Résultat de la recherche
On potential cooperation in predator-prey interactions in fishes
L'interaction prédateur-proie fournit le contexte de certains des cas de coopération les mieux étudiés. Certaines espèces de prédateurs peuvent chasser ensemble et coordonner leurs mouvements dans des rôles actifs et divers pour augmenter les taux de capture de leurs proies ; c'est ce qu'on appelle la chasse coopérative. Les poissons-lions sont des piscivores communs dans l'Indo-Pacifique et envahissants dans les Caraïbes. Étant donné que les poissons-lions chassent seuls par nature, une étude d'un ancien chercheur qui a démontré un recrutement actif, une coordination et une frappe alternée (peut-être réciproque) chez le poisson-lion nain Dendrochirus zebra a suscité beaucoup d'intérêt. On a vu que le poisson-lion zèbre utilise un motif d'évasement des nageoires qui implique une ondulation de la nageoire caudale et des évasements successifs des deux nageoires pectorales pour indiquer le début de la chasse coopérative. Les résultats suggèrent que la capacité de chasser en coopération peut avoir contribué au succès d'une espèce sœur de poisson-lion, Pterois miles et P. volitans, à envahir les Caraïbes.
Ici, j'ai étudié Pterois miles - l'une des espèces envahissantes - dans son aire de répartition naturelle en mer Rouge. Sur le terrain, je n'ai trouvé aucun signe de chasse coordonnée. J'ai complété les observations de terrain par une expérience en laboratoire, dans laquelle j'ai exposé des individus à un éventuel partenaire de chasse et à des proies inaccessibles dans un logement transparent. J'ai observé le schéma d'évasement des nageoires, mais il est essentiel de noter que le partenaire n'était pas la cible de ce signal d'évasement des nageoires. Les découvertes sur le terrain selon lesquelles cette espèce de la mer Rouge ne dépend pas de la chasse coopérative pour attraper du poisson sont également appuyées par le fait que les deux poissons-lions ne se sont pas rassemblés dans les zones de proies. J'ai en outre étayé ces résultats en examinant les mouvements coordonnés et l'alternance des frappes pendant la chasse. J'ai exposé des sujets d'appariements de P. miles à des proies inaccessibles dans trois logements clairs. En présence de proies, les deux poissons-lions ne se sont pas rassemblés dans la même maison de proies dans l'espace ou dans le temps. Dans une deuxième expérience, j'ai mis des morceaux de nourriture sur un bâton "d'arbre à nourrir" pour tester l'alternance réciproque des frappes. J'ai généralement vu moins d'alternances que prévu par hasard, et j'ai découvert que les alternances peuvent être augmentées en mettant des contraintes sur la monopolisation individuelle de la nourriture.
En conclusion, le modèle de mouvement d'évasement des nageoires observé chez l'espèce sœur de la mer Rouge, P. miles, qui était auparavant considéré comme un signal, était maintenant interprété comme un mode de nage. De plus, les paires de milles P. dans la mer Rouge n'alternaient pas réciproquement leurs frappes. J'ai interprété le résultat de l'étude précédente de D. zebra qu'une certaine alternance pourrait être générée si les proies devenaient alternativement disponibles à deux coins dans un espace confiné, chaque poisson-lion préférant monopoliser un coin chacun.
Finalement, en raison de certains défis rencontrés dans l'étude originale, qui m'ont empêché de mener des recherches plus empiriques, j'ai complété les chapitres empiriques de la thèse de doctorat avec une revue de recherche sur les perspectives de l'inspection des prédateurs chez les poissons. Le sujet a été choisi parce que l'inspection des prédateurs est un autre exemple classique de coopération. Cet examen a examiné les objectifs et les fonctions possibles des poissons proies inspectant les prédateurs potentiels et la manière dont les proies les approchent en fonction des objectifs d'inspection. Nous avons discuté de l'évaluation des motivations des proies et des indicateurs qui sont passés de la présence de prédateurs et des indicateurs d'état qui pourraient montrer pourquoi une attaque a été faite. Nous avons également discuté des types de jeux impliqués dans le comportement d'inspection des prédateurs. L'examen a identifié plusieurs lacunes importantes dans nos connaissances qui empêchent actuellement une évaluation appropriée des jeux de coopération qui pourraient s'appliquer.
Abstract
Predator – prey interaction provide the context for some of the best-studied cases of cooperation. Some predator species can hunt together and coordinate their moves within active and diverse roles to increase capture rates of their prey; this is known as cooperative hunting. Lionfish are common piscivores in the Indo-Pacific and invasive in the Caribbean. Since lionfishes hunt alone by nature, a study by a former researcher that demonstrated active recruitment, coordination, and alternated (perhaps reciprocal) striking in the dwarf lionfish Dendrochirus zebra has attracted much interest. Zebra lionfish have been seen to use a fin-flaring pattern that involves undulation of the caudal fin and successive flares of both pectoral fins to indicate the start of cooperative hunting. The findings suggested that the ability to hunt cooperatively may have contributed to the success of a sister lionfish species, Pterois miles and P. volitans, in invading the Caribbean.
Here, I investigated Pterois miles - one of the invasive species - in its natural range in the Red Sea. In the field, I found no signs of coordinated hunting. I supplemented field observations with a laboratory experiment, in which I exposed individuals to a possible hunting partner and inaccessible prey in a transparent housing. I observed the fin-flaring pattern, but it is vital to note that the partner was not the target of this fin-flaring signal. Also supporting the field findings that this species in the Red Sea does not rely on cooperative hunting to catch fish is the result that the two lionfish did not congregate at the prey patches. I further supported these findings by examining coordinated movement and strike alternation during hunting. I exposed subjects of P. miles pairings to inaccessible prey in three clear housings. In the presence of prey, the two lionfish did not congregate at the same prey house in space or time. In a second experiment, I put food pieces on a "feeding tree" stick to test for reciprocal alternation of strikes. I generally saw fewer alternations than expected by chance, and found that alternations can be increased by putting constaints on individual monopolization of food.
