Microgeographic socio-genetic structure of an African cooperative breeding passerine revealed: integrating behavioural and genetic data

Dispersal can be motivated by multiple factors including sociality. Dispersal behaviour affects population genetic structure that in turn reinforces social organization. We combined observational information with individual-based genetic data in the Karoo scrub-robin, a facultative cooperatively breeding bird, to understand how social bonds within familial groups affect mating patterns, cause sex asymmetry in dispersal behaviour and ultimately influence the evolution of dispersal. Our results revealed that males and females do not have symmetrical roles in structuring the population. Males are extremely philopatric and tend to delay dispersal until they gain a breeding position within a radius of two territories around the natal site. By contrast, females dispersed over larger distances, as soon as they reach independence. This resulted in male neighbourhoods characterized by high genetic relatedness. The long-distance dispersal strategy of females ensured that Karoo scrub-robins do not pair with relatives thereby compensating for male philopatry caused by cooperation. The observed female-biased strategy seems to be the most prominent mechanism to reduce the risk of inbreeding that characterizes social breeding system. This study demonstrates that tying together ecological data, such as breeding status, determining social relationships with genetic data, such as kinship, provides valuable insights into the proximate causes of dispersal, which are central to any evolutionary interpretation.     

The maintenance of heritable variation through social competition

The paradoxical persistence of heritable variation for fitness-related traits is an evolutionary conundrum that remains a preeminent problem in evolutionary biology. Here we describe a simple mechanism in which social competition results in the evolutionary maintenance of heritable variation for fitness related traits. We demonstrate this mechanism using a genetic model with two primary assumptions: the expression of a trait depends upon success in social competition for limited resources; and competitive success of a genotype depends on the genotypes that it competes against. We find that such social competition generates heritable (additive) genetic variation for "competition-dependent" traits. This heritable variation is not eroded by continuous directional selection because, rather than leading to fixation of favored alleles, selection leads instead to allele frequency cycling due to the concerted coevolution of the social environment with the effects of alleles. Our results provide a mechanism for the maintenance of heritable variation in natural populations and suggest an area for research into the importance of competition in the genetic architecture of fitness related traits.     

A comparison of nuclear and cytoplasmic genetic effects on sperm competitiveness and female remating in a seed beetle

It is widely assumed that male sperm competitiveness evolves adaptively. However, recent studies have found a cytoplasmic genetic component to phenotypic variation in some sperm traits presumed important in sperm competition. As cytoplasmic genes are maternally transmitted, they cannot respond to selection on sperm and this constraint may affect the scope in which sperm competitiveness can evolve adaptively. We examined nuclear and cytoplasmic genetic contributions to sperm competitiveness, using populations of Callosobruchus maculatus carrying orthogonal combinations of nuclear and cytoplasmic lineages. Our design also enabled us to examine genetic contributions to female remating. We found that sperm competitiveness and remating are primarily encoded by nuclear genes. In particular, a male's sperm competitiveness phenotype was contingent on an interaction between the competing male genotypes. Furthermore, cytoplasmic effects were detected on remating but not sperm competitiveness, suggesting that cytoplasmic genes do not generally play a profound evolutionary role in sperm competition.     

TRIBUTE: In Goethe's Wake: Marvalee Wake's conceptual contributions to the development and evolution of a science of morphology

Decrying the typological approach in much of the teaching of morphology, from the outset of her career Marvalee Wake advocated a synthetic, mechanistic and pluralistic developmental and evolutionary morphology. In this short essay, I do not evaluate Wake's contributions to our knowledge of the morphology of caecilians, nor her contributions to viviparity, both of which are seminal and substantive, nor do I examine her role as mentor, supervisor and collaborator, but assess her broader conceptual contributions to the development and evolution of morphology as a science. One of the earliest morphologists to take on board the concept of constraint, she viewed constraint explicitly in relation to adaptation and diversity. Her approach to morphology as a science was hierarchical – measure form and function in a phylogenetic context; seek explanations at developmental, functional, ecological, evolutionary levels of the biological hierarchy; integrate those explanations to the other levels. The explanatory power of morphology thus practised allows morphology to inform evolutionary biology and evolutionary theory, and paves the way for the integrative biology Wake has long championed.     

Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber

Naked mole-rats are fossorial, eusocial rodents that naturally exhibit high levels of inbreeding. Persistent inbreeding in animals often results in a substantial decline in fitness and, thus, dispersal and avoidance of kin as mates are two common inbreeding avoidance mechanisms. In the naked mole-rat evidence for the former has recently been found. Here we address the latter mechanism by investigating kin recognition and female mate choice using a series of choice tests in which the odour, social and mate preferences of females were determined. Discrimination by females appears to be dependent on their reproductive status. Reproductively active females prefer to associate with unfamiliar males, whereas reproductively inactive females do not discriminate. Females do not discriminate between kin and non-kin suggesting that the criterion for recognition is familiarity, not detection of genetic similarity per se. In the wild, naked mole-rats occupy discrete burrow systems and dispersal and mixing with non-kin is thought to be comparatively rare. Thus, recognition by familiarity may function as a highly efficient kin recognition mechanism in the naked mole-rat. A preference by reproductively active females for unfamiliar males is interpreted as inbreeding avoidance. These findings suggest that, despite an evolutionary history of close inbreeding, naked mole-rats may not be exempt from the effects of inbreeding depression and will attempt to outbreed should the opportunity arise.     

Genetic variation in social influence on mate preferences

Patterns of phenotypic variation arise in part from plasticity owing to social interactions, and these patterns contribute, in turn, to the form of selection that shapes the variation we observe in natural populations. This proximate–ultimate dynamic brings genetic variation in social environments to the forefront of evolutionary theory. However, the extent of this variation remains largely unknown. Here, we use a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess how mate preferences are influenced by genetic variation in the social environment. We used full-sibling split-families as ‘treatment’ social environments, and reared focal females alongside each treatment family, describing the mate preferences of the focal females. With this method, we detected substantial genetic variation in social influence on mate preferences. The mate preferences of focal females varied according to the treatment families along with which they grew up. We discuss the evolutionary implications of the presence of such genetic variation in social influence on mate preferences, including potential contributions to the maintenance of genetic variation, the promotion of divergence, and the adaptive evolution of social effects on fitness-related traits.     

Simulating the Evolution of the Human Family: Cooperative Breeding Increases in Harsh Environments

Verbal and mathematical models that consider the costs and benefits of behavioral strategies have been useful in explaining animal behavior and are often used as the basis of evolutionary explanations of human behavior. In most cases, however, these models do not account for the effects that group structure and cultural traditions within a human population have on the costs and benefits of its members'' decisions. Nor do they consider the likelihood that cultural as well as genetic traits will be subject to natural selection. In this paper, we present an agent-based model that incorporates some key aspects of human social structure and life history. We investigate the evolution of a population under conditions of different environmental harshness and in which selection can occur at the level of the group as well as the level of the individual. We focus on the evolution of a socially learned characteristic related to individuals'' willingness to contribute to raising the offspring of others within their family group. We find that environmental harshness increases the frequency of individuals who make such contributions. However, under the conditions we stipulate, we also find that environmental variability can allow groups to survive with lower frequencies of helpers. The model presented here is inevitably a simplified representation of a human population, but it provides a basis for future modeling work toward evolutionary explanations of human behavior that consider the influence of both genetic and cultural transmission of behavior.     

Fine-scale population genetic structure in