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Rethinking Recognition: Social Context in Adult Life Rather Than Early Experience Shapes Recognition in a Social Wasp

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Rethinking Recognition: Social Context in Adult Life Rather Than Early Experience Shapes Recognition in a Social Wasp Submitted to Phil. Trans. R. Soc. B - Issue Rethinking recognition: social context in adult life rather than early experience shapes recognition in a social wasp Journal: Philosophical Transactions B Manuscript ID RSTB-2019-0468.R1 Article Type:ForResearch Review Only Date Submitted by the 20-Feb-2020 Author: Complete List of Authors: Cappa, Federico; Università degli Studi di Firenze Cini, Alessandro; University College London Signorotti, Lisa; Università degli Studi di Firenze, Dipartmento di Biologia CERVO, Rita; Università degli Studi di Firenze, Biologia ; Issue Code (this should have already been entered but SIGNAL please contact the Editorial Office if it is not present): Subject: Behaviour < BIOLOGY ontogeny of recognition, referent template, nestmate recognition, social Keywords: insects, Polistes http://mc.manuscriptcentral.com/issue-ptrsb Page 1 of 25 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 3 Author-supplied statements 4 5 6 Relevant information will appear here if provided. 7 8 Ethics 9 10 Does your article include research that required ethical approval or permits?: 11 Yes 12 13 Statement (if applicable): 14 Wasps used in this work were reared under laboratory conditions and treated as well as possible 15 16 given the constraints of the experimental design. This study was carried out in accordance with the 17 Italian guidelines on animal wellness. 18 19 Data 20 21 It is a condition of publicationFor that data, Review code and materials Only supporting your paper are made publicly 22 available. Does your paper present new data?: 23 Yes 24 25 26 Statement (if applicable): 27 The datasets supporting this article have been uploaded as part of the Supplementary Material. 28 29 Conflict of interest 30 31 I/We declare we have no competing interests 32 33 Statement (if applicable): 34 35 CUST_STATE_CONFLICT :No data available. 36 37 Authors’ contributions 38 39 This paper has multiple authors and our individual contributions were as below 40 41 Statement (if applicable): 42 FC, RC and LS conceived and designed the study. FC and RC performed the experiments. AC carried 43 44 out data analyses. RC provided materials and facilities. FC drafted the manuscript and all authors 45 corrected, read and approved the final version of the manuscript. 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 http://mc.manuscriptcentral.com/issue-ptrsb Submitted to Phil. Trans. R. Soc. B - Issue Page 2 of 25 1 2 3 4 1 Rethinking recognition: social context in adult life rather than early 5 2 experience shapes recognition in a social wasp 6 3 Federico Cappa1, Alessandro Cini1, 2, Lisa Signorotti1, Rita Cervo1 7 4 8 5 1Dipartimento di Biologia, Università di Firenze, Firenze, Italy 9 6 2Centre for Biodiversity and Environment Research, University College London, London, 10 7 United Kingdom 11 8 12 9 13 10 14 11 Abstract 15 12 Social recognition represents the foundation of social living. To what extent is social recognition 16 17 13 hard-determined by early-life experience or flexible and influenced by social context of later life- 18 19 14 stages is a crucial question in animal behaviour studies. Social insects have represented classic model 20 15 to investigate the subject, and the acknowledged idea is that relevant information to create the referent 21 For Review Only 22 16 template for nestmate recognition (NMR) is usually acquired during an early sensitive period in adult 23 24 17 life. Experimental evidence, however, highlighted that also other processes may be at work in creating 25 18 the template, and that such a template may be updated during adult life according to social 26 27 19 requirements. However, currently we lack an ad hoc experiment testing the alternative hypotheses at 28 29 20 the basis NMR ontogeny in social insects. Thus, to investigate the mechanisms underlying the 30 31 21 ontogeny of NMR in Polistes wasps, a model genus in recognition studies, and their different role in 32 22 determining recognition abilities, we subjected Polistes dominula workers to different olfactory 33 34 23 experiences in different phases of their life before inserting them into the social environment of a 35 36 24 novel colony and testing them in recognition bioassays. Our results show that workers develop their 37 38 25 NMR abilities based on their social context rather than through preimaginal and early learning or 39 26 self-referencing. Our study demonstrates, for the first time, that the social context represents the major 40 41 27 component shaping recognition abilities in a social wasp, therefore shedding new light on the 42 43 28 ontogeny of recognition in paper wasps and prompting the reader to rethink about the traditional 44 29 knowledge at the basis of the recognition in social insects. 