In conclusion, the fin flaring movement pattern seen in the Red Sea sister species P. miles that were previously thought to be a signal was now interpreted as a swimming mode. Additionally, pairs of P. miles in the Red Sea did not reciprocally alternate their strikes. I interpreted the result of the previous study of D. zebra that some alternation might be generated if prey items become alternately available at two corners in a confined space, with each lionfish preferring to monopolize one corner each.
Eventually, due to some challenges encountered in the original study, which prevented me from conducting more empirical research, I complimented the empirical chapters of the PhD thesis with a research review on the perspectives of predator inspection in fishes. The topic was chosen because predator inspection is another classic example of cooperation. This review looked at the possible goals and functions of prey fishes inspecting potential predators and how prey approach them based on the inspection goals. We discussed the assessment of prey motivations and indicators that moved from predator presence and state indicators that could show why an attack was made. Also, we discussed what types of games are involved in predator inspection behaviour. The review identified several important gaps in our knowledge that currently prevent a proper assessment of what cooperation games might apply.
In conclusion, the thesis demonstrates that it is an important scientific task to revisit apparently well-established examples and to challenge previous interpretations.
Collaborative hunting in the yellow saddle goatfish (Parupeneus cyclostomus)
Cooperation is of great interdisciplinary interest because we need to reconcile its occurrence with evolutionary theory and its emphasis on self-regarding individuals. Group hunting in various vertebrates has attracted much and continued attention from researchers because it provides the opportunity to study the evolution and stability of cooperation, the potential links between cooperation and cognitive abilities. Until now, all studies on coordinated hunting have been field observations and are hence correlative. Therefore, many conclusions are rather preliminary, like the repeatedly observed positive correlation between group size and hunting success as evidence for cooperation. In my PhD-thesis I conducted an unprecedented experimental study using yellow saddle goatfish (Parupeneus cyclostomus) as a study species. Yellow saddle goatfish are the first fish species described to be collaborative hunters. Individuals play different roles during a hunt (‘chasers’ and ‘blockers’), encircling prey hiding in coral crevices and trying to pry it out with means of inserting their barbels. I designed an experimental set-up in which the yellow saddle goatfish were confronted with a) mock prey that was pulled towards a shelter with multiple entrances; b) lively mobile prey hiding in an artificial coral reef. Cameras which were installed above and below allowed me to conduct detailed behavioural analyses i) to find out which decision rules underlie collaborative hunting in the yellow saddle goatfish; ii) to test the relationship between group size and hunting success; iii) to find out which payoff matrix conforms best to the hunting scenario when yellow saddle goatfish try to pry out the prey hidden in the shelter. The findings of my first chapter demonstrate that collaborative hunting in yellow saddle goatfish is based on simple, distance-based, self-serving decision rules. The individual that first detected the moving mock-prey always initiated a direct pursuit. Similarly, goatfish that were second to react in our experiments directly pursued the prey in almost all trials when they were in close proximity to the initiator. However, when lagging behind the initiator, the follower opted for a longer, less direct path to the prey. In the second chapter I showed that overall hunting efficiency (probability and speed of catching prey) is a function of group size. Larger groups of yellow saddle goatfish performed better and generally caught prey faster than smaller groups did. Groups of all sizes (2-4 individuals) were significantly more successful and faster than singleton hunters. Furthermore, I demonstrated that efficiency as singleton hunters did not predict hunting success when in a group. However, with my experimental set-up I could not address the question of how net calorie intake is affected by group size, as singleton success rate was already much higher than success rates observed in nature. The findings of my third chapter, where I investigated on how yellow saddle goatfish behave in order to pry out the hidden prey from the coral rock, demonstrate that actions were mainly maintained in order to obtain immediate benefits. Only the first barbel insertion decreased immediate benefits to the actor and created a public good resulting in payoff matrices similar to Snowdrift (2 players) and Volunteer’s Dilemma (N-players) games. However, further insertion effort did not lower capture probability, which even increased for the individuals that touched the prey first. Hence, besides being the first to insert, barbel-insertion can be considered as self-serving. Barbel insertion effort decreased from the singleton to the group hunting level and remained constant from 2-player to N-player situations, a finding which stands in contrast to theoretical predictions. These would expect a decline in the described situations, however under the assumption that the entire game is a Snowdrift/Volunteer’s Dilemma game. Interestingly, I could not find a correlation between insertion effort from singleton to group hunts, meaning that individuals seem to adjust their behaviour independently from whether they hunt alone or with others. In conclusion, the results of my PhD-thesis show that yellow saddle goatfish predominantly hunt self-servingly by following strategies which underlie simple decision rules. Overall, I propose that seemingly complex cooperation / collaboration can be based on simple rules. The challenge for researchers studying large-brained species is hence to test whether larger brains lead to more complex decision rules or whether collaborative hunting is generally a rather simple story.
The ecology underlying decision rules of bluestreak cleaner wrasse during client interactions
La coopération est définie comme un «comportement d'aide» qui offre des avantages directs à d'autres individus. Un tel comportement a longtemps intrigué les biologistes car il pose un problème pour la théorie évolutive classique : pourquoi un individu devrait-il effectuer un comportement qui bénéficie un autre individu plutôt que lui-même? En effet, un vaste ensemble de travaux sur la théorie des jeux évolutifs ainsi que des études empiriques ont depuis identifié de nombreux mécanismes qui expliquent le maintien d’une coopération stable entre des individus non apparentés. Cependant, le comportement humain ne correspond souvent pas aux stratégies optimales prédites par les modèles théoriques, d’où la nécessité de comprendre les processus de prises de décisions. Par exemple, l'utilisation de raccourcis de décision, correspondant à une heuristique connue (ou d'une règle empirique dans le cas des animaux non-humains), permet aux individus de prendre des décisions rapides et précises dans des situations auxquels ils sont fréquemment confrontés. Par contre, ces raccourcis peuvent conduire à des comportements sub-optimaux dans des contextes nouveaux. Les contraintes cognitives, telles que les capacités d'apprentissage ou l'incapacité à identifier les indices environnementaux ou sociaux pertinents, peuvent également entraîner des différences par rapport au comportement prédit.
