Evolutionary Biology

Primate sympatry shapes the evolution of their brain architecture

10.24072/pcjournal.259 - Peer Community Journal, Volume 3 (2023), article no. e37.

Get full text PDF Peer reviewed and recommended by PCI

The main hypotheses on the evolution of animal cognition emphasise the role of conspecifics in affecting the socio-ecological environment shaping cognition. Yet, space is often simultaneously occupied by multiple species from the same ecological guild. These sympatric species can compete for food, which may thereby stimulate or hamper cognition. Considering brain size as a proxy for cognition, we tested whether species sympatry impacted the evolution of cognition in frugivorous primates. We first retraced the evolutionary history of sympatry between frugivorous primate lineages. We then fitted phylogenetic models of the evolution of the size of several brain regions in frugivorous primates, considering or not species sympatry. We found that the evolution of the whole brain or brain regions used in immediate information processing was best fitted with models not considering sympatry. By contrast, models considering species sympatry best predicted the evolution of brain regions related to long-term memory of interactions with the socio-ecological environment, with a decrease in their size the higher the sympatry. We speculate that species sympatry, by generating intense food depletion, might lead to an over-complexification of resource spatiotemporality that counteracts the benefits of high cognitive abilities and/or might drive niche partitioning and specialisation, thereby inducing lower brain region sizes. In addition, we reported that primate species in sympatry diversify more slowly. This comparative study suggests that species sympatry significantly contributes to shaping primate evolution.

Published online:
DOI: 10.24072/pcjournal.259
Keywords: Brain size - Cognition - Diversification - Frugivory - Primates - Sympatry
Keywords: Brain size, Cognition, Diversification, Frugivory, Primates, Sympatry
Robira, Benjamin 1, 2; Perez-Lamarque, Benoît 3, 4

1 CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France
2 Eco-anthropologie (EA), Muséum National d’Histoire Naturelle, CNRS, Université de Paris, Musée de l’Homme, Paris, France
3 Institut de Biologie de l’École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France
4 Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Robira, Benjamin and Perez-Lamarque, Beno{\^\i}t},
     title = {Primate sympatry shapes the evolution of their brain architecture
     journal = {Peer Community Journal},
     eid = {e37},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.259},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.259/}
AU  - Robira, Benjamin
AU  - Perez-Lamarque, Benoît
TI  - Primate sympatry shapes the evolution of their brain architecture

JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.259/
DO  - 10.24072/pcjournal.259
ID  - 10_24072_pcjournal_259
ER  - 
%0 Journal Article
%A Robira, Benjamin
%A Perez-Lamarque, Benoît
%T Primate sympatry shapes the evolution of their brain architecture

%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.259/
%R 10.24072/pcjournal.259
%F 10_24072_pcjournal_259
Robira, Benjamin; Perez-Lamarque, Benoît. Primate sympatry shapes the evolution of their brain architecture
. Peer Community Journal, Volume 3 (2023), article  no. e37. doi : 10.24072/pcjournal.259. https://peercommunityjournal.org/articles/10.24072/pcjournal.259/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100548

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Arbour, J. H.; Santana, S. E. A major shift in diversification rate helps explain macroevolutionary patterns in primate species diversity, Evolution, Volume 71 (2017) no. 6, pp. 1600-1613 | DOI

[2] Aristide, L.; dos Reis, S. F.; Machado, A. C.; Lima, I.; Lopes, R. T.; Perez, S. I. Brain shape convergence in the adaptive radiation of New World monkeys, Proceedings of the National Academy of Sciences, Volume 113 (2016) no. 8, pp. 2158-2163 | DOI

[3] Ashton, B. J.; Kennedy, P.; Radford, A. N. Interactions with conspecific outsiders as drivers of cognitive evolution, Nature Communications, Volume 11 (2020) no. 1 | DOI

[4] Avarguès‐Weber, A.; Dawson, E. H.; Chittka, L. Mechanisms of social learning across species boundaries, Journal of Zoology, Volume 290 (2013) no. 1, pp. 1-11 | DOI

[5] Báez-Mendoza, R.; Schultz, W. The role of the striatum in social behavior, Frontiers in Neuroscience, Volume 7 (2013) | DOI

[6] Barton, R. A.; Harvey, P. H. Mosaic evolution of brain structure in mammals, Nature, Volume 405 (2000) no. 6790, pp. 1055-1058 | DOI

[7] Benson-Amram, S.; Dantzer, B.; Stricker, G.; Swanson, E. M.; Holekamp, K. E. Brain size predicts problem-solving ability in mammalian carnivores, Proceedings of the National Academy of Sciences, Volume 113 (2016) no. 9, pp. 2532-2537 | DOI

