The effect of genotype on attention bias in rhesus macaques, Macaca mulatta, as a welfare indicator.

Rhesus macaques, Macaca mulatta, are one of the most commonly used non-human primates in biomedical research in the UK. Their welfare is of great concern for both ethical and quality-of-science reasons. Attention bias (AB), a measure of cognitive bias, assesses whether an individual is stressed, predicts vulnerability to stress, and identifies the effectiveness of interventions to improve well-being. In both humans and macaques, genetic factors can result in variation of behavioural traits, attentional processes and susceptibility to stress-related neuropsychiatric disorders.Here, sixty-five female macaques were genotyped for known variants in the following genes: serotonin transporter (5-HTTLPR; short and long allele), tryptophan hydroxylase 2 (TPH2; short and long allele), monoamine oxidase A (MAOA; 5-, 6- and 7-repeat allele) and mu-opioid receptor (OPRM1; C and G allele). Additionally, sequencing was utilised to identify novel SNPs in the dopamine receptor D4 (DRD4). The 5-HTTLPR short-, TPH2 long-, MAOA 7-repeat and OPRM1 G-allele are low-expressing alleles leading to lower levels of circulating neurotransmitters in the brain, and have been shown to be linked to anxiety, coping mechanisms and vulnerability to stress in macaques. Twenty-nine of the genotyped macaques underwent AB testing with conspecific stimuli (aggressive vs. neutral facial expression, Experiment 1) and stimuli of the facilitie’s veterinarian (photograph vs. pixelated photograph, Experiment 2). Additionally, to assess the effectiveness of habituation to change cognitive responses and improve well-being, females underwent different amounts of habituation to the veterinarian. Video footage was blind-coded for gaze towards stimuli and female’s behaviour following AB tests was recorded. Associations between AB scores, other behavioural measures, and these genetic polymorphisms were investigated in the R package and in SPSS.In Experiment 1, females were more avoidant of aggressive conspecific stimuli when they carried the HTTLPR short- or MAOA 5- and 6-repeat allele and in Experiment 2 females were more avoidant of vet photographs when they carried HTTLPR long- plus TPH2 short alleles only. DRD4 T-allele carriers showed increased amounts of aggressive behaviours and MAOA 7- repeat allele carriers showed increased amounts of affiliative and reduced amounts of maintenance behaviours. Genotype did not have an effect on habituation in Experiment 2, but the more habituation females received the less vigilant they became for the vet photograph.This was the first study showing that genotype impacts on AB in macaques. Advice on further development of methods and future studies is given

Physiological stress response of African elephants to wildlife tourism in Madikwe Game Reserve, South Africa

Context: Wildlife tourism has been shown to increase stress in a variety of species and can negatively affect individuals’ survival, reproduction, welfare, and behaviour. In African elephants Loxodonta africana increased physiological stress has been linked to use of refugia, rapid movement through corridors, and heightened aggression towards humans. However, we are unaware of any studies assessing the impact of tourist pressure (tourist numbers) on physiological stress in elephants. Aims: We used faecal glucocorticoid metabolite (fGCM) concentrations to investigate whether tourist numbers in Madikwe Game Reserve, South Africa, were related to changes in physiological stress in elephants. Methods: We repeatedly collected dung samples (n=43) from 13 individually identified elephants over 15 months. Using a Generalised Linear Mixed Model and a Kenward-Roger approximation, we assessed the impact of monthly tourist numbers, season, age, and sex on elephant fGCM concentrations. Key results: High tourist numbers were significantly related to elevated fGCM concentrations. Overall, fGCM concentrations increased by 112% (from 0.26 to 0.55 µg/g dry weight) in the months with highest tourist pressure, compared to months with lowest tourist pressure. Conclusions: Managers of fenced reserves should consider providing potential alleviation measures for elephants during high tourist pressure, for example, by ensuring refuge areas are available. This may be of even higher importance if elephant populations have had traumatic experiences with humans in the past, such as poaching or translocation. Such management action will improve elephant welfare and increase tourist safety. Implications: Whilst tourism can generate substantial revenue to support conservation action, careful monitoring of its impact on wildlife is required to manage potential negative effects

Genetic polymorphisms in the serotonin, dopamine and opioid pathways influence social attention in rhesus macaques (Macaca mulatta)

Behaviour has a significant heritable component; however, unpicking the variants of interest in the neural circuits and molecular pathways that underpin these has proven difficult. Here, we present a comprehensive analysis of the relationship between known and new candidate genes from identified pathways and key behaviours for survival in 109 adult rhesus macaques (Macaca mulatta). Eight genes involved in emotion were analysed for variation at a total of nine loci. Genetic data were then correlated with cognitive and observational measures of behaviour associated with wellbeing and survival using MCMC-based Bayesian GLMM in R, to account for relatedness within the macaque population. For four loci the variants genotyped were length polymorphisms (SLC6A4 5-hydroxytryptamine transporter length-polymorphic repeat (5-HTTLPR), SLC6A4 STin polymorphism, Tryptophan 5- hydroxylase 2 (TPH2) and Monoamine oxidase A (MAOA)) whilst for the other five (5- hydroxytryptamine receptor 2A (HTR2A), Dopamine Receptor D4 (DRD4), Oxytocin receptor (OXTR), Arginine vasopressin receptor 1A (AVPR1a), Opioid receptor mu(μ) 1 (OPRM1)) SNPs were analysed. STin genotype, DRD4 haplotype and OXTR haplotype were significantly associated with the cognitive and observational measures of behaviour associated with wellbeing and survival. Genotype for 5-HTTLPR, STin and AVPR1a, and haplotype for HTR2A, DRD4 and OXTR were significantly associated with the duration of behaviours including fear and anxiety. Understanding the biological underpinnings of individual variation in negative emotion (e.g., fear and anxiety), together with their impact on social behaviour (e.g., social attention including vigilance for threat) has application for managing primate populations in the wild and captivity, as well as potential translational application for understanding of the genetic basis of emotions in humans