En étudiant le labre nettoyeur (Labroides dimidiatus) comme modèle, cette thèse avait pour objectifs : 1) d'étudier les importantes disparités entre les données expérimentales et les prévisions théoriques standard concernant les décisions animales lors d’interactions coopératives; et 2) d’explorer la façon dont les nettoyeurs sont en mesure de facilement identifier et utiliser des repères pertinents pour la prise de décision. Les nettoyeurs participent à des interactions mutualistes avec des poissons de récifs coralliens appelés «clients» qui viennent les visiter dans leur territoire afin de se faire déparasiter. Cependant les nettoyeurs préfèrent se comporter en parasites et tricher en se nourrissant du mucus des clients qui est riche en azote plutôt que de leurs parasites. Par conséquent, pour encourager les nettoyeurs à être coopératifs, les clients utilisent divers mécanismes de contrôle tels que la punition et le changement de partenaire. Ce mutualisme entre nettoyeurs et clients a jusqu'ici fourni de solides preuves empiriques soutenant l’usage de la théorie des jeux évolutifs pour prédire le comportement coopératif.
Dans le chapitre 2, je démontre que les nettoyeurs qui proviennent de récifs caractérisés par une structure sociale complexe surpassent largement les nettoyeurs provenant de récifs caractérisés par une structure sociale simple lors d’expériences classiques de coopération et de cognition. Les récifs « simples » sont caractérisés par une abondance et une diversité de clients moindre ainsi qu'une plus faible densité de nettoyeurs par rapport aux récifs « complexes ». Mes expériences démontrent que les nettoyeurs provenant d’environnements simples ne réussissent généralement pas à: 1) se nourrir contre leur préférence, 2) adapter leur comportement coopératif en présence d'un observateur et 3) offrir systématiquement la priorité à une source de nourriture temporaire plutôt qu’à une source de nourriture permanente. Ces résultats contrastent fortement avec les données publiées sur des comportements de recherche de nourriture dans des expériences en laboratoire traditionnelles. Pour mieux comprendre ces disparités, j'ai étudié dans le chapitre 3 si les deux groupes de nettoyeurs utilisent des indices différents lors de la prise de décisions au moment où ils vont se nourrir, particulièrement en ce qui concerne la priorité offerte aux clients. Les nettoyeurs provenant d'environnements socialement complexes sont capables de trouver un repère précis lors de la prise de décision, conduisant à une plus grande précision dans les tâches en laboratoire. Par contre, les nettoyeurs provenant d'environnements socialement simples utilisent une règle de base qui conduit à une performance plus faible lors de la même tâche.
Dans le chapitre 4, j'ai déterminé que les règles appliquées par les deux groupes de nettoyeurs en milieu naturel semblent être adaptées à leur habitat respectifs et que les contraintes cognitives des nettoyeurs de l'environnement socialement simple étaient spécifiques au contexte dans lequel ils vivent et dues au fait que la santé des nettoyeurs et leur performance cognitive dans un tâche abstraite ne diffèrent pas entre les deux groupes. Finalement, dans le chapitre 5, j'ai étudié la façon dont les nettoyeurs sont en mesure d'extraire des indices pertinents pour les décisions impliquant la tricherie et la recherche de refuge. J'ai démontré que la capacité des nettoyeurs à généraliser la reconnaissance de différentes espèces de prédateurs dans un contexte d'outil social. Cependant, cette capacité disparait lorsque les nettoyeurs sont testés dans un contexte abstrait.
Les résultats de cette thèse ont des retombées importantes pour faire avancer notre compréhension de la cognition chez les animaux et de la théorie des jeux évolutifs. Les résultats sont discutés en soulignant l’importance de l'approche écologique de la cognition et en suggérant des possibilités d’amélioration des modèles théoriques sur la question., Cooperation is defined as a ‘helping’ behaviour that provides direct fitness benefits to other individuals. Such behaviours have long intrigued biologists, as it poses a problem for classic evolutionary theory, i.e. why should an individual perform a behaviour that is beneficial to other individuals? Indeed, an expansive body of work on evolutionary game theory, as well as, empirical studies, have provided many mechanisms for promoting stable cooperation between unrelated individuals. Humans, however, often deviate from the optimal strategies predicted by theoretical models, which has emphasized the need to understand decision making processes. For example, the use of decision short cuts, known heuristics (or rules of thumb in non-human animals), allows individuals to make decisions quickly and accurately in frequently occurring situations, but may lead to less than optimal behaviour in novel contexts. Additionally, cognitive constraints, such as learning capabilities or failure to identify relevant environmental or social cues, may also cause deviations from predicated behaviour.
Using bluestreak ‘cleaner’ wrasse (Labroides dimidiatus) as a model system, the primary aims of this PhD thesis were 1) to investigate important mismatches between standard theoretical predictions regarding animal decisions during cooperative interactions and experimental data, as well as, 2) to explore how well cleaners are able to readily identify and use relevant cues for decision making. Cleaners engage in mutualistic relationships with so-called reef fish ‘clients’, which visit cleaner territories for ectoparasite removal. Cleaners, however, prefer feeding on nitrogen-rich client mucus, which constitutes cheating. Hence, to help ensure a cooperative cleaner, clients employ various partner control mechanisms, including punishment and partner switching. This dynamic cleaning mutualism has hitherto provided strong empirical evidence in support of evolutionary game theory for predicting cooperative behaviour.
In Chapter 2, however, I demonstrate that cleaners from socially complex reef environments largely outperform cleaners from socially simple reefs in classic cooperation- and cognition-based experiments. A lower abundance and diversity of reef fish clients, as well as, a lower density of cleaners, characterize socially simple reefs. Cleaners from these simple environments generally failed to: 1) feed against their preference, 2) adjust their cooperative behaviour in the presence of an audience, and 3) consistently provide service priority to a temporary food source over a permanent food source. These findings strongly contrast published evidence on cleaner foraging behaviour in laboratory-based experiments. To further understand these inconsistencies, in Chapter 3, I investigated whether the two cleaner groups used different cues when making foraging decisions; specifically, in regards to client service priority. Cleaners from the socially complex reef environment were found to use a precise cue when making decisions, leading to higher accuracy in the laboratory, whereas cleaners from the socially simple reef environment used a correlated cue, or a rule of thumb, which lead to an overall poorer performance.