[8] Blomberg, S. P.; Garland, T.; Ives, A. R. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile, Evolution, Volume 57 (2003) no. 4, pp. 717-745 | DOI

[9] Blomberg, S. P.; Rathnayake, S. I.; Moreau, C. M. Beyond Brownian motion and the Ornstein-Uhlenbeck process: Stochastic diffusion models for the evolution of quantitative characters, The American Naturalist, Volume 195 (2020) no. 2, pp. 145-165 | DOI

[10] Bollback, J. P. SIMMAP: Stochastic character mapping of discrete traits on phylogenies, BMC Bioinformatics, Volume 7 (2006) no. 1 | DOI

[11] Hamady, M.; Peden, E.; Knight, R.; Singh, R. Fast-Find: A novel computational approach to analyzing combinatorial motifs, BMC Bioinformatics, Volume 7 (2006) no. 1 | DOI

[12] Burgess, N.; Maguire, E. A.; O'Keefe, J. The human hippocampus and spatial and episodic memory, Neuron, Volume 35 (2002) no. 4, pp. 625-641 | DOI

[13] Burnham, K. P.; Anderson, D. R. Model selection and multimodel inference: A practical information-theoretic approach, Springer New York, New York, NY, 2002 | DOI

[14] Byrne, R. W. Evolution of primate cognition, Cognitive Science, Volume 24 (2000) no. 3, pp. 543-570 | DOI

[15] Byrne, R. W. Machiavellian intelligence retrospective., Journal of Comparative Psychology, Volume 132 (2018) no. 4, pp. 432-436 | DOI

[16] Roeder, D. V.; Husak, M. S.; Murphy, M. T.; Patten, M. A. Size, ornamentation, and flight feather morphology promote within-pair paternity in a sexually dimorphic passerine, Behavioral Ecology and Sociobiology, Volume 73 (2019) no. 7 | DOI

[17] Carroll, L. Through the looking glass, Macmillan, London, U.K., 1871

[18] Clutton‐Brock, T. H.; Harvey, P. H. Primates, brains and ecology, Journal of Zoology, Volume 190 (1980) no. 3, pp. 309-323 | DOI

[19] Condamine, F. L.; Rolland, J.; Morlon, H. Assessing the causes of diversification slowdowns: temperature‐dependent and diversity‐dependent models receive equivalent support, Ecology Letters, Volume 22 (2019) no. 11, pp. 1900-1912 | DOI

[20] Rocha, J. M. d. A.; Pinto, M. P.; Boubli, J. P.; Grelle, C. E. V. The Role of competition in structuring primate communities under different productivity regimes in the amazon, PLOS ONE, Volume 10 (2015) no. 12 | DOI

[21] Deane, A. S.; Nargolwalla, M. C.; Kordos, L.; Begun, D. R. New evidence for diet and niche partitioning in Rudapithecus and Anapithecus from Rudabánya, Hungary, Journal of Human Evolution, Volume 65 (2013) no. 6, pp. 704-714 | DOI

[22] Deaner, R. O.; Nunn, C. L.; van Schaik, C. P. Comparative tests of primate cognition: Different scaling methods produce different results, Brain, Behavior and Evolution, Volume 55 (2000) no. 1, pp. 44-52 | DOI

[23] DeCasien, A. R.; Higham, J. P. Primate mosaic brain evolution reflects selection on sensory and cognitive specialization, Nature Ecology & Evolution, Volume 3 (2019) no. 10, pp. 1483-1493 | DOI

[24] DeCasien, A. R.; Williams, S. A.; Higham, J. P. Primate brain size is predicted by diet but not sociality, Nature Ecology & Evolution, Volume 1 (2017) no. 5 | DOI

[25] Drury, J.; Clavel, J.; Manceau, M.; Morlon, H. Estimating the effect of competition on trait evolution using maximum likelihood inference, Systematic Biology, Volume 65 (2016) no. 4, pp. 700-710 | DOI

[26] Drury, J. P.; Cowen, M. C.; Grether, G. F. Competition and hybridization drive interspecific territoriality in birds, Proceedings of the National Academy of Sciences, Volume 117 (2020) no. 23, pp. 12923-12930 | DOI

[27] Drury, J. P.; Tobias, J. A.; Burns, K. J.; Mason, N. A.; Shultz, A. J.; Morlon, H. Contrasting impacts of competition on ecological and social trait evolution in songbirds, PLOS Biology, Volume 16 (2018) no. 1 | DOI

[28] Dunbar, R. I. M.; Shultz, S. Evolution in the social brain, Science, Volume 317 (2007) no. 5843, pp. 1344-1347 | DOI

