A MODEL FOR GENOMIC IMPRINTING IN THE SOCIAL BRAIN: ADULTS

Genomic imprinting refers to genes that are silenced when inherited via sperm or via egg. The silencing of genes conditional upon their parental origin requires an evolutionary explanation. The most widely accepted theory for the evolution of genomic imprinting—the kinship theory—argues that conflict between maternally inherited and paternally inherited genes over phenotypes with asymmetric effects on matrilineal and patrilineal kin results in self‐imposed silencing of one of the copies. This theory has been applied to imprinting of genes expressed in the placenta, and infant brain determining the allocation of parental resources being the source of conflict parental promiscuity. However, there is growing evidence that imprinted genes are expressed in the postinfant brain where parental promiscuity per se is no longer a source of conflict. Here, we advance the kinship theory by developing an evolutionary model of genomic imprinting in adults, driven by intragenomic conflict over allocation to parental versus communal care. We consider the role of sex differences in dispersal and variance in reproductive success as sources of conflict. We predict that, in hominids and birds, parental care will be expressed by maternally inherited genes. In nonhominid mammals, we predict more diversity, with some mammals showing the same pattern and other showing the reverse. We use the model to interpret experimental data on imprinted genes in the house mouse: specifically, paternally expressed Peg1 and Peg3 genes, underlying maternal care, and maternally expressed Gnas and paternally expressed Gnasxl genes, underlying communal care. We also use the model to relate ancestral demography to contemporary imprinting disorders of adults, in humans and other taxa.     

Genomic imprinting and the social brain

Genomic imprinting refers to the parent-of-origin-specific epigenetic marking of a number of genes. This epigenetic mark leads to a bias in expression between maternally and paternally inherited imprinted genes, that in some cases results in monoallelic expression from one parental allele. Genomic imprinting is often thought to have evolved as a consequence of the intragenomic conflict between the parental alleles that occurs whenever there is an asymmetry of relatedness. The two main examples of asymmetry of relatedness are when there is partiality of parental investment in offspring (as is the case for placental mammals, where there is also the possibility of extended postnatal care by one parent), and in social groups where there is a sex-biased dispersal. From this evolutionary starting point, it is predicted that, at the behavioural level, imprinted genes will influence what can broadly be termed bonding and social behaviour. We examine the animal and human literature for examples of imprinted genes mediating these behaviours, and divide them into two general classes. Firstly, mother-offspring interactions (suckling, attachment and maternal behaviours) that are predicted to occur when partiality in parental investment in early postnatal offspring occurs; and secondly, adult social interactions, when there is an asymmetry of relatedness in social groups. Finally, we return to the evolutionary theory and examine whether there is a pattern of behavioural functions mediated by imprinted genes emerging from the limited data, and also whether any tangible predictions can be made with regards to the direction of action of genes of maternal or paternal origin.     

A maternal-offspring coadaptation theory for the evolution of genomic imprinting

Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother–offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.     

A Maternal–Offspring Coadaptation Theory for the Evolution of Genomic Imprinting

Imprinted genes are expressed either from the maternally or paternally inherited copy only, and they play a key role in regulating complex biological processes, including offspring development and mother–offspring interactions. There are several competing theories attempting to explain the evolutionary origin of this monoallelic pattern of gene expression, but a prevailing view has emerged that holds that genomic imprinting is a consequence of conflict between maternal and paternal gene copies over maternal investment. However, many imprinting patterns and the apparent overabundance of maternally expressed genes remain unexplained and may be incompatible with current theory. Here we demonstrate that sole expression of maternal gene copies is favored by natural selection because it increases the adaptive integration of offspring and maternal genomes, leading to higher offspring fitness. This novel coadaptation theory for the evolution of genomic imprinting is consistent with results of recent studies on epigenetic effects, and it provides a testable hypothesis for the origin of previously unexplained major imprinting patterns across different taxa. In conjunction with existing hypotheses, our results suggest that imprinting may have evolved due to different selective pressures at different loci.     