In Chapter 4, I determined that the rules applied by the two cleaner groups in nature appear to be locally adaptive and that the cognitive constraints displayed by cleaners from the socially simple reef environment were context specific, as both cleaner body condition and cognitive performance in an abstract task did not differ between reef environments. Finally, in Chapter 5, I investigated how well cleaners are able to extract relevant cues for decisions involving cheating and refuge-seeking. Here, I demonstrated the ability of cleaners to generalize predator species in a social tool context; yet this ability disappeared when cleaners were tested in an abstract context.
Collectively, these results have important implications for both cognition and evolutionary game theory. The results are discussed with an emphasis placed on the importance of the ecological approach to cognition, as well as, suggestions for future modifications to theoretical models.
Strategic social behaviour in wild vervet monkeys
In comparison to other vertebrates, primates have a large brain in relation to their body size. It has been hypothesised that the degree of social complexity is the major predictor for such variation. In group living species, individuals face various social challenges which can include finding the right balance between cooperation and competition with other group members. Thus to survive and reproduce individuals would have to show an adapted cognitive flexibility. Following this argument, two parallel hypotheses emerged; the “Machiavellian intelligence” and the “Social brain” hypotheses propose that the social complexity of group living selected respectively for advanced cognitive abilities and an increase in relative brain/neocortex size (i.e. complexity). However, finding a positive correlation between the complexity linked to social life, corresponding advanced cognitive processes and brain size/complexity remains challenging. First, adequate proxies of social complexity that could be applied to various taxa remain to be found. Second, examples of strategic social behaviour such as proposed by the Machiavellian intelligence have been described in many taxa suggesting that more comparative studies are needed to distinguish between advanced cognitive processes and those that could rely on associative learning. Finally, a potential link between cognitive abilities and brain/neocortex size remains largely unexplored.
By studying wild vervet monkeys (Chlorocebus aethiops) in South Africa, the aim of this thesis was to test for the presence of some social knowledge facets in their behaviour. I also wanted to assess their ability to use such knowledge strategically in both cooperation and competition contexts. Vervet monkeys represent an ideal species as they are highly social, have a strict linear female and male hierarchies and are usually very willing to participate in set-up experiments involving food.
In Chapter I, I tested the effect of natural migration, births and deaths on the individual centrality and strength of dyadic relationships within the grooming, 1m and 5m proximity social networks (i.e. method 1). I also used a new method (i.e. SIENA; method 2) to test both the network structure and the relationships dynamics. With both methods, I found a strong among-group variation. In addition, results suggest that females and juveniles have more influence than males on the stability at both the individual and dyadic levels, especially within the grooming network. Social relationships might be subject to frequent and significant changes often linked to natural demographic variation. Thus, social network analyses have the potential to capture important aspects of the cognitive social challenges an individual has to cope with. In Chapter II, I conducted rank reversal playbacks to test vervet monkeys’ knowledge about the entire group’s hierarchy. I found that females know about both female and male hierarchies while males and juveniles seem to lack such knowledge about the female hierarchy. Results therefore suggest sex and developmental differences in the extent of third party rank relationships. In Chapter III, I first trained females to consistently approach their personalised boxes to obtain a food reward, which allowed staging potential conflicts by placing two boxes next to each other. With such experiments I could show that subordinates trade grooming for tolerance and coalitionary support and that such trading is modified by the composition of the audience (i.e. individuals within 10m). However data also suggest that subordinates are not able to incorporate the effect of their grooming on dominants’ decision-making to their own advantage.
In summary, the results of this thesis provide important insights on vervet social strategies and underlying cognitive processes. The introduced methodological advances regarding social network analyses and experimentation to reveal social strategies offer a basis for future research on other primate species for comparison. Such data would then be amenable for correlative studies that link the results to brain evolution. In such a way, one can hope to make important progress regarding the major quest: to assess how social complexity, strategic social behaviours and brain size are interlinked.
What the cognitive abilities of the cleaner fish "Labroides dimidiatus" may tell us about vertebrate brain evolution
La grande variation existant chez les vertébrés concernant la taille relative du cerveau en comparaison à la taille du corps a toujours été un challenge scientifique majeur ; les scientifiques ont tenté de comprendre quels facteurs y étaient impliqués, ainsi que l’implication d’avoir un plus grand cerveau, autrement dit est-ce que la taille du cerveau est liée aux capacités cognitives ? Plusieurs hypothèses comme celle de l’intelligence sociale (social brain), de l’intelligence écologique (ecological intelligence), ainsi que plus récemment celle de l’intelligence générale (general intelligence) présentent différents facteurs qui pourraient expliquer cette variation. Pourtant, les résultats obtenus jusqu’à maintenant peuvent souvent être interprétés comme soutenant différentes hypothèses, démontrant que des études supplémentaires sont nécessaires pour trouver quels facteurs sélectifs sont les principaux vecteurs de l’évolution cérébrale. Le fait que la taille cérébrale relative diffère en moyenne d’un facteur 10 entre les endo- et les ectothermes, c’est-à-dire qu’un ectotherme qui a le même poids qu’un endotherme possède un cerveau 10 fois plus petit, est particulièrement intriguant. Alors qu’autant les ecto- que les endothermes font face à des challenges aussi bien sociaux qu’environnementaux, nous devons comprendre quels aspects sont d’une différence si fondamentale qu’un facteur 10 apparaisse. C’est pourquoi les processus cognitifs sont étudiés dans différentes espèces animales, via des tâches écologiques ou abstraites pour tester leur relation à la taille cérébrale, et si ces processus cognitifs sont liés à l’intelligence générale. Ma thèse de doctorat avait pour objectif d’enquêter si le poisson nettoyeur Labroides dimidiatus, une espèce avec une taille cérébrale moyenne chez les ectothermes, démontre des capacités cognitives dîtes avancées. Ce poisson nettoyeur interagit de manière mutualiste avec d’autres poissons du récif corallien, communément appelés ‘poissons clients’. Il ôte les parasites externes (ectoparasites) se trouvant sur la peau des poissons clients, constituant