[29] Dunbar, R. I. M.; Shultz, S. Why are there so many explanations for primate brain evolution?, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 372 (2017) no. 1727 | DOI

[30] Dunlap, A. S.; Nielsen, M. E.; Dornhaus, A.; Papaj, D. R. Foraging bumble bees weigh the reliability of personal and social information, Current Biology, Volume 26 (2016) no. 9, pp. 1195-1199 | DOI

[31] Estrada, A.; Garber, P. A.; Rylands, A. B.; Roos, C.; Fernandez-Duque, E.; Di Fiore, A.; Nekaris, K. A.-I.; Nijman, V.; Heymann, E. W.; Lambert, J. E.; Rovero, F.; Barelli, C.; Setchell, J. M.; Gillespie, T. R.; Mittermeier, R. A.; Arregoitia, L. V.; de Guinea, M.; Gouveia, S.; Dobrovolski, R.; Shanee, S.; Shanee, N.; Boyle, S. A.; Fuentes, A.; MacKinnon, K. C.; Amato, K. R.; Meyer, A. L. S.; Wich, S.; Sussman, R. W.; Pan, R.; Kone, I.; Li, B. Impending extinction crisis of the world’s primates: Why primates matter, Science Advances, Volume 3 (2017) no. 1 | DOI

[32] Gómez-Robles, A.; Hopkins, W. D.; Sherwood, C. C. Modular structure facilitates mosaic evolution of the brain in chimpanzees and humans, Nature Communications, Volume 5 (2014) no. 1 | DOI

[33] Gonda, A.; Herczeg, G.; Merilä, J. Evolutionary ecology of intraspecific brain size variation: a review, Ecology and Evolution, Volume 3 (2013) no. 8, pp. 2751-2764 | DOI

[34] González-Forero, M.; Gardner, A. Inference of ecological and social drivers of human brain-size evolution, Nature, Volume 557 (2018) no. 7706, pp. 554-557 | DOI

[35] Goodale, E.; Beauchamp, G.; Magrath, R. D.; Nieh, J. C.; Ruxton, G. D. Interspecific information transfer influences animal community structure, Trends in Ecology & Evolution, Volume 25 (2010) no. 6, pp. 354-361 | DOI

[36] Grueter, C. C. Home range overlap as a driver of intelligence in primates, American Journal of Primatology, Volume 77 (2015) no. 4, pp. 418-424 | DOI

[37] Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package, Journal of Statistical Software, Volume 33 (2010) no. 2 | DOI

[38] Friedman, J.; Hastie, T.; Tibshirani, R. Regularization Paths for Generalized Linear Models via Coordinate Descent, Journal of Statistical Software, Volume 33 (2010) no. 1 | DOI

[39] Havmøller, L. W.; Loftus, J. C.; Havmøller, R. W.; Alavi, S. E.; Caillaud, D.; Grote, M. N.; Hirsch, B. T.; Tórrez‐Herrera, L. L.; Kays, R.; Crofoot, M. C. Arboreal monkeys facilitate foraging of terrestrial frugivores, Biotropica, Volume 53 (2021) no. 6, pp. 1685-1697 | DOI

[40] Healy, S. D.; Rowe, C. A critique of comparative studies of brain size, Proceedings of the Royal Society B: Biological Sciences, Volume 274 (2007) no. 1609, pp. 453-464 | DOI

[41] Henke-von der Malsburg, J.; Kappeler, P. M.; Fichtel, C. Linking ecology and cognition: does ecological specialisation predict cognitive test performance?, Behavioral Ecology and Sociobiology, Volume 74 (2020) no. 12 | DOI

[42] Westrick, S. E.; Taylor, R. W.; Boutin, S.; Lane, J. E.; McAdam, A. G.; Dantzer, B. Attentive red squirrel mothers have faster growing pups and higher lifetime reproductive success, Behavioral Ecology and Sociobiology, Volume 74 (2020) no. 6 | DOI

[43] Herrmann, E.; Call, J.; Hernàndez-Lloreda, M. V.; Hare, B.; Tomasello, M. Humans Have Evolved Specialized Skills of Social Cognition: The Cultural Intelligence Hypothesis, Science, Volume 317 (2007) no. 5843, pp. 1360-1366 | DOI

[44] Heymann, E. W.; Buchanan-Smith, H. M. The behavioural ecology of mixed-species troops of callitrichine primates, Biological Reviews of the Cambridge Philosophical Society, Volume 75 (2000) no. 2, pp. 169-190 | DOI