The evolution of reciprocal sharing

Genetical models of the evolution of reciprocal altruism (as distinct from cooperation, mutualism, or nepotism) have difficulty explaining the initial establishment of an altruist gene in a selfish deme. Though potential mechanisms have been suggested, there is an alternative: much “altruistic” behavior may in fact be purely selfish in origin and consequently reciprocity need not be invoked to provide a selective benefit to the actor. Sharing and helping are fundamentally different behavior categories and should not be confused. Patterns of resource sharing in chimpanzees correspond to predictions made by a selfish model but not to those of a reciprocal altruism model, and many observations of human gift exchange are consistent with the selfish, but not the altruistic, model. This suggests that presumed hominid meat exchange may have been the result of competition, not altruism or even cooperation, and that evolutionary models of “altruistic” behavior should be treated with caution.     

A model for genomic imprinting in the social brain: elders

Genomic imprinting refers to the process whereby genes are silenced when inherited via sperm or egg. The most widely accepted theory for the evolution of genomic imprinting-the kinship theory-argues that conflict between maternally inherited and paternally inherited genes over phenotypes with asymmetric effects on matrilineal and patrilineal kin results in self-imposed silencing of one of the copies. This theory was originally developed in the context of fitness interactions within nuclear families, to understand intragenomic conflict in the embryo and infant, but it has recently been extended to encompass interactions within wider social groups, to understand intragenomic conflict over the social behavior of juveniles and adults. Here, we complete our model of genomic imprinting in the social brain by considering age-specific levels of expression in a society were generations overlap, to determine how intragenomic conflict plays out in older age. We determine the role of sex bias in juvenile dispersal, reproductive success, and adult mortality in mediating the direction and intensity of conflict over the competing demands of parental and communal care as the individual ages. We discover that sex-specific asymmetries in these demographic parameters result in intragenomic conflict at early age but this conflict gradually decays with age. Although individuals are riven by internal conflict in their youth and middle age, they put their demons to rest in later life.     

The evolution of genomic imprinting: costs,benefits and long‐term consequences

Genomic imprinting refers to a pattern of gene expression in which a specific parent's allele is either under‐expressed or completely silenced. Imprinting is an evolutionary conundrum because it appears to incur the costs of diploidy (e.g. presenting a larger target than haploidy to mutations) while foregoing its benefits (protection from harmful recessive mutations). Here, we critically evaluate previously proposed evolutionary benefits of imprinting and suggest some additional ones. We discuss whether each benefit is capable of explaining both the origin and maintenance of imprinting, and examine how the different benefits interact. We then outline the many costs of imprinting. Simple models show that circulating deleterious recessives can prevent the initial spread of imprinting, even if imprinting would be evolutionarily stable if it could persist long enough to purge these. We also show that imprinting can raise or lower the mutation load, depending on the selective regime and the degree of dominance. We finish by discussing the population‐level consequences of imprinting, which can be both positive and negative. Imprinting offers many insights into evolutionary conflict, the interaction between individual‐ and population‐level fitness effects, and the ‘gene's‐eye view’ of evolution.     

Sexual selection modulates genetic conflicts and patterns of genomic imprinting

Recent years have seen a surge of interest in linking the theories of kin selection and sexual selection. In particular, there is a growing appreciation that kin selection, arising through demographic factors such as sex‐biased dispersal, may modulate sexual conflicts, including in the context of male–female arms races characterized by coevolutionary cycles. However, evolutionary conflicts of interest need not only occur between individuals, but may also occur within individuals, and sex‐specific demography is known to foment such intragenomic conflict in relation to social behavior. Whether and how this logic holds in the context of sexual conflict—and, in particular, in relation to coevolutionary cycles—remains obscure. We develop a kin‐selection model to investigate the interests of different genes involved in sexual and intragenomic conflict, and we show that consideration of these conflicting interests yields novel predictions concerning parent‐of‐origin specific patterns of gene expression and the detrimental effects of different classes of mutation and epimutation at loci underpinning sexually selected phenotypes.     