ainsi leurs ressources alimentaires. De ce fait, les poissons clients sont nettoyés de leurs parasites. Cependant, le poisson nettoyeur a une préférence gustative pour le mucus des poissons clients par rapport aux ectoparasites ; dans ce cas l’interaction n’est plus considérée comme mutualiste n’étant plus bénéfique pour le poisson client, ce qui est considéré comme de la triche. À cause de ce comportement de triche, le poisson nettoyeur démontre de grandes stratégies comportementales sophistiquées, qui ont été documentées précédemment, comme par exemple l’effet d’audience, la gestion de sa réputation, et la priorisation des différents types de poissons clients afin de les maintenir dans leur territoire. Premièrement, les capacités cognitives étaient testées séparément puis avec ou sans pertinence écologique pour le poisson nettoyeur. Avec cette première approche, j’ai pu découvrir si le poisson nettoyeur était capable de démontrer des capacités cognitives uniquement dans un contexte écologique ou s’il était également capable d’en démontrer dans un contexte plus abstrait. Deuxièmement, j’étais intéressée de tester la présence d’intelligence générale chez les ectothermes en expérimentant cette fois-ci différents processus cognitifs. Quatre tâches cognitives n’avaient aucune pertinence écologique et une était liée à l’écologie du poisson nettoyeur en question. Dans le premier chapitre, j’ai étudié le comportement des poissons dans un paradigme de gratification différée. Dans ledit paradigme, il a été démontré que les primates révèlent une performance élevée qui a été liée au haut niveau de maîtrise de soi, ainsi qu’à la compréhension de la remise de bénéfice dans le futur, affirmant ainsi la demande cognitive de cette tâche. J’ai travaillé avec deux espèces de poissons nettoyeurs (L. dimidiatus et L. bicolor), ainsi que deux espèces de poissons non-nettoyeurs de la famille des Labres (Halichoeres trimaculatus and H. hortulanus). Les deux espèces de poissons nettoyeurs diffèrent dans leur écologie : L. dimidiatus habitent dans des stations de nettoyage permettant les clients de décider dans quelle station ils veulent se faire nettoyer et par quel poisson nettoyeur. En revanche, L. bicolor ont un territoire plus grand et dépourvu de stations de nettoyage. Ce comportement dit errant permet à L. bicolor de tricher et ce plus souvent envers les poissons clients étant donné que ces derniers ne peuvent se remémorer par quel poisson nettoyeur ils ont été nettoyés. Les deux espèces de poissons non-nettoyeurs se nourrissent, quant à eux, de petits crustacés qu’ils trouvent dans le sable. Je me suis demandée si l’écologie spécifique des poissons nettoyeurs augmenterait leur performance par rapport à celle des poissons non-nettoyeurs qui n’ont aucune raison écologique pour réussir autant bien que les poissons nettoyeurs. Toutes les différentes espèces de poisson testées dans ce paradigme ont réussi de manière égale à contrôler leur impulsion envers la nourriture pour en obtenir plus. En revanche, seulement les poissons nettoyeurs ont démontré une compréhension de la tâche en prenant préalablement la décision d’attendre ou non pour obtenir plus de nourriture, démontrant ainsi leur capacité d’anticipation. Dans le second chapitre, L. dimidiatus a été testé selon une expérience abstraite sur l’apprentissage de concept, soit une approche classique pour tester si les animaux peuvent apprendre sans de renforcement spécifique (conditionnement). L’appariement à l’échantillon (matching-to-sample) a été utilisé comme expérience, dans sa forme la plus générale, par rapport à ce qui avait déjà été fait. Les poissons nettoyeurs ont rempli les conditions de réussite de cette tâche, nous démontrant ainsi qu’ils possèdent le processus cognitif de l’apprentissage de concept, autrement dit la capacité de raisonnement. De plus, un poisson a été testé dans un appariement à l’échantillon différé (delayed matching-to-sample) ; il a cependant échoué dans cette expérience. Du fait qu’un seul poisson a été testé dans cette dernière tâche, il est difficile de conclure que les poissons nettoyeurs ne possèdent pas le processus cognitif de la mémoire de travail (working memory). Finalement, dans le troisième chapitre, L. dimidiatus ont été exposés à différentes tâches conçues pour tester l’intelligence générale. Les performances relatives à chaque tâche étaient respectivement évaluées et notées afin de vérifier la présence ou non d’un facteur d’intelligence générale dit ‘g’ (general intelligence factor). Un aspect intéressant est que la variation intra spécifique dans les stratégies dites sophistiquées est liée à la densité de poissons indiquant une probable corrélation de la complexité intra- et interspécifique. Dès lors que ces stratégies étaient mises en relation à l’écologie du poisson nettoyeur, la question principale était de savoir si les performances des poissons nettoyeurs variaient dépendamment de la tâche écologiquement pertinente ou non. De ce fait, la moitié des individus venait d’une forte densité de poissons, tandis que l’autre moitié provenait d’une faible densité de poissons. Les poissons nettoyeurs ont démontré des capacités dans trois processus cognitifs sur quatre, c’est-à-dire en apprentissage et flexibilité, en inhibition, ainsi qu’en raisonnement quantitatif ; mais, ils échouèrent dans la tâche de la mémoire de travail (working memory). Quand bien même les poissons nettoyeurs ont démontré de bonnes performances dans ces différentes tâches, je n’ai pas trouvé une forme d’intelligence générale chez ce poisson ; les différentes tâches n’étant pas positivement corrélées entre elles dans une analyse de facteur de composant principal. De plus, la complexité de l’environnement, c’-est-à-dire la densité de poissons, n’a pas affecté la performance des poissons nettoyeurs et ce dans aucune des tâches. En conclusion, cette thèse augmente l’évidence que les poissons nettoyeurs, comme représentants des ectothermes avec un cerveau relativement plus petit comparé aux endothermes, possèdent une variété de processus cognitifs considérés comme avancés, qu’ils peuvent appliquer à des situations non-écologiquement pertinentes. De ce fait, les résultats de cette thèse réfutent l’hypothèse que les majeures différences dans les capacités cognitives expliquent la différence d’un facteur 10 dans la taille relative du cerveau entre les vertébrés dits endothermes et ceux dits ectothermes. Cependant, malgré les capacités cognitives avancées des poissons nettoyeurs, ils sont dépourvus d’intelligence générale. Ce résultat nous amène à se poser la question de savoir si l’absence d’intelligence générale est un élément commun des ectothermes. Si ceci est confirmé, l’intelligence générale pourrait fournir une nouvelle explication quant à la division dans l’index d’encéphalisation entre endothermes et ectothermes. ABSTRACT Explaining the great variation in relative brain size in comparison to body size among vertebrates has been a great scientific challenge. Scientists have tried to understand what factors triggered this relative difference, as well as what it implies to have a bigger brain, i.e. how is brain size linked to cognitive abilities? Various hypotheses such as the social brain hypothesis, the ecological intelligence hypothesis, as well as most recently the general intelligence hypothesis propose different factors that could explain this variation. However, current results can often be interpreted as supporting various hypotheses, showing that additional