[45] Heymann, E. W.; Hsia, S. S. Unlike fellows – a review of primate–non‐primate associations, Biological Reviews, Volume 90 (2015) no. 1, pp. 142-156 | DOI

[46] Tung Ho, L. s.; Ané, C. A linear-time algorithm for gaussian and non-gaussian trait evolution models, Systematic Biology, Volume 63 (2014) no. 3, pp. 397-408 | DOI

[47] Isler, K.; van Schaik, C. P. The expensive brain: A framework for explaining evolutionary changes in brain size, Journal of Human Evolution, Volume 57 (2009) no. 4, pp. 392-400 | DOI

[48] The IUCN red list of threatened species, IUCN, 2021 (https://www.iucnredlist.org/)

[49] Janmaat, K. R.; Boesch, C.; Byrne, R.; Chapman, C. A.; Goné Bi, Z. B.; Head, J. S.; Robbins, M. M.; Wrangham, R. W.; Polansky, L. Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit, American Journal of Primatology, Volume 78 (2016) no. 6, pp. 626-645 | DOI

[50] Janmaat, K. R. L.; Chapman, C. A.; Meijer, R.; Zuberbühler, K. The use of fruiting synchrony by foraging mangabey monkeys: a ‘simple tool’ to find fruit, Animal Cognition, Volume 15 (2012) no. 1, pp. 83-96 | DOI

[51] Janmaat, K. R.; de Guinea, M.; Collet, J.; Byrne, R. W.; Robira, B.; van Loon, E.; Jang, H.; Biro, D.; Ramos-Fernández, G.; Ross, C.; Presotto, A.; Allritz, M.; Alavi, S.; Van Belle, S. Using natural travel paths to infer and compare primate cognition in the wild, iScience, Volume 24 (2021) no. 4 | DOI

[52] Johnson, A.; van der Meer, M. A.; Redish, A. D. Integrating hippocampus and striatum in decision-making, Current Opinion in Neurobiology, Volume 17 (2007) no. 6, pp. 692-697 | DOI

[53] Kamilar, J. M. Environmental and geographic correlates of the taxonomic structure of primate communities, American Journal of Physical Anthropology, Volume 139 (2008) no. 3, pp. 382-393 | DOI

[54] Kamilar, J. M.; Ledogar, J. A. Species co-occurrence patterns and dietary resource competition in primates, American Journal of Physical Anthropology, Volume 144 (2011) no. 1, pp. 131-139 | DOI

[55] Kashetsky, T.; Avgar, T.; Dukas, R. The cognitive ecology of animal movement: Evidence from birds and mammals, Frontiers in Ecology and Evolution, Volume 9 (2021) | DOI

[56] Kitamura, T.; Ogawa, S. K.; Roy, D. S.; Okuyama, T.; Morrissey, M. D.; Smith, L. M.; Redondo, R. L.; Tonegawa, S. Engrams and circuits crucial for systems consolidation of a memory, Science, Volume 356 (2017) no. 6333, pp. 73-78 | DOI

[57] Koziol, L. F.; Budding, D.; Andreasen, N.; D’Arrigo, S.; Bulgheroni, S.; Imamizu, H.; Ito, M.; Manto, M.; Marvel, C.; Parker, K.; Pezzulo, G.; Ramnani, N.; Riva, D.; Schmahmann, J.; Vandervert, L.; Yamazaki, T. Consensus paper: The cerebellum's role in movement and cognition, Cerebellum, Volume 13 (2013) no. 1, pp. 151-177 | DOI

[58] Logan, C. J.; Avin, S.; Boogert, N.; Buskell, A.; Cross, F. R.; Currie, A.; Jelbert, S.; Lukas, D.; Mares, R.; Navarrete, A. F.; Shigeno, S.; Montgomery, S. H. Beyond brain size: Uncovering the neural correlates of behavioral and cognitive specialization, Comparative Cognition and Behavior Reviews, Volume 13 (2018), pp. 55-89 | DOI

[59] Losin, N.; Drury, J. P.; Peiman, K. S.; Storch, C.; Grether, G. F. The ecological and evolutionary stability of interspecific territoriality, Ecology Letters, Volume 19 (2016) no. 3, pp. 260-267 | DOI

