Comparative Primatology Research Articles

Lessons from comparative primatology for understanding trait covariation and diversity in evolutionary ecology

ABSTRACT Given the position of humans in the tree of life, comparative research on non‐human primates has attracted the interest of researchers in biology, medical sciences, anthropology, psychology, and sociology. Covariation of species' phenotypes has been of particular interest. Learning from the historical development of comparative research with primates should thus be particularly valuable for evolutionary ecology and to improve understanding of phenotypic integration and diversity. Such learning would also help identify knowledge gaps, disputed questions, and new avenues of both basic and applied research in relation to the evolution of primate features and the conservation of our close relatives. We conducted a historical assessment through a non‐systematic review and a systematic review, focusing on how the integration of different research lines in evolutionary ecology focused on primate phenotypic covariation unfolded throughout the 20th Century. The non‐systematic review allowed us to reconstruct the history of the discipline from its earliest origins, when bibliometric assessments were more limited in scope, and to identify the most appropriate keywords for the systematic review. We employed a standard protocol for the systematic review, applying two complementary analyses: co‐occurrence of keywords and bibliographic coupling of references. These analyses described the development of the conceptual and intellectual structures of comparative primatology from 1966 to 2020. By identifying the most influential researchers and concept interrelations, we highlight primate phenotypes critical for the development of the discipline (in particular, brain and body sizes and behavioural patterns), showcasing the reach of these investigations for evolutionary ecology. Overall, our findings emphasise the crucial role that comparative primatology has played in developing the study of phenotypic integration and the very onset of phylogenetic comparative methods.

The origins of children's understanding of technologies: A focused rapid review of three approaches

How children's understanding of emerging technologies originates is a critical, fundamental, and challenging research question. Placing this question in the history of human evolution and technology development, the present article uses a newly designed literature review method, focused rapid review, to synthesize three fields of research, developmental psychology, behavioral archaeology, and comparative primatology. The six highly cited empirical studies highlighted in the review demonstrate how infants understand simple artifacts, how ancient humans made, used, and understood stone technologies, and how non-human primates make, use, and understand simple tools. The article concludes with a discussion of four implications for examining the origins of children's understanding of emerging technologies in a broader intellectual context.

Multilevel selection and Tomasello’s A Natural History of Human Morality: A translation manual

ABSTRACTTomasello’s view of comparative primatology and human evolution is part of an emerging paradigm and his main empirical contribution has been the comparative study of great apes and human children. He has also contributed to the overall theoretical framework, but his rendering of the major theories of social evolution – such as kin selection, reciprocity, and levels of selection – is problematic. To correct this problem, I briefly review the concept of equivalence (theories that invoke the same causal processes from different perspectives) and provide a “translation manual” so that the thesis of Tomasello’s book can be seen more clearly and better related to the work of others who are helping to develop the same paradigm.

The meat of the matter: an evolutionary perspective on human carnivory

ABSTRACTNatural selection, as both a process and a scientific concept, is eloquently simple. Unfortunately, this simplicity sometimes belies Darwin’s broader view of evolution as a multifaceted process that proceeds from both ecological pressures and phylogenetic history. Darwin further understood that it is not just physical traits that are transmitted generationally, but also behavioural patterns, both of which are subject to the shaping influences of environment and phylogeny. Chimpanzees, bonobos and humans are the most carnivorous extant primates, an observation that serves as the basis of our extended argument that vertebrate predation is a synapomorphy of these sister taxa. From there, we use archaeological data to trace the inferred polarity of hominin carcass foraging and meat-eating from their first archaeological indications ∼2.6 million years ago (Mya). A review of the early Pleistocene African record demonstrates that taphonomic evidence of a hominin predatory/meat-eating behavioral module clarifies ∼2.0 Mya, a critical time period characterised by traces of advanced carcass foraging, which, in turn, suggest that an earlier phase(s) of vertebrate capture by hominins was/were simpler. In rounding out this meta-analytical consideration of hominin carnivory, we draw on comparative primatology, ecology and archaeology in order to build a holistic model of this fundamental behavioural adaptation.

The Importance of Development for Comparative Primatology

It is a truism to say that primates develop, but it is also important to acknowledge that development occurs across many domains, including motor behavior, socioemotional behavior, communication, and cognition. In this review, we focus on those aspects of development that impact social cognition outcomes in infancy. Triadic engagements, such as those of joint attention, cooperation, and intentional communication, develop in the first year of life in chimpanzees and humans. Joint attention, for example, occurs when infants coordinate their attention to a social partner while also attending to an object or event. Hominoids are strongly influenced by experiences during early development, especially experiences that are foundational for these coordinated triadic engagements. Purported species differences in triadic engagements are highlighted in current evolutionary theories of primate social cognition, but conclusions about species differences are unfounded when development is ignored. Developmental experiences must be matched, controlled, or systematically varied in experimental designs that make cross-species comparisons. Considerations of development, across species and across rearing experiences, would contribute to more accurate evolutionary theories of primate social cognition.

Neuroanatomical causes and social consequences of variation in facial motor control: what comparative primatology can teach us about autism spectrum disorders

A limited body of evidence suggests that people with severe Autism Spectrum Disorders (ASD) are generally less expressive than mental age‐matched controls. The objective of my talk is to demonstrate how a comparative primatological perspective can help to elucidate the neuroanatomical and social correlates of facial expressivity. I will review research on the evolution of facial nucleus volume in a wide range of nonhuman primates. Previous studies demonstrate that species that have relatively large facial motor nuclei tend to have larger brains, live in larger social groups, and spend more time social grooming than species with relatively small facial nuclei. These observations support the notion that the facial motor nucleus is an essential part of the network of brain regions that is impaired in ASD, i.e., the “social brain.” I will also present new results of a recent pilot study examining the correlation between emotional expressiveness and serotonin transporter genotype (5‐HTTLPR) in free‐ranging rhesus macaques (Macaca mulatta). Our preliminary findings suggest that female macaques with the SS genotype tend to be more expressive overall than LL individuals, even after controlling for dominance rank. This observation calls into question the hypothesis that the S allele is responsible for the relative lack of expressiveness observed in some people with ASD.

The Influence of Nutrition on Primate Sociality

Copyright: © 2012 Wallner B. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. This editorial is based on two comprehensive reviews about the effects of nutrients on aggressive, respectively, impulsive behavior in comparative primatology [1,2]. The aim of this work is to highlight the importance of feeding ecology in primates either in experimental or in field studies in relation to its modulatory effects on aggression and its impact to sociality and social styles. Aggressive behavior can be generated, stimulated, and modulated through both intrinsic and extrinsic factors, e.g. social and nutritional influences, endocrine, and neurophysiological regulatory mechanisms. Most of these factors are interrelated and seemed to play important roles during evolutionary adaptative processes.

The evolutionary biology of child health.

I apply evolutionary perspectives and conceptual tools to analyse central issues underlying child health, with emphases on the roles of human-specific adaptations and genomic conflicts in physical growth and development. Evidence from comparative primatology, anthropology, physiology and human disorders indicates that child health risks have evolved in the context of evolutionary changes, along the human lineage, affecting the timing, growth-differentiation phenotypes and adaptive significance of prenatal stages, infancy, childhood, juvenility and adolescence. The most striking evolutionary changes in humans are earlier weaning and prolonged subsequent pre-adult stages, which have structured and potentiated maladaptations related to growth and development. Data from human genetic and epigenetic studies, and mouse models, indicate that growth, development and behaviour during pre-adult stages are mediated to a notable degree by effects from genomic conflicts and imprinted genes. The incidence of cancer, the primary cause of non-infectious childhood mortality, mirrors child growth rates from birth to adolescence, with paediatric cancer development impacted by imprinted genes that control aspects of growth. Understanding the adaptive significance of child growth and development phenotypes, in the context of human-evolutionary changes and genomic conflicts, provides novel insights into the causes of disease in childhood.

Comparative primatology attempts to explain differences but not to judge them

Chimpanzees are one of the most flexible and diverse primate species known today (McGrew et al. 1996; Wrangham et al. 1994; Mitani et al. 2002), and with each new population studied, new behavioural and social aspects of this species are revealed (Sanz et al. 2009; Boesch et al. 2009; Pruetz 2007; Pruetz and Bertolani 2007). As a result of this, one of the challenges we currently face is documenting and explaining how such diversity between populations came about in chimpanzees. I wrote my book, ‘‘The real chimpanzee: sex strategies in the Forest’’ (Boesch 2009), with the intention of exploring the important social and reproductive diversity seen in chimpanzees, as I clearly state on pages 5 and 6 of my introduction. The conclusion of my book is that:

Performance of distance-based DNA barcoding in the molecular identification of Primates

For comparative primatology proper recognition of basal taxa (i.e. species) is indispensable, and in this the choice of a suitable gene with high phylogenetic resolution is crucial. For the goals of species identification in animals, the cytochrome c oxidase subunit 1 ( cox1) has been introduced as standard marker. Making use of the difference in intra- and interspecific genetic variation – the DNA barcoding gap – cox1 can be used as a fast and accurate marker for the identification of animal species. For the Order Primates we compare the performance of cox1 (166 sequences; 50 nominal species) in species-identification with that of two other mitochondrial markers, 16S ribosomal RNA (412 sequences, 92 species) and cytochrome b ( cob: 547 sequences, 72 species). A wide gap exist between intra- and interspecific divergences for both cox1 and cob genes whereas this gap is less apparent for 16S, indicating that rRNA genes are less suitable for species delimitation in DNA barcoding. For those species where multiple sequences are available there are significant differences in the intraspecific genetic distances between different mitochondrial markers, without, however, showing a consistent pattern. We conclude that cox1 allows accurate differentiation of species and as such DNA barcoding may have an important role to play in comparative primatology.

Human mating models can benefit from comparative primatology and careful methodology

Conditional mating strategies and within-sex variation in mating patterns occur across a wide range of primate taxa. Attempts to model the evolution of human mating strategies should incorporate current primatological data sets and phylogenetic perspectives. However, comparisons between interview and questionnaire-based human behavioral data and observationally and experimental generated nonhuman behavioral data should be conducted with prudence.

Reaching into Thought: The Minds of the Great Apes

1. Exploring the minds of the great apes: Issues and controversies Anne E. Russon and Kim A. Bard Part I. The Scope of Great Ape Intelligence: 2. Chimpanzees and capuchin monkeys: Comparative cognition James R. Anderson 3. Acting and understanding: tool use revisited through the minds of capuchin monkeys Elisabetta Visalberghi and Luca Limongelli 4. Consolation, reconciliation, and a possible cognitive difference between macaques and chimpanzees Frans B.M. de Waal and Filippo Aureli 5. The misunderstood ape: Cognitive skills of the gorilla Richard W. Byrne 6. Ostensive behavior in great apes: the role of eye contact Juan Carlos Gomez 7. Imitation in everyday use: matching and rehearsal in the spontaneous imitation of rehabilitant orangutans Anne E. Russon 8. 'More is less': the elicitation of rule-governed resource distribution in chimpanzees Sarah T. Boysen 9. Tool-using behavior in wild Pan paniscus: Social and ecological considerations Ellen J. Ingmanson 10. Comparison of chimpanzee material culture between Bossou and Nimba, West Africa Tetsuro Matsuzawa and Gen Yamakoshi Part II. Organization of Great Ape Intelligence: Development, Culture and Evolution: 11. Influences on development in infant chimpanzees: Enculturation, temperament and cognition Kim A. Bard and Kathryn H. Gardner 12. Heterochrony and the evolution of primate cognitive development Jonas Langer 13. Simon says: The development of imitation in an enculturated orangutan H. Lyn Miles, Robert W. Mitchell and Stephen E. Harper 14. Imitation, pretense, and mindreading: secondary representation in comparative primatology and developmental psychology? Andrew Whiten 15. Self-awareness and self-knowledge in humans, apes and monkeys Daniel Hart and Mary Pat Karmel 16. Apprenticeship in tool-mediated extractive foraging: the origins of imitation, teaching and self-awareness in great apes Sue Taylor Parker 17. The effect of humans on the cognitive development of apes Josep Call and Michael Tomasello 18. Three approaches for assessing chimpanzee culture Christophe Boesch 19. On the wild side of culture and cognition in the great apes Sue Taylor Parker and Anne E. Russon Index.

Ape language in a new light

1. The enemy within Comparative primatology is a subversive enterprise. Not of humanist prejudices; these were subverted a long time ago. It is rather Cognitive Science that is being transformed by ape language studies. For Cognitive Science was originally conceived on the post-computational mechanist paradigm (see Shanker, 1992). But primatology is usurping the pivotal role hitherto played by AI. It offers as an alternative to the study of artificial ‘toy domains’ an actual species whose cognitive capacities seem roughly comparable to that of the preverbal infant (with debates over whether chimpanzees can think taking the place of the 1960s debates over whether machines can think). But whereas AI was almost exclusively concerned with problem-solving, comparative primatology has placed the focus on languagelearning. Far more is involved here than a simple shift in subject-matter. Comparative primatologists have so far sought to present their work within the framework of what we might call classical Cognitive Science in order to establish how chimpanzees can be said to possess more sophisticated cognitive abilities than either linguists or ethologists have hitherto been prepared to concede. On this picture, the cognitive mechanisms which guide non-human primate behaviour are seen as an even greater mystery than those of humans; for our ability to penetrate the chimpanzee’s mind is said to be severely limited by the fact that we cannot communicate with our subjects. But through the combined use of controlled experiments (both laboratory and field), and the theoretical constructs afforded by information-processing models, we can justifiably infer that non-human primates are capable of such things as analogical reasoning (however limited this might be). It little matters that comparative primatology is endeavouring to establish itself within the orbit of classical Cognitive Science, however; for often the most subversive movements are those that are unaware of the fact. On the variant reading which will be explored in this paper, primatology is actually undermining the framework it has embraced. This entails a sharp conflict between theory and practice. It means that what comparative primatologists are doing calls into question the very theories they seek to instantiate. This is a result of the fact that the field is engaged in both a conceptual and an empirical investigation. For example, in How Monkeys See the World, Cheney and Seyfarth speculate that

The hominoid os capitatum, with special reference to the fossil bones from Sterkfontein and Olduvai Gorge

Current speculations about australopithecine hand function undoubtedly derive in large measure from the published reports on the Sterkfontein capitate. The credibility of these reports is, however, gravely impaired when the inadequacy of the then available comparative morphological data is realized; this paper attempts to rectify this important hiatus in comparative primatology. A detailed description is given of the form of the os capitatum in living hominoids, of the joints in which it participates, and of the functional import of these features. It is shown that the Sterkfontein capitate, far from being essentially human in appearance (an oft-quoted statement), conserves, with but little progressive modification, important biomechanical characteristics still found in Pan. There are indications that the capitate from Bed I, Olduvai Gorge, although badly damaged, was essentially similar in form.