studies are needed in order to disentangle which selective factors are the main driver of brain evolution. Particularly intriguing is the observation that relative brain size differs on average by a factor 10 between endo- and ectotherms, i.e. an ectotherm of the same weight of an endotherm possesses a ten times smaller brain. Thus, while both ecto- and endotherms face social and environmental challenges, we need to understand what aspects are of such fundamental difference that a factor 10 emerges. Therefore, cognitive processes are studied in various animal species via ecological or abstract task to test their relationship to brain size, and whether cognitive processes are linked to general intelligence. My PhD thesis aimed to investigate whether cleaner fish Labroides dimidiatus, a species with a rather average ectotherm brain size, show advanced cognitive abilities. Cleaner fish engage in mutualistic interactions with so-called client fish. They remove the ectoparasites from their clients, constituting their food resources, and clients, in turn, get cleaned. However, cleaners prefer to eat mucus over ectoparasites constituting cheating. Because of this cheating behaviour, cleaners show great sophisticated strategies behaviour previously documented, such as audience effect, reputation management, and client type prioritization in order to retain their clients. First, cognitive processes were tested separately and with or without ecological relevance to the fish. With this first approach, I was able to disentangle whereas cleaner fish were also able to show cognitive abilities only in an ecological context or also in an abstract situation. Second, I was interested in testing the presence of general intelligence in ectotherms by testing this time different cognitive processes. Four cognitive tasks were lacking ecological relevance and one was related to cleaners’ ecology. In the first chapter, I tested fish in a delay of gratification paradigm. High performance in primates has been linked to high levels of self-control and low discounting of future benefits, proposing that the ability is cognitively demanding. I used two cleaner fish species (L. dimidiatus and L. bicolor), and noncleaner wrasse species (Halichoeres trimaculatus and H. hortulanus) were used. Cleaner fish species differ in their ecology as L. dimidiatus live at cleaning stations, allowing clients to decide whether to seek or avoid any particular cleaner. In contrast, L. bicolor are roving cleaners lacking cleaning stations. Such roving behaviour allows L. bicolor to cheat more towards their clients as these ones are not capable of following the cleaners bicolor individually. Both non-cleaner wrasses eat small crustaceans in the sand. I asked whether the special ecology of cleaners would increase their performance compared to non-cleaners which lack any ecological reason to perform well in this task. Fish species performed well at controlling their impulse toward food in order to get more. In contrast, only cleaners show an understanding of the task by making the decision early on to wait or not for a bigger food reward, showing the ability to anticipate. In the second chapter, L. dimidiatus were tested in an abstract experimental design of concept learning, a classic approach to test whether animals can learn without specific reinforcement (conditioning). The matching-to-sample task was used in the most general form compared to previous experiments. Cleaners overall performed above chance in this task, suggesting that they possess the cognitive process of concept learning, i.e. reasoning ability. Furthermore, one individual was tested in a delayed matching-to-sample experiment but did not succeed. As only one individual was tested, it is rather difficult to conclude that cleaners lack working memory cognitive process. Finally, in the third chapter, L. dimidiatus individuals were exposed to different tasks designed to test for general intelligence, and their performances in each task were ranked to check for the presence/absence of ‘g’. Interestingly, intraspecific variation in sophisticated strategies were linked to fish densities as a likely correlate of intra- and interspecific complexity. Since those strategies were related to cleaners' ecology, the main question was whether cleaners' performances vary depending on if the task was ecologically relevant or not. Therefore, half of the individuals were coming from a high fish density and the other half from a low fish density. Cleaners showed abilities in three out of four cognitive processes, i.e. learning-flexibility, inhibition, and quantitative reasoning. They failed in the working memory task. Even though cleaners performed well in the tasks, I found no evidence for general intelligence, i.e. the tasks were not positively loading on a single main principal component factor. Moreover, the complexity of the environment, i.e. fish density, did not affect cleaners' performance in any task. In conclusion, this thesis increases evidence that cleaner fish, as representatives of ectotherms with relatively smaller brains compared to endotherms, possess a variety of supposedly advanced cognitive processes, which they can also apply to non-ecologically relevant situations. Therefore, the results from this thesis refute the hypothesis that major differences in the cognitive tool set may explain the 10-fold difference in relative brain size between endotherm and ectotherm vertebrates. However, despite cleaners' advanced cognitive abilities, they lack general intelligence. This result raises the question of whether the absence of general intelligence is a common pattern in ectotherms. If this was confirmed, general intelligence may provide a new explanation for the endotherm-ectotherm divide in the encephalization index.
Endogenous oxytocin predicts helping and conversation as a function of group membership.
Humans cooperate with unrelated individuals to an extent that far outstrips any other species. We also display extreme variation in decisions about whether to cooperate or not, and the mechanisms driving this variation remain an open question across the behavioural sciences. One candidate mechanism underlying this variation in cooperation is the evolutionary ancient neurohormone oxytocin (OT). As current research focuses on artificial administration of OT in asocial tasks, little is known about how the hormone in its naturally occurring state actually impacts behaviour in social interactions. Using a new optimal foraging paradigm, the 'egg hunt', we assessed the association of endogenous OT with helping behaviour and conversation. We manipulated players' group membership relative to each other prior to an egg hunt, during which they had repeated opportunities to spontaneously help each other. Results show that endogenous baseline OT predicted helping and conversation type, but crucially as a function of group membership. Higher baseline OT predicted increased helping but only between in-group players, as well as decreased discussion about individuals' goals between in-group players but conversely more of such discussion between out-group players. Subsequently, behaviour but not conversation during the hunt predicted change in OT, in that out-group members who did not help showed a decrease in OT from baseline levels. In sum, endogenous OT predicts helping behaviour and conversation, importantly as a function of group membership, and this effect occurs in parallel to uniquely human cognitive processes.