[60] MacLean, E. L.; Hare, B.; Nunn, C. L.; Addessi, E.; Amici, F.; Anderson, R. C.; Aureli, F.; Baker, J. M.; Bania, A. E.; Barnard, A. M.; Boogert, N. J.; Brannon, E. M.; Bray, E. E.; Bray, J.; Brent, L. J. N.; Burkart, J. M.; Call, J.; Cantlon, J. F.; Cheke, L. G.; Clayton, N. S.; Delgado, M. M.; DiVincenti, L. J.; Fujita, K.; Herrmann, E.; Hiramatsu, C.; Jacobs, L. F.; Jordan, K. E.; Laude, J. R.; Leimgruber, K. L.; Messer, E. J. E.; de A. Moura, A. C.; Ostojić, L.; Picard, A.; Platt, M. L.; Plotnik, J. M.; Range, F.; Reader, S. M.; Reddy, R. B.; Sandel, A. A.; Santos, L. R.; Schumann, K.; Seed, A. M.; Sewall, K. B.; Shaw, R. C.; Slocombe, K. E.; Su, Y.; Takimoto, A.; Tan, J.; Tao, R.; van Schaik, C. P.; Virányi, Z.; Visalberghi, E.; Wade, J. C.; Watanabe, A.; Widness, J.; Young, J. K.; Zentall, T. R.; Zhao, Y. The evolution of self-control, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 20 | DOI

[61] Mahler, D. L.; Ingram, T.; Revell, L. J.; Losos, J. B. Exceptional convergence on the macroevolutionary landscape in island lizard radiations, Science, Volume 341 (2013) no. 6143, pp. 292-295 | DOI

[62] Maliet, O.; Hartig, F.; Morlon, H. A model with many small shifts for estimating species-specific diversification rates, Nature Ecology & Evolution, Volume 3 (2019) no. 7, pp. 1086-1092 | DOI

[63] Maliet, O.; Morlon, H. Fast and accurate estimation of species-specific diversification rates using data augmentation, Systematic Biology, Volume 71 (2021) no. 2, pp. 353-366 | DOI

[64] Many Primates; Altschul, D. M.; Beran, M. J.; Bohn, M.; Call, J.; DeTroy, S.; Duguid, S. J.; Egelkamp, C. L.; Fichtel, C.; Fischer, J.; Flessert, M.; Hanus, D.; Haun, D. B. M.; Haux, L. M.; Hernandez-Aguilar, R. A.; Herrmann, E.; Hopper, L. M.; Joly, M.; Kano, F.; Keupp, S.; Melis, A. P.; Motes Rodrigo, A.; Ross, S. R.; Sánchez-Amaro, A.; Sato, Y.; Schmitt, V.; Schweinfurth, M. K.; Seed, A. M.; Taylor, D.; Völter, C. J.; Warren, E.; Watzek, J. Establishing an infrastructure for collaboration in primate cognition research, PLOS ONE, Volume 14 (2019) no. 10 | DOI

[65] Matzke, N. J. Probabilistic historical biogeography: New models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing, Frontiers of Biogeography, Volume 5 (2013) no. 4 | DOI

[66] Matzke, N. J. Stochastic mapping under biogeographical models. , PhyloWiki BioGeoBEARS, 2016 (http://phylo.wikidot.com/biogeobears-stochastic-mapping)

[67] Melchionna, M.; Mondanaro, A.; Serio, C.; Castiglione, S.; Di Febbraro, M.; Rook, L.; Diniz-Filho, J. A. F.; Manzi, G.; Profico, A.; Sansalone, G.; Raia, P. Macroevolutionary trends of brain mass in Primates, Biological Journal of the Linnean Society, Volume 129 (2019), pp. 14-25 | DOI

[68] Merceron, G.; Scott, J.; Scott, R. S.; Geraads, D.; Spassov, N.; Ungar, P. S. Folivory or fruit/seed predation for Mesopithecus, an earliest colobine from the late Miocene of Eurasia?, Journal of Human Evolution, Volume 57 (2009) no. 6, pp. 732-738 | DOI

[69] Milham, M. P.; Ai, L.; Koo, B.; Xu, T.; Amiez, C.; Balezeau, F.; Baxter, M. G.; Blezer, E. L.; Brochier, T.; Chen, A.; Croxson, P. L.; Damatac, C. G.; Dehaene, S.; Everling, S.; Fair, D. A.; Fleysher, L.; Freiwald, W.; Froudist-Walsh, S.; Griffiths, T. D.; Guedj, C.; Hadj-Bouziane, F.; Ben Hamed, S.; Harel, N.; Hiba, B.; Jarraya, B.; Jung, B.; Kastner, S.; Klink, P. C.; Kwok, S. C.; Laland, K. N.; Leopold, D. A.; Lindenfors, P.; Mars, R. B.; Menon, R. S.; Messinger, A.; Meunier, M.; Mok, K.; Morrison, J. H.; Nacef, J.; Nagy, J.; Rios, M. O.; Petkov, C. I.; Pinsk, M.; Poirier, C.; Procyk, E.; Rajimehr, R.; Reader, S. M.; Roelfsema, P. R.; Rudko, D. A.; Rushworth, M. F.; Russ, B. E.; Sallet, J.; Schmid, M. C.; Schwiedrzik, C. M.; Seidlitz, J.; Sein, J.; Shmuel, A.; Sullivan, E. L.; Ungerleider, L.; Thiele, A.; Todorov, O. S.; Tsao, D.; Wang, Z.; Wilson, C. R.; Yacoub, E.; Ye, F. Q.; Zarco, W.; Zhou, Y.-d.; Margulies, D. S.; Schroeder, C. E. An open resource for non-human primate imaging, Neuron, Volume 100 (2018) no. 1, pp. 61-74 | DOI

