Genotype-by-Environment Interactions and Reliable Signaling of Male Quality in Bank Voles

Evolutionary Conflict Between Maternal and Paternal Interests: Integration with Evolutionary Endocrinology

International audience; Conflict between mates, as well as conflict between parents and offspring are due to divergent evolutionary interests of the interacting individuals. Hormone systems provide genetically based proximate mechanisms for mediating phenotypic adaptation and maladaptation characteristic of evolutionary conflict between individuals. Testosterone (T) is among the most commonly studied hormones in evolutionary biology, and as such, its role in shaping sexually dimorphic behaviors and physiology is relatively well understood, but its role in evolutionary conflict is not as clear. In this review, we outline the genomic conflicts arising within the family unit, and incorporate m…

Imagination in human social cognition, autism, and psychotic-affective conditions

Abstract Complex human social cognition has evolved in concert with risks for psychiatric disorders. Recently, autism and psychotic-affective conditions (mainly schizophrenia, bipolar disorder, and depression) have been posited as psychological ‘opposites’ with regard to social-cognitive phenotypes. Imagination, considered as ‘forming new ideas, mental images, or concepts’, represents a central facet of human social evolution and cognition. Previous studies have documented reduced imagination in autism, and increased imagination in association with psychotic-affective conditions, yet these sets of findings have yet to be considered together, or evaluated in the context of the diametric mode…

Maintenance costs of male dominance and sexually antagonistic selection in the wild

Variation in dominance status determines male mating and reproductive success, but natural selection for male dominance can be detrimental or antagonistic for female performance, and ultimately their fitness. Attaining and maintaining a high dominance status in a population of competing individuals is physiologically costly for males. But how male dominance status is mediated by maintenance energetics is currently not well understood, nor are the corresponding effects of male energetics on his sisters recognized. We conducted laboratory and field experiments on rodent populations to test whether selective breeding for male dominance status (dominant vs. subordinate breeding lines) antagonis…

Balancing selection maintains polymorphisms at neurogenetic loci in field experiments

Most variation in behavior has a genetic basis, but the processes determining the level of diversity at behavioral loci are largely unknown for natural populations. Expression of arginine vasopressin receptor 1a (Avpr1a) and oxytocin receptor (Oxtr) in specific regions of the brain regulates diverse social and reproductive behaviors in mammals, including humans. That these genes have important fitness consequences and that natural populations contain extensive diversity at these loci implies the action of balancing selection. In Myodes glareolus, Avpr1a and Oxtr each contain a polymorphic microsatellite locus located in their 5′ regulatory region (the regulatory region-associated microsatel…

Stabilizing selection on microsatellite allele length at arginine vasopressin 1a receptor and oxytocin receptor loci

The loci arginine vasopressin receptor 1a ( avpr1a ) and oxytocin receptor ( oxtr ) have evolutionarily conserved roles in vertebrate social and sexual behaviour. Allelic variation at a microsatellite locus in the 5′ regulatory region of these genes is associated with fitness in the bank vole Myodes glareolus . Given the low frequency of long and short alleles at these microsatellite loci in wild bank voles, we used breeding trials to determine whether selection acts against long and short alleles. Female bank voles with intermediate length avpr1a alleles had the highest probability of breeding, while male voles whose avpr1a alleles were very different in length had reduced probability of …

Sexual antagonism for testosterone maintains multiple mating behaviour

Summary 1. The persistence of multiple mating remains one of the fundamental questions in evolutionary biology. In theory, multiple mating is predicted to improve female fitness cumulatively through direct and ⁄ or genetic benefits. However, intra-locus sexual conflicts may potentially constrain or even eliminate these benefits owing to the gender load imposed by sexually antagonistic selection. 2. Here, we tested whether sexually antagonistic selection can maintain the variance in multiple mating behaviour of bank voles (Myodes glareolus) by manipulating the hormone testosterone through artificial selection in the laboratory. Among mammals, testosterone is a sexually dimorphic fitness-rela…

Negative frequency-dependent selection of sexually antagonistic alleles in Myodes glareolus.

Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show …

Genomic conflicts and sexual antagonism in human health: Insights from oxytocin and testosterone

We review the hypothesized and observed effects of two of the major forms of genomic conflicts, genomic imprinting and sexual antagonism, on human health. We focus on phenotypes mediated by peptide and steroid hormones (especially oxytocin and testosterone) because such hormones centrally mediate patterns of physical and behavioral resource allocation that underlie both forms of conflict. In early development, a suite of imprinted genes modulates the human oxytocinergic system as predicted from theory, with paternally inherited gene expression associated with higher oxytocin production, and increased solicitation to mothers by infants. This system is predicted to impact health through the i…

Socio-Reproductive Conflicts and the Father’s Curse Dilemma

Evolutionary conflicts between males and females can manifest over sexually antagonistic interactions at loci or over sexually antagonistic interests within a locus. The latter form of conflict, intralocus sexual conflict, arises from sexually antagonistic selection and constrains the fitness of individuals through a phenotypic compromise. These conflicts, and socio-reproductive interactions in general, are commonly mediated by hormones, and thus predictive insights can be gained from studying their mediating effects. Here, we integrate several lines of evidence to describe a novel, hormonally mediated reproductive dilemma that we call the father’s curse, which results from an intralocus co…

ESM for Watts et al. Stabilising selection on microsatellite allele length from Stabilizing selection on microsatellite allele length at arginine vasopressin 1a receptor and oxytocin receptor loci

Details of model selection procedure (Supplementary Tables 1, 2) and analyses of effect of microsatellite allele length on litter size (Supplementary Methods, Results, Supplementary Table 3).

Sex-specific effects of natural and sexual selection on the evolution of life span and ageing in Drosophila simulans

Summary Variation in the strength of age-dependent natural selection shapes differences in ageing rates across species and populations. Likewise, sexual selection can promote divergent patterns of senescence across the sexes. However, the effects of these processes on the evolution of ageing have largely been considered independently, and interactions between them are poorly understood. We use experimental evolution to investigate how natural and sexual selection affect life span and ageing in Drosophila simulans. Replicate populations were evolved under lifetime monogamy (relaxed sexual selection) or lifetime polyandry (elevated sexual selection) and at one of two temperatures, 25 °C (rela…

Early life of fathers affects offspring fitness in a wild rodent.

Intergenerational fitness effects on offspring due to the early life of the parent are well studied from the standpoint of the maternal environment, but intergenerational effects owing to the paternal early life environment are often overlooked. Nonetheless, recent laboratory studies in mammals and ecologically relevant studies in invertebrates predict that paternal effects can have a major impact on the offspring's phenotype. These nongenetic, environment-dependent paternal effects provide a mechanism for fathers to transmit environmental information to their offspring and could allow rapid adaptation. We used the bank vole Myodes glareolus, a wild rodent species with no paternal care, to …

The 'Extreme Female Brain' : Increased Cognitive Empathy as a Dimension of Psychopathology

Abstract Baron-Cohen's ‛extreme male brain' theory postulates that autism involves exaggerated male-typical psychology, with reduced empathizing (considered here as social–emotional interest, motivation and abilities) and increased systemizing (non-social, physical-world and rule-based interest, motivation and abilities), in association with its male-biased sex ratio. The concept of an ‘extreme female brain', involving some combination of increased empathizing and reduced systemizing, and its possible role in psychiatric conditions, has been considerably less well investigated. Female-biased sex ratios have been described in two conditions, depression and borderline personality disorder (BP…

The evolutionary ecology of deception

Through dishonest signals or actions, individuals often misinform others to their own benefit. We review recent literature to explore the evolutionary and ecological conditions for deception to be more likely to evolve and be maintained. We identify four conditions: (1) high misinformation potential through perceptual constraints of perceiver; (2) costs and benefits of responding to deception; (3) asymmetric power relationships between individuals and (4) exploitation of common goods. We discuss behavioural and physiological mechanisms that form a deception continuum from secrecy to overt signals. Deceptive tactics usually succeed by being rare and are often evolving under co-evolutionary a…

Data from: Stabilising selection on microsatellite allele length at arginine vasopressin 1a receptor and oxytocin receptor loci

The loci arginine vasopressin receptor 1a (avpr1a) and oxytocin receptor (oxtr) have evolutionarily conserved roles in vertebrate social and sexual behavior. Allelic variation at a microsatellite locus in the 5’ regulatory region of these genes is associated with fitness in the bank vole Myodes glareolus. Given the low frequency of long and short alleles at these microsatellite loci in wild bank voles, we used breeding trials to determine whether selection acts against long and short alleles. Female bank voles with intermediate length avpr1a alleles had the highest probability of breeding, while male voles whose avpr1a alleles were very different in length had reduced probability of breedin…

Data from: Negative frequency-dependent selection of sexually antagonistic alleles in Myodes glareolus

Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show …

Data from: Maintenance costs of male dominance and sexually antagonistic selection in the wild

1. Variation in dominance status determines male mating and reproductive success, but natural selection for male dominance can be detrimental or antagonistic for female performance, and ultimately their fitness. Attaining and maintaining a high dominance status in a population of competing individuals is physiologically costly for males. But how male dominance status is mediated by maintenance energetics is currently not well understood, nor are the correlational effects of male energetics on his sisters recognized. 2. We conducted laboratory and field experiments on rodent populations to test whether selective breeding for male dominance status (dominant vs. subordinate breeding lines) ant…