Partner control mechanisms in repeated social interactions
Les individus qui interagissent socialement doivent souvent décider entre aider leur prochain, en leur procurant un bénéfice a un possible cout, ou pas. Tandis qu'une paire d'individus s'en sort mieux si les deux s'entraident, un individu peut tirer un bénéfice relatif s'il se décide à ne pas aider tandis que l'autre l'aide. Cette situation crée un dilemme social. Parce que les interactions sociales sont souvent répétées, les individus peuvent conditionner leurs propres actions sur les actions de leur partenaire lors d'interactions passées. Il existe trois mécanismes de contrôle de partenaire qui stabilisent la coopération lors d'interactions répétées entre paires d'individus: la réciprocité positive (la décision d'aider est conditionnée sur l'aide du partenaire lors de l'interaction précédente), la punition, et le changement de partenaire. Mais les conditions sous lesquelles un mécanisme domine sur les autres lorsque les trois mécanismes coévoluent dans une même population sont mal comprises.
Un autre point qu'il est important de considérer pour comprendre les interactions sociales est que le comportement exprimé peut aussi dépendre sur l'environnement. Il est probable que le toilettage social chez les primates, par exemple, dépend de la compétition sur les ressources de nourriture. Si la nourriture est concentrée dans l'espace et facilement monopolisée, les individus en haut de la hiérarchie sociale peuvent défendre ces ressources, auquel cas les individus en bas de la hiérarchie doivent les toiletter afin d'être tolérer sur leur territoire et accéder à leur ressource. Afin de comprendre ce comportement, il est nécessaire de comprendre les conditions sous lesquelles le toilettage est échangé contre du toilettage, ou contre la tolérance sur un territoire.
Dans cette thèse, je développe et utilise des modèles agents basés pour explorer la coévolution des mécanismes de contrôle de partenaire et l'évolution de patrons de toilettage chez les primates.
Dans le premier chapitre, je démontre que dans une population panmictique, plus les interactions sont répétées, plus il est probable que le changement de partenaire soit le mécanisme de contrôle de partenaire dominant. Si les interactions sont restreintes au sein de petits groupes de non-apparentés, alors la punition est le mécanisme le plus probablement favorisé par la sélection. Les conditions pour que la réciprocité positive soit dominante sont moins clairement définies.
Dans le deuxième chapitre, j'étudie comment la dispersion limitée chez la progéniture, le recouvrement de génération, et le cout de la complexité influencent la compétitivité de chaque mécanisme de contrôle. Il est démontré que la compétitivité du changement de partenaire est accrue par le recouvrement de génération tandis que celle de la punition est très diminuée par le cout de complexité. De plus, alors que les conditions pour que ces mécanismes de contrôle de partenaire soient dominants s'élargissent avec la structure d'apparentement, les conditions pour que l'aide inconditionnelle domine sur l'aide conditionnelle se restreignent.
Dans le troisième chapitre, je développe un modèle d'apprentissage par renforcement pour simuler les interactions de toilettage et l'accès a la nourriture chez les primates. On observe des patrons de toilettage réciproque lorsqu'il n'y pas de compétition pour les ressources, et des patrons de toilettage dirigé vers le haut de l'échelle hiérarchique lorsque la compétition pour les ressources augmente. Il est montré que l'effort dans le toilettage n'augmente pas forcément avec la compétition pour les ressources, et qu'une augmentation d'agressivité amène le toilettage à être plus réciproque.
En bref, les comportements sociaux d'entraide dans les milieux naturels sont observés dans une multitude d'interactions sociales répétées. En explorant une gamme variée de conditions, les modèles développés dans cette thèse permettent de mieux comprendre quels mécanismes de contrôle de partenaire sont favorisés par la sélection naturelle. De plus, le modèle du troisième chapitre montre que les patrons de toilettage dépendent de plusieurs paramètres naturels importants., Individuals that interact socially regularly have to make decisions whether to help another individual (provide some payoff benefit, possible at a personal payoff cost) or not. Here, a pair of individuals is best off if both individuals help each other, but a single individual may gain a relative payoff advantage by not helping (defecting) while the partner does choose to help, thus creating a dilemma. Because social interactions are often repeated, individuals can condition the actions they take on the actions taken by their partner in previous rounds of interaction. The so-called partner control mechanisms positive reciprocity (where acts of helping are conditioned on receiving help from the partner), punishment, and partner switching have all been shown to stabilize cooperation in populations where the individuals engage in repeated pairwise interactions. What remains unclear, however, is under which conditions each partner control mechanism will be dominant in a population if the the partner control mechanisms coevolve.
Additionally, the expressed behaviour in repeated social interactions may depend on the state of the environment in which the interactions take place. Social grooming in primates is likely to depend on the food competition that the individuals experience. If food is clustered and monopolizable, high ranked individuals may defend food sources, where low ranked individuals then need to groom high ranked ones in order to be tolerated on the food source, resulting in grooming being directed up the hierarchy. However, the conditions that cause grooming to be traded for grooming or grooming to be traded for tolerance have yet to be quantified.
In this thesis, I developed several agent-based models in order to investigate both the coevolution of various partner control mechanisms and the grooming patterns in primates.
In chapter one, I demonstrated that in a well-mixed population the likelihood of partner switching being the dominant partner control mechanism increases with increasing number of rounds of interaction. Furthermore, if interactions are localized to small groups of unrelated individuals, then punishment is more likely to be favoured by selection compared to the well-mixed case, while the conditions where positive reciprocity is dominant are less clearly defined.
In chapter two, I investigated how limited migration of offspring, overlapping generations, and complexity costs affect the competitiveness of each partner control mechanism. It is shown that the relative competitiveness of partner switching is increased due to generational overlap, while punishment is most strongly negatively affected by complexity costs. Additionally, while the conditions where these partner control mechanisms are dominant in the population increases if the population is kin structured, the conditions where unconditional helping is dominant over conditional helping strategies are rather stringent.