[70] Milton, K. Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development, American Anthropologist, Volume 83 (1981) no. 3, pp. 534-548 | DOI

[71] Minot, E. O. Effects of interspecific competition for food in breeding blue and great tits, The Journal of Animal Ecology, Volume 50 (1981) no. 2 | DOI

[72] Modolo, L.; Salzburger, W.; Martin, R. D. Phylogeography of Barbary macaques (Macaca sylvanus) and the origin of the Gibraltar colony, Proceedings of the National Academy of Sciences, Volume 102 (2005) no. 20, pp. 7392-7397 | DOI

[73] Morlon, H.; Lewitus, E.; Condamine, F. L.; Manceau, M.; Clavel, J.; Drury, J. RPANDA: An R package for macroevolutionary analyses on phylogenetic trees, Methods in Ecology and Evolution, Volume 7 (2016) no. 5, pp. 589-597 | DOI

[74] Mundry, R. Statistical issues and assumptions of phylogenetic generalized least squares, Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology, Springer Berlin Heidelberg, Berlin, Heidelberg, 2014, pp. 131-153 | DOI

[75] Navarrete, A. F.; Blezer, E. L.; Pagnotta, M.; de Viet, E. S.; Todorov, O. S.; Lindenfors, P.; Laland, K. N.; Reader, S. M. Primate brain anatomy: New volumetric MRI measurements for neuroanatomical studies, Brain, Behavior and Evolution, Volume 91 (2018) no. 2, pp. 109-117 | DOI

[76] Navarrete, A.; van Schaik, C. P.; Isler, K. Energetics and the evolution of human brain size, Nature, Volume 480 (2011) no. 7375, pp. 91-93 | DOI

[77] Nuismer, S. L.; Harmon, L. J. Predicting rates of interspecific interaction from phylogenetic trees, Ecology Letters, Volume 18 (2015) no. 1, pp. 17-27 | DOI

[78] Olupot, W.; Waser, P. M.; Chapman, C. A. Fruit finding by mangabeys (Lophocebus albigena): Are monitoring of fig trees and use of sympatric frugivore calls possible strategies?, International Journal of Primatology, Volume 19 (1998) no. 2, pp. 339-353 | DOI

[79] Pavoine, S.; Bonsall, M. B.; Davies, T. J.; Masi, S. Mammal extinctions and the increasing isolation of humans on the tree of life, Ecology and Evolution, Volume 9 (2019) no. 3, pp. 914-924 | DOI

[80] Pearce, F.; Carbone, C.; Cowlishaw, G.; Isaac, N. J. B. Space-use scaling and home range overlap in primates, Proceedings of the Royal Society B: Biological Sciences, Volume 280 (2013) no. 1751 | DOI

[81] Pennell, M. W.; Eastman, J. M.; Slater, G. J.; Brown, J. W.; Uyeda, J. C.; FitzJohn, R. G.; Alfaro, M. E.; Harmon, L. J. geiger v2.0: An expanded suite of methods for fitting macroevolutionary models to phylogenetic trees, Bioinformatics, Volume 30 (2014) no. 15, pp. 2216-2218 | DOI

[82] Pepperberg, I. M. Allospecific referential speech acquisition in grey parrots (Psittacus erithacus): Evidence for multiple levels of avian vocal imitation. In: Imitation in Animals and Artifacts, MIT Press (2002), pp. 109-131 | DOI

[83] Persson, T.; Sauciuc, G.-A.; Madsen, E. A. Spontaneous cross-species imitation in interactions between chimpanzees and zoo visitors, Primates, Volume 59 (2018) no. 1, pp. 19-29 | DOI

[84] Pigot, A. L.; Tobias, J. A. Species interactions constrain geographic range expansion over evolutionary time, Ecology Letters, Volume 16 (2013) no. 3, pp. 330-338 | DOI

[85] Porter, L. M. Benefits of polyspecific associations for the Goeldi?s monkey (Callimico goeldii), American Journal of Primatology, Volume 54 (2001) no. 3, pp. 143-158 | DOI

