cuckolder males show consistent spatial preferences for chemical cues from unfamiliar relatives compared to unfamiliar non-relatives. The source of these phenotypic cues and the sensory systems of progeny involved in perceiving the cues are yet to be uncovered. Nonetheless, the progeny of cuckolder males show a consistent behavioural association with kin, even when they had been reared in a mixed-paternity brood of one cuckolder and one parental male. These kin-directed behaviours of the progeny of cuckholder males are in contrast with those of the progeny of parental males, which do not show preferences for association with kin in the same choice tests. Although the lack of behavioural discrimination does not imply lack of recognition or perceptual discrimination [19Mateo J.M. Kin recognition abilities and nepotism as a function of sociality.Proc. Roy. Soc. B. 2002; 269: 721-727Crossref PubMed Scopus (115) Google Scholar], the observed behavioural differences between parental and cuckolder offspring under the same experimental conditions clearly imply that different decision rules govern the affiliations of these fish. Offspring of neither type of male show discrimination between familiar and unfamiliar kin, indicating that generally familiarity plays no major role in kin discrimination in the bluegill. While this work follows other recent work on self-referent phenotype matching as an important mechanism for kin recognition [8Hauber M.E. Sherman P.W. Self-referent phenotype matching: theoretical considerations and empirical evidence.Trends Neurosci. 2001; 24: 609-616Abstract Full Text Full Text PDF PubMed Scopus (259) Google Scholar], the authors take advantage of the external fertilization of bluegills and use in vitro methods to be the first to remove the possibility of in utero learning or indirect recognition between broodmates. Using microsatellite data on relatedness of brood mates in natural nests, the authors are also able to quantify the evolutionary benefits of kin discrimination in bluegill sunfish: by using self-referencing — rather than familiarity — to associate with kin, the progeny of promiscuous males may increase their fitness by a factor of four. Although ecologists had considered the diversity of the social contexts in which self-referencing may occur (Box 1), a further insight derived from this new work is that different cognitive decision rules are being used within one species, depending on the reproductive strategy of the father. What remains to be uncovered is whether the genomic and ecological control mechanisms that are involved in determining male breeding strategies are also involved in shaping the cognitive architecture of the progeny of males from either reproductive tactic. As is the case for many complex social systems, such as that of the bluegill sunfish, familiarity alone will not solve the problem of discerning kin from non-kin. Broods of mixed paternity appear to be the rule and not the exception [20Mays Jr., H.L. Hill G.E. Choosing mats: genes that are good versus genes that are a good fit.Trends in Ecol. Evol. 2004; 19: 554-559Abstract Full Text Full Text PDF PubMed Scopus (302) Google Scholar] and while there is mounting evidence that mating decisions are based on genomic recognition, we lack a basic understanding of the mechanisms that underlie these associations. We thus await experimentation on the role of self-referent phenotype matching not only in the context of cooperation among siblings, where related individuals are predicted to be present, but also within the ecology of optimal outbreeding through mate choice, and in the contexts of social transactions at large.