45 46 30 47 48 31 Keywords: ontogeny of recognition, referent template, nestmate recognition, social insects, Polistes 49 50 32 51 33 INTRODUCTION 52 34 53 35 Understanding the timing and cues of social recognition 54 55 36 Recognition represents the essential foundation of animal interactions. From sexual 56 57 58 37 encounters between potential partners to the most complex animal societies, each individual has to 59 60 38 recognize the ones encountered in order to decide how to behave towards them. Recognition occurs http://mc.manuscriptcentral.com/issue-ptrsb Page 3 of 25 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 3 39 when specific phenotypic cues, or labels, expressed by an individual (’cue-bearer’) are perceived by 4 5 6 40 another individual (‘evaluator’) and then compared with an internal “referent template” of the latter 7 8 41 [1-4]. According to the degree of correspondence between the encountered phenotype labels and the 9 10 42 referent template, the evaluator performs the consequent recognition action, ranging from strong 11 12 43 rejection to complete acceptance [1-5]. Given the spread and importance of recognition processes, 13 14 15 44 the mechanisms at their basis have been extensively studied over the years both in vertebrates and 16 17 45 invertebrates [2-8]. 18 19 46 As regards the nature of the cues potentially used by animals to create their template and 20 21 For Review Only 22 47 compare the phenotype of others, different sensory channels are often involved depending on the 23 24 48 species and the different recognition contexts [9-12]. Discrimination can occur through the use of 25 26 49 environmental (e.g. nest odour) or genetic cues: animals can learn their own phenotypes (self-referent 27 28 50 phenotype matching) or those of their relatives, and later compare the phenotypes of unknown 29 30 31 51 individuals to this learned recognition template [2-5,7,8,13] . 32 33 52 Various processes explain when and how an animal acquires the crucial cues to create a 34 35 53 template and perform correct phenotypic comparisons [2-5,14-17]. In particular, early experience 36 37 38 54 coupled with a short sensitive period has been claimed to be a common and widespread evolutionary 39 40 55 strategy to restrict the storage of biologically relevant information to a precocious developmental 41 42 56 stage of the individual, thus reducing the risks of future recognition errors [15,17-21]. From the 43 44 45 57 pioneer work of Konrad Lorenz [22] to the wide body of following research, early experience leading 46 47 58 to imprinting-like phenomena appeared to play a major role in shaping recognition in animals [15,18- 48 49 59 21,23-25]. Information acquired during an early sensitive window for learning are used by individuals 50 51 60 across different contexts, to recognize parents and offspring [21,26,27], to discriminate kin from non- 52 53 54 61 kin [28,29], to choose a sexual partner of the same species [24,30-33] and to select the most profitable 55 56 62 food source [34-36]. In more recent years, however, a growing attention has also been devoted to the 57 58 63 importance of the social surroundings of an animal, especially for those species living in socially 59 60 64 structured groups, for the development of efficient recognition systems, with different studies http://mc.manuscriptcentral.com/issue-ptrsb Submitted to Phil. Trans. R. Soc. B - Issue Page 4 of 25 1 2 3 65 highlighting that in impoverished social circumstances individuals struggle to develop adequate 4 5 6 66 recognition patterns [19,37-41]. In both vertebrates [37-39] and invertebrates [40,41] social isolation 7 8 67 affects or impairs the individual ability to recognize other group members. 9 10 68 A social group is usually a highly complex environment, which can change over time both in 11 12 69 the composition and social role of their members, and recognition processes appear to be finely 13 14 15 70 entwined to the social network of interactions that an individual experiences through its life [42,43]. 16 17 71 Given the plasticity in the structure of many social environments [44-46], it may be evolutionary 18 19 72 advantageous that group members should reflect a certain degree of plasticity in their recognition 20 21 For Review Only 22 73 system with the ability to adjust or update their templates based on contextual contingencies 23 24 74 [42,43,47]. For example, in many social insect species, the colony odour is dynamic and can change 25 26 75 over time due to multiple factors (i.e. colony age, usurpation or replacement of the dominant 27 28 76 individuals, colony relocation to a new nesting site, social interactions and cues exchanges among 29 30 31 77 colony members, presence of parasites or pathogens, etc.) [48-56], therefore, for the recognition 32 33 78 system to maintain its efficacy, at least in some species, individuals should be able to update their 34 35 79 template during their life [43,47].
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