[86] Powell, L. E.; Barton, R. A.; Street, S. E. Maternal investment, life histories and the evolution of brain structure in primates, Proceedings of the Royal Society B: Biological Sciences, Volume 286 (2019) no. 1911 | DOI

[87] Powell, L. E.; Isler, K.; Barton, R. A. Re-evaluating the link between brain size and behavioural ecology in primates, Proceedings of the Royal Society B: Biological Sciences, Volume 284 (2017) no. 1865 | DOI

[88] Price, T. D.; Kirkpatrick, M. Evolutionarily stable range limits set by interspecific competition, Proceedings of the Royal Society B: Biological Sciences, Volume 276 (2009) no. 1661, pp. 1429-1434 | DOI

[89] R Core Team R: A language and environment for statistical computing. R, Foundation for Statistical Computing, Vienna, Austria, 2020 (https://www.r-project.org/)

[90] Rabosky, D. L.; Lovette, I. J. Density-dependent diversification in North American wood warblers, Proceedings of the Royal Society B: Biological Sciences, Volume 275 (2008) no. 1649, pp. 2363-2371 | DOI

[91] Rafacz, M.; Templeton, J. J. Environmental unpredictability and the value of social information for foraging starlings, Ethology, Volume 109 (2003) no. 12, pp. 951-960 | DOI

[92] Ramdarshan, A.; Merceron, G.; Marivaux, L. Spatial and temporal ecological diversity amongst eocene primates of france: Evidence from teeth, American Journal of Physical Anthropology, Volume 147 (2012) no. 2, pp. 201-216 | DOI

[93] Reader, S. M.; Laland, K. N. Social intelligence, innovation, and enhanced brain size in primates, Proceedings of the National Academy of Sciences, Volume 99 (2002) no. 7, pp. 4436-4441 | DOI

[94] Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things), Methods in Ecology and Evolution, Volume 3 (2012) no. 2, pp. 217-223 | DOI

[95] Robira, B.; Benhamou, S.; Masi, S.; Llaurens, V.; Riotte-Lambert, L. Foraging efficiency in temporally predictable environments: Is a long-term temporal memory really advantageous?, Royal Society Open Science, Volume 8 (2021) no. 9 | DOI

[96] Robira, B.; Perez-Lamarque, B. Primate sympatry shapes the evolution of their brain architecture (Data, scripts, codes), Zenodo, 2023a | DOI

[97] Robira, B.; Perez-Lamarque, B. Primate sympatry shapes the evolution of their brain architecture (Supplementary Materials), Zenodo, 2023b | DOI

[98] Rosati, A. G. Foraging cognition: Reviving the ecological intelligence hypothesis, Trends in Cognitive Sciences, Volume 21 (2017) no. 9, pp. 691-702 | DOI

[99] Sayol, F.; Lapiedra, O.; Ducatez, S.; Sol, D. Larger brains spur species diversification in birds, Evolution, Volume 73 (2019) no. 10, pp. 2085-2093 | DOI

[100] Schilder, B. M.; Petry, H. M.; Hof, P. R. Evolutionary shifts dramatically reorganized the human hippocampal complex, Journal of Comparative Neurology, Volume 528 (2020) no. 17, pp. 3143-3170 | DOI

[101] Schreier, B. M.; Harcourt, A. H.; Coppeto, S. A.; Somi, M. F. Interspecific competition and niche separation in primates: A global analysis, Biotropica, Volume 41 (2009) no. 3, pp. 283-291 | DOI

[102] Shettleworth, S. J. Cognition, evolution, and behavior, Oxford university press, 2009 (https://global.oup.com/academic/product/cognition-evolution-and-behavior-9780195319842?cc=us&lang=en&)

[103] Shultz, S.; Dunbar, R. Chimpanzee and felid diet composition is influenced by prey brain size, Biology Letters, Volume 2 (2006) no. 4, pp. 505-508 | DOI

[104] Slater, G. J.; Harmon, L. J.; Wegmann, D.; Joyce, P.; Revell, L. J.; Alfaro, M. E. Fitting models of continuous trait evolution to incompletely sampled comparative data using approximate bayesian computation, Evolution, Volume 66 (2012) no. 3, pp. 752-762 | DOI

[105] Smaers, J. B.; Rothman, R. S.; Hudson, D. R.; Balanoff, A. M.; Beatty, B.; Dechmann, D. K. N.; de Vries, D.; Dunn, J. C.; Fleagle, J. G.; Gilbert, C. C.; Goswami, A.; Iwaniuk, A. N.; Jungers, W. L.; Kerney, M.; Ksepka, D. T.; Manger, P. R.; Mongle, C. S.; Rohlf, F. J.; Smith, N. A.; Soligo, C.; Weisbecker, V.; Safi, K. The evolution of mammalian brain size, Science Advances, Volume 7 (2021) no. 18 | DOI