In chapter three, I developed a reinforcement learning model that simulated grooming and feeding interactions in primates. The model generated patterns of grooming reciprocity in the absence of food competition, while grooming was found to be directed up the hierarchy if individuals compete for food. It is shown that grooming up the hierarchy may not necessarily increase with increasing food competition, and that an increase in aggressiveness causes grooming to become more reciprocal.
In summary, helping behaviours occur in a diversity of repeated social interactions in natural populations. By exploring a large range of conditions, the models developed in this thesis provide insights regarding which partner control mechanism is likely to be dominant in a population. In addition, the model from chapter three shows how grooming patterns may depend on a variety of relevant parameters.
Long‐term memory retention in a wild fish species “Labroides dimidiatus” eleven months after an aversive event
Memory is essential to enhance future survival and reproduction as it helps in storing and retrieving useful information to solve particular environmental problems. However, we lack quantitative evidence on how far animals in the wild can maintain given information for extended periods without reinforcement. Here, we document correlative evidence of cleaner fish Labroides dimidiatus remembering being caught in a barrier net for up to 11 months. In 2015, about 60% of cleaners from one large isolated reef had been used for laboratory experiments and then returned to their site of capture. Eleven months later, 50% of cleaners at the same site showed an unusual hiding response to the placement of the barrier net, in contrast to three control sites where no cleaners had been caught during the last 2 years. The results suggest that a single highly aversive event (i.e., being caught in a barrier net) resulted in cleaners storing long‐term crucial information that allowed them to avoid being caught again. Our results further our knowledge of fish cognitive capacities and long‐term memory retention.
The language of cooperation: shared intentionality drives variation in helping as a function of group membership
While we know that the degree to which humans are able to cooperate is unrivalled by other species, the variation humans actually display in their cooperative behaviour has yet to be fully explained. This may be because research based on experimental game-theoretical studies neglects fundamental aspects of human sociality and psychology, namely social interaction and language. Using a newoptimal foraging game loosely modelled on the prisoner’s dilemma, the Egg Hunt, we categorized players as either in-group or out-group to each other and studied their spontaneous language usage while they made interactive, potentially cooperative decisions. Both shared group membership and the possibility to talk led to increased cooperation and overall success in the hunt. Notably, analysis of players’ conversations showed that in-group members engaged more in shared intentionality, the human ability to both mentally represent and then adopt another’s goal, whereas out-group members discussed individual goals more. Females also helped more and displayed more shared intentionality in discussions than males. Crucially, we show that shared intentionality was the mechanism driving the increase in helping between in-group players over out-group players at a cost to themselves. By studying spontaneous language during social interactions and isolating shared intentionality as the mechanism underlying successful cooperation, the current results point to a probable psychological source of the variation in cooperation humans display.
What makes a cleaner a cleaner ?
In his last presidential address to the Royal Society in 2005, Robert M. May stated that “The most important unanswered question in evolutionary biology, and more generally in the social sciences, is how cooperative behaviour evolved and can be maintained”. My thesis provides a contribution to answering this big question by investigating how one particular species evolved for an ecology that rests heavily upon cooperative interactions: the bluestreak cleaner wrasse Labroides dimidiatus. This species engages in up to 2000 cooperative interactions per day with dozens of other ‘client’ coral reef fishes, thus making it a prime system for studying cooperation between unrelated individuals. Conflicts between cleaners and clients arise because the former prefer to bite clients to eat their protective mucus rather than focusing on ectoparasites. In response to such exploitation, clients use various forms of partner control mechanisms that promote cooperative behaviour in cleaners. As a result, cleaners are known to use a diversity of strategic behaviours to determine when to cheat and when to cooperate. Cleaners’ behaviour thus appears very well adapted to the demands of their peculiar ecology.
In my thesis, I used a comparative approach to investigate which traits appear to be associated with the highly social ecology of cleaners, or in other words: What makes a cleaner a cleaner? Through a series of experiments, I compared the cognitive skills, escape performance, foraging ecology and vision of L. dimidiatus with other species of labrids that do not engage in cleaning (or only occasionally). These comparisons allowed me to identify some of the characteristics that set cleaners apart, and thus further our understanding of how social ecology can affect the evolution of a species.
In the first chapter, I showed that L. dimidiatus was able to fine-tune its level of cooperation to the specifics of different cleaning-related situations, an ability that was absent in the closely related Halichoeres melanurus. In the second chapter, I investigated whether the demands of a highly social lifestyle led to an overall increase of cognitive performance in L. dimidiatus, or whether performance was tightly linked to ecological demands. L. dimidiatus outperformed five other species of labrids in two ecologically relevant tasks. However, all species performed similarly in a task with little ecological relevance, suggesting that cognition in cleaners is tightly linked to the challenges faced in nature. In the third chapter, results from foraging experiments suggest that L. dimidiatus evolved a foraging position that allows for increased efficiency in cleaning interactions. In comparison with four other species, L. dimidiatus adopted a significantly lower body angle with regards to the substrate when foraging. Furthermore, this species experienced almost no reduction in efficiency when searching for cryptic food items in comparison with conspicuous ones, while the other species all performed worse in the cryptic condition. It thus appears that the peculiar foraging posture of L. dimidiatus is well suited for cleaning interactions. Unfortunately, my current data did not allow assessing whether the visual system also adapted for a low body angle while foraging. Finally, in the last chapter, I asked whether because of the service they provide to predators, a reduction in predation pressures led to the decay of escape performance in L. dimidiatus. Interestingly, measures of escape performance in a controlled laboratory setup showed that L. dimidiatus was among the top performers in comparison with 5 other labrids. These results suggest that the risks associated with cleaning interactions are sufficient to maintain a high escape performance in cleaners, despite their privileged relationship with predatory clients.
In summary, a wide range of characteristics appear to be important for cleaning interactions, and species that specialized in this activity seem to have undergone very different selective pressures than fishes with more standard ecologies. Identifying some of the key aspects related to the ecology of cleaners provides a good example of how the evolution of a species can be affected by the demands of a highly social life. In this system, I argue that competition among service providers and conflicts of interests between cleaners and clients appear to be the major drivers of adaptation.