UMD BIOL 608W - Kin recognition in the ant Formica fusca

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Are you my mother? Kin recognition in the ant Formica fuscaS. EL-SHOWK*, J. S. VAN ZWEDEN!, P. D’ETTORRE! & L. SUNDSTRO¨M**Department of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland!Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, DenmarkIntroductionIn group-living animals, reliable parent–offspring recog-nition systems are expected to evolve (e.g. Beecher, 1991),as this decreases the risk that a parent will direct care tounrelated young and prevents the offspring from receivingaggressive behaviour from unrelated adults. Precisemother-offspring recognition, based on different commu-nication channels, is well documented in many animals,from reptiles (e.g. lizards, Main & Bull, 1996) to birds (e.g.swallows, Leonard et al., 1997; penguins, Searby et al.,2004) and mammals (e.g. humans, Porter, 1991; sheep,Searby & Jouventin, 2003). Although mutual recognitionis beneficial to both parties, parent–offspring conflicttheory (Trivers, 1974) predicts that the young should beunder stronger selection to develop recognition abilitiestowards their parents as failing to do so would increaseoffspring mortality. Indeed, pups of northern fur sealshave been shown to put more effort in the reunion processwith their mothers than vice versa (Insley, 2001).In social insects, workers trade personal reproductionfor indirect fitness returns from helping their mother torear collateral kin (Hamilton, 1964a,b; Trivers & Hare,1976). Colony membership is generally used as a proxyfor discriminating between kin and nonkin. Failure todiscriminate colony members (i.e. their mother queenand ⁄ or her offspring) from unrelated hetero-colonialindividuals (i.e. individuals from a different colony), andconsequently exclude intruders, will significantly reducethe inclusive fitness returns from helping. In the extremecase, social parasites are able to enter the colonyexploiting the host worker force to rear their own young(Lenoir et al., 2001). The process of recognition isthought to involve matching a specific set of detectedcues (the label) against a neural representation of thesecues (the template), both of which may compriseenvironmentally and genetically determined compo-nents (e.g. Hepper, 1991; Lenoir et al., 1999). Recogni-tion in social insects is mainly mediated by chemicalcompounds, mostly cuticular hydrocarbons (Lahav et al.,1999; Wagner et al., 2000; Guerrieri et al., 2009). Lenoiret al. (1999) suggested that template acquisition and labeldevelopment are facilitated by a lack of hydrocarbons onnewly emerged individuals (callows). This is followed bya period of chemical integration, when callows learn theCorrespondence: Jelle S. van Zweden, Centre for Social Evolution,Department of Biology, University of Copenhagen,Universitetsparken 15, 2100 Copenhagen, Denmark.Tel.: +45 35 32 12 38; fax: +45 35 32 12 50;e-mail: [email protected]ª 2 0 0 9 T H E A U T H O R S . J . E V O L . B I O L . 23 ( 2 0 1 0 ) 3 9 7 – 4 0 6J O U R N A L C O M P I L A T I O N ª 2 0 0 9 E U R O P E A N S O C I E T Y F O R E V O L U T I O N A R Y B I O L O G Y397Keywords:cross-fostering;cuticular hydrocarbons;parent–offspring recognition;social insects.AbstractIn social insects, workers trade personal reproduction for indirect fitnessreturns from helping their mother rear collateral kin. Colony membership isgenerally used as a proxy for kin discrimination, but the question remainswhether recognition allows workers to discriminate between kin and nonkinregardless of colony affiliation. We investigated whether workers of the antFormica fusca can identify their mother when fostered with their mother, theirsisters, a hetero-colonial queen or hetero-colonial workers. We found thatworkers always displayed less aggression towards both their mother and theirfoster queen, as compared to an unfamiliar hetero-colonial queen. In supportof this finding, workers maintain their colony hydrocarbon profile regardlessof foster regime, yet show modifications when exposed to different environ-ments. This indicates that recognition entails environmental and geneticcomponents, which allow both discrimination of kin in the absence of priorcontact and learning of recognition cues based on group membership.doi:10.1111/j.1420-9101.2009.01912.xcolony odour and attain their own hydrocarbon profilethrough synthesis, grooming and the exchange of liquidfood.Between-colony recognition has been well establishedby several studies (reviewed in Lenoir et al., 1999; vanZweden & d’Ettorre, in press). The question remains,though, whether genetically determined cues, effectivelygenerating individual signatures, alone are sufficient forrecognition, e.g. whether worker ants can recognizerelatives despite being raised by unrelated individuals.Such recognition would require a strong enough geneticcomponent and would represent true kin recognition(sensu Grafen, 1990). However, theory predicts thatselection tends to erode cue diversity in genetic recogni-tion systems, as this allows within-colony nepotisticbehaviour and, hence, social disruption (Keller, 1997;Boomsma et al., 2003; Dani et al., 2004). This mayexplain why within-colony kin recognition has beennotoriously difficult to demonstrate in social Hymenop-tera (De Heer & Ross, 1997; Strassmann et al., 2000;Goodisman et al., 2007; but see Hannonen & Sundstro¨m,2003). Nonetheless, extrinsic selection pressures maymaintain cue diversity, thereby catering for the mainte-nance of a genetic recognition system (Rousset & Roze,2007). Social parasitism, wherein queens enter hetero-specific host colonies and exploit these, may provide onesuch extrinsic selection force by selecting for enhancedrecognition abilities in host species, and consequently themaintenance of high diversity in recognition cues.The ant Formica fusca has previously been used to studyrecognition systems, both with respect to colony closureand brood recognition (Wallis, 1962; Helantera¨&Sundstro¨m, 2005). The species is also subject to extensivetemporary social parasitism by ants of the Formica rufas.str. group. Parasitized colonies die within a year(Collingwood, 1979; Czechowski et al., 2002), and thisis likely to select for enhanced recognition abilities.Hannonen & Sundstro¨m (2003) found evidence forworkers favouring closely related brood over less relatedbrood in multi-queen colonies. Workers of this speciesalso discriminate against eggs laid by hetero-colonialqueens


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