[106] Sokolov, A. A.; Miall, R. C.; Ivry, R. B. The cerebellum: Adaptive prediction for movement and cognition, Trends in Cognitive Sciences, Volume 21 (2017) no. 5, pp. 313-332 | DOI

[107] Sol, D.; Székely, T.; Liker, A.; Lefebvre, L. Big-brained birds survive better in nature, Proceedings of the Royal Society B: Biological Sciences, Volume 274 (2007) no. 1611, pp. 763-769 | DOI

[108] Springer, M. S.; Meredith, R. W.; Gatesy, J.; Emerling, C. A.; Park, J.; Rabosky, D. L.; Stadler, T.; Steiner, C.; Ryder, O. A.; Janečka, J. E.; Fisher, C. A.; Murphy, W. J. Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix, PLoS ONE, Volume 7 (2012) no. 11 | DOI

[109] Tung Ho, L. s.; Ané, C. A linear-time algorithm for Gaussian and non-Gaussian trait evolution models, Systematic Biology, Volume 63 (2014) no. 3, pp. 397-408 | DOI

[110] Todorov, O. S.; Weisbecker, V.; Gilissen, E.; Zilles, K.; de Sousa, A. A. Primate hippocampus size and organization are predicted by sociality but not diet, Proceedings of the Royal Society B: Biological Sciences, Volume 286 (2019) no. 1914 | DOI

[111] Tomasello, M. The cultural origins of human cognition, Harvard University Press, 2019 (https://www.hup.harvard.edu/catalog.php?isbn=9780674005822)

[112] Trapanese, C.; Robira, B.; Tonachella, G.; di Gristina, S.; Meunier, H.; Masi, S. Where and what? Frugivory is associated with more efficient foraging in three semi-free ranging primate species, Royal Society Open Science, Volume 6 (2019) no. 5 | DOI

[113] van Schaik, C. P.; Burkart, J. M. Social learning and evolution: the cultural intelligence hypothesis, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 366 (2011) no. 1567, pp. 1008-1016 | DOI

[114] van Schaik, C. P.; Triki, Z.; Bshary, R.; Heldstab, S. A. A farewell to the encephalization quotient: A new brain size measure for comparative primate cognition, Brain, Behavior and Evolution, Volume 96 (2021) no. 1, pp. 1-12 | DOI

[115] Weir, J. T.; Mursleen, S. Diversity-dependent cladogenesis and trait evolution in the adaptive radiation of the auks (Aves Alcidae), Evolution, Volume 67 (2013) no. 2, pp. 403-416 | DOI

[116] Whiten, A.; van Schaik, C. P. The evolution of animal ‘cultures’ and social intelligence, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 362 (2007) no. 1480, pp. 603-620 | DOI

[117] Willems, E. P.; Hellriegel, B.; van Schaik, C. P. The collective action problem in primate territory economics, Proceedings of the Royal Society B: Biological Sciences, Volume 280 (2013) no. 1759 | DOI

[118] Wilson, A. From molecular evolution to body and brain evolution In: Perspectives on cellular regulation: From bacteria to cancer, J. Wiley & Sons (1991), pp. 331-340

[119] Wiltgen, B. J.; Brown, R. A.; Talton, L. E.; Silva, A. J. New circuits for old memories, Neuron, Volume 44 (2004) no. 1, pp. 101-108 | DOI

[120] Wisniewski, A. L.; Lloyd, G. T.; Slater, G. J. Extant species fail to estimate ancestral geographical ranges at older nodes in primate phylogeny, Proceedings of the Royal Society B: Biological Sciences, Volume 289 (2022) no. 1975 | DOI

[121] Zeileis, A. Implementing a class of structural change tests: An econometric computing approach, Computational Statistics & Data Analysis, Volume 50 (2006) no. 11, pp. 2987-3008 | DOI

[122] Zeileis, A.; Kleiber, C.; Krämer, W.; Hornik, K. Testing and dating of structural changes in practice, Computational Statistics & Data Analysis, Volume 44 (2003) no. 1-2, pp. 109-123 | DOI

[123] Zeileis, A.; Leisch, F.; Hornik, K.; Kleiber, C. Strucchange: An R package for testing for structural change in linear regression models, Journal of Statistical Software, Volume 7 (2002) no. 2, pp. 1-38 | DOI

Cited by Sources: