Evolutionary and biomedical implications of sex differences in the primate brain transcriptome.

Data and code availability. RNA-seq data have been deposited in the Gene Expression Omnibus (GEO) and are publicly available as of the date of publication. Accession numbers are listed in the key resources table. All code has been deposited in a publicly available GitHub Repository and an unchanging archive of this repository was created in Zenodo. Links to both repositories are listed in the key resources table Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.This is the final version. Available from Cell Press via the DOI in this record. Humans exhibit sex differences in the prevalence of many neurodevelopmental disorders and neurodegenerative diseases. Here, we generated one of the largest multi-brain-region bulk transcriptional datasets for the rhesus macaque and characterized sex-biased gene expression patterns to investigate the translatability of this species for sex-biased neurological conditions. We identify patterns similar to those in humans, which are associated with overlapping regulatory mechanisms, biological processes, and genes implicated in sex-biased human disorders, including autism. We also show that sex-biased genes exhibit greater genetic variance for expression and more tissue-specific expression patterns, which may facilitate rapid evolution of sex-biased genes. Our findings provide insights into the biological mechanisms underlying sex-biased disease and support the rhesus macaque model for the translational study of these conditions.National Institutes of HealthNational Science FoundationNational Institute of Mental Healt

Social connections predict brain structure in a multidimensional free-ranging primate society

This is the final version. Available on open access from the American Association for the Advancement of Science via the DOI in this recordData and materials availability: All data, code, and materials used in this study are available on the Open Science Framework platform (osf.io). Link: https://osf.io/xfz3r/?view_only=66633a9490e649038330a98788a0cca3. Original brain tissue samples can be provided by the University of Pennsylvania pending scientific review and a completed material transfer agreement. Requests for brain tissues should be submitted to: [email protected] and survival in most primate species reflects management of both competitive and cooperative relationships. Here, we investigated the links between neuroanatomy and sociality in free-ranging rhesus macaques. In adults, the number of social partners predicted the volume of the mid-superior temporal sulcus and ventral-dysgranular insula, implicated in social decision-making and empathy, respectively. We found no link between brain structure and other key social variables such as social status or indirect connectedness in adults, nor between maternal social networks or status and dependent infant brain structure. Our findings demonstrate that the size of specific brain structures varies with the number of direct affiliative social connections and suggest that this relationship may arise during development. These results reinforce proposed links between social network size, biological success, and the expansion of specific brain circuits

Cognitive performance is linked to group size and affects fitness in Australian magpies

This is the author accepted manuscript. The final version is available from Springer Nature via the DOI in this recordThe social intelligence hypothesis states that the demands of social life drive cognitive evolution. This idea receives support from comparative studies that link variation in group size or mating systems with cognitive and neuroanatomical differences across species, but findings are contradictory and contentious. To understand the cognitive consequences of sociality, it is also important to investigate social variation within species. Here we show that in wild, cooperatively breeding Australian magpies, individuals that live in large groups show increased cognitive performance, which is linked to increased reproductive success. Individual performance was highly correlated across four cognitive tasks, indicating a 'general intelligence factor' that underlies cognitive performance. Repeated cognitive testing of juveniles at different ages showed that the correlation between group size and cognition emerged in early life, suggesting that living in larger groups promotes cognitive development. Furthermore, we found a positive association between the task performance of females and three indicators of reproductive success, thus identifying a selective benefit of greater cognitive performance. Together, these results provide intraspecific evidence that sociality can shape cognitive development and evolution.This work was funded by an ARC Discovery grant awarded to A.R.R., A.T. and M. B. V. Bell, and a University of Western Australia International Postgraduate Research Scholarship and Endeavour Research Fellowship awarded to B.J.A. A.T. received additional support from a BBSRC David Phillips Fellowship (BB/H021817/1)

Sociality does not drive the evolution of large brains in eusocial African mole-rats

The social brain hypothesis (SBH) posits that the demands imposed on individuals by living in cohesive social groups exert a selection pressure favouring the evolution of large brains and complex cognitive abilities. Using volumetry and the isotropic fractionator to determine the size of and numbers of neurons in specific brain regions, here we test this hypothesis in African mole-rats (Bathyergidae). These subterranean rodents exhibit a broad spectrum of social complexity, ranging from strictly solitary through to eusocial cooperative breeders, but feature similar ecologies and life history traits. We found no positive association between sociality and neuroanatomical correlates of information-processing capacity. Solitary species are larger, tend to have greater absolute brain size and have more neurons in the forebrain than social species. The neocortex ratio and neuronal counts correlate negatively with social group size. These results are clearly inconsistent with the SBH and show that the challenges coupled with sociality in this group of rodents do not require brain enlargement or fundamental reorganization. These findings suggest that group living or pair bonding per se does not select strongly for brain enlargement unless coupled with Machiavellian interactions affecting individual fitness.The Czech Science Foundation (14–2758 S, to P.N.), Grant Agency of Charles University (325515, to K.K.) and the European Social Fund and the state budget of the Czech Republic (CZ.1.07/2.3.00/30.0022, to S.O.).http://www.nature.com/srepam2018Mammal Research InstituteZoology and Entomolog