Conflict theory of genomic imprinting in mammals

In mammals, some embryonic genes are expressed differently depending on whether they are inherited from the sperm or egg, a phenomenon known as genomic imprinting. The information on the parental origin is transmitted by an epigenetic mark. Both the molecular mechanisms and evolutionary processes of genomic imprinting have been studied extensively. Here, I illustrate the simplest evolutionary dynamics of imprinting evolution based on the “conflict theory,” by considering the evolution of a gene encoding an embryonic growth factor controlling the maternal resource supply. It demonstrates that (a) the autosomal genes controlling placenta development to modify maternal resource acquisition may evolve a strong asymmetry of gene expression, provided the mother has some chance of accepting multiple males. (b) The genomic imprinting may not evolve if there is a small fraction of recessive deleterious mutations on the gene. (c) The growth-enhancing genes should evolve to paternally expressed, while the growth-suppressing genes should evolve to maternally expressed. (d) The X-linked genes also evolve genomic imprinting, but the main evolutionary force is the sex difference in the optimal embryonic size. I discuss other aberrations that can be explained by the modified versions of the basic model.     

Intragroup and intragenomic conflict over chemical defense against predators

Insects are often chemically defended against predators. There is considerable evidence for a group‐beneficial element to their defenses, and an associated potential for individuals to curtail their own investment in costly defense while benefitting from the investments of others, termed “automimicry.” Although females in chemically defended taxa often lay their eggs in clusters, leading to siblings living in close proximity, current models of automimicry have neglected kin‐selection effects, which may be expected to curb the evolution of such selfishness. Here, we develop a general theory of automimicry that explicitly incorporates kin selection. We investigate how female promiscuity modulates intragroup and intragenomic conflicts overinvestment into chemical defense, finding that individuals are favored to invest less than is optimal for their group, and that maternal‐origin genes favor greater investment than do paternal‐origin genes. We translate these conflicts into readily testable predictions concerning gene expression patterns and the phenotypic consequences of genomic perturbations, and discuss how our results may inform gene discovery in relation to economically important agricultural products.     

On the relationship between evolutionary and psychological definitions of altruism and selfishness

I examine the relationship between evolutionary definitions of altruism that are based on fitness effects and psychological definitions that are based on the motives of the actor. I show that evolutionary altruism can be motivated by proximate mechanisms that are psychologically either altruistic or selfish. I also show that evolutionary definitions do rely upon motives as a metaphor in which the outcome of natural selection is compared to the decisions of a psychologically selfish (or altruistic) individual. Ignoring the precise nature of both psychological and evolutionary definitions has obscured many important issues, including the biological roots of psychological altruism.     

The influence of genomic imprinting on brain development and behavior

Genomic imprinting, a newly discovered and significant form of gene regulation, refers to the differential expression of a gene depending on whether it is inherited from the male or female parent. The genetic conflict theory of genomic imprinting postulates that conflicts between the genetic interests of mothers, fathers, and their offspring, as well as asymmetric genetic relationships with maternal and paternal kin, led to an evolutionary “arms race” within the genome, which resulted in the expression of these conflicts at the phenotypic level. This paper provides background and evidence regarding genomic imprinting and its role in brain development, describes the cognitive and behavioral phenomena that have been interpreted in terms of the genetic conflict model, and points to potential avenues of further research.     

Host defenses to transposable elements and the evolution of genomic imprinting

Genomic imprinting is the differential expression of maternally and paternally inherited alleles of specific genes. Several organismic level hypotheses have been offered to explain the evolution of genomic imprinting. We argue that evolutionary explanations of the origin of imprinting that focus exclusively on the organismic level are incomplete. We propose that the complex molecular mechanisms that underlie genomic imprinting originally evolved as an adaptive response to the mutagenic potential of transposable elements (TEs). We also present a model of how these mechanisms may have been co-opted by natural selection to evolve molecular features characteristic of genomic imprinting.     

ON THE PARADIGM OF ALTRUISTIC SUICIDE IN THE UNICELLULAR WORLD

Altruistic suicide is best known in the context of programmed cell death (PCD) in multicellular individuals, which is understood as an adaptive process that contributes to the development and functionality of the organism. After the realization that PCD‐like processes can also be induced in single‐celled lineages, the paradigm of altruistic cell death has been extended to include these active cell death processes in unicellular organisms. Here, we critically evaluate the current conceptual framework and the experimental data used to support the notion of altruistic suicide in unicellular lineages, and propose new perspectives. We argue that importing the paradigm of altruistic cell death from multicellular organisms to explain active death in unicellular lineages has the potential to limit the types of questions we ask, thus biasing our understanding of the nature, origin, and maintenance of this trait. We also emphasize the need to distinguish between the benefits and the adaptive role of a trait. Lastly, we provide an alternative framework that allows for the possibility that active death in single‐celled organisms is a maladaptive trait maintained as a byproduct of selection on pro‐survival functions, but that could—under conditions in which kin/group selection can act—be co‐opted into an altruistic trait.     

DO EMBRYOS INFLUENCE MATERNAL INVESTMENT? EVALUATING MATERNAL‐FETAL COADAPTATION AND THE POTENTIAL FOR PARENT‐OFFSPRING CONFLICT IN A PLACENTAL FISH

The evolution of matrotrophy introduces the potential for genomic conflicts between mothers and embryos. These conflicts are hypothesized to accelerate the evolution of reproductive isolation and to influence the evolution of life-history traits, reproductive structures, and genomic imprinting. These hypotheses assume offspring can influence the amount of maternal investment they receive and that there is a trade-off between maternal investment into individual offspring and maternal survival or fecundity. We used field data and laboratory crosses to test whether these assumptions are met in the matrotrophic poeciliid fish Heterandria formosa . Comparisons of life histories between two natural populations demonstrated a trade-off between the level of maternal investment into individual embryos and maternal fecundity. Laboratory crosses between individuals from these populations revealed that offspring genotype exerts an influence on the level of maternal investment and affects maternal fecundity through higher rates of embryo abortion and lower numbers of full-term offspring. Our results show that the prerequisites for parent–offspring conflict to be a potent evolutionary force in poeciliid fish are present in H. formosa. However, determining whether this conflict has shaped maternal investment in nature will require disentangling any effects of conflict from those of several ecological factors that are themselves correlated with the expected intensity of conflict.     

Mutability as an altruistic trait in finite asexual populations

Mutation rate (MR) is a crucial determinant of the evolutionary process. Optimal MR may enable efficient evolutionary searching and therefore increase the fitness of the population over time. Nevertheless, individuals may favor MRs that are far from being optimal for the whole population. Instead, each individual may tend to mutate at rates that selfishly increase its own relative fitness. We show that in some cases, undergoing a mutation is altruistic, i.e., it increases the expected fitness of the population, but decreases the expected fitness of the mutated individual itself. In this case, if the population is uniform (completely mixed, undivided), immutability is evolutionary stable and is probably selected for. However, our examination of a segregated population, which is divided into several groups (or patches), shows that the optimal, altruistic MR may out-compete the selfish MR if the coupling between the groups is neither too strong nor too weak. This demonstrates that the population structure is crucial for the succession of the evolutionary process itself. For example, in a uniform population, the evolutionary process may be stopped before the highest fitness is reached, as demonstrated in a one-pick fitness landscape. In addition, we show that the dichotomy between evolutionary stable and optimal MRs can be seen as a special case of a more general phenomenon in which optimal behaviors may be destabilized in finite populations, since optimal sub-populations may become extinct before the benefit of their behavior is expressed.     

Screening of duplicated loci reveals hidden divergence patterns in a complex salmonid genome

A whole‐genome duplication (WGD) doubles the entire genomic content of a species and is thought to have catalysed adaptive radiation in some polyploid‐origin lineages. However, little is known about general consequences of a WGD because gene duplicates (i.e., paralogs) are commonly filtered in genomic studies; such filtering may remove substantial portions of the genome in data sets from polyploid‐origin species. We demonstrate a new method that enables genome‐wide scans for signatures of selection at both nonduplicated and duplicated loci by taking locus‐specific copy number into account. We apply this method to RAD sequence data from different ecotypes of a polyploid‐origin salmonid (Oncorhynchus nerka) and reveal signatures of divergent selection that would have been missed if duplicated loci were filtered. We also find conserved signatures of elevated divergence at pairs of homeologous chromosomes with residual tetrasomic inheritance, suggesting that joint evolution of some nondiverged gene duplicates may affect the adaptive potential of these genes. These findings illustrate that including duplicated loci in genomic analyses enables novel insights into the evolutionary consequences of WGDs and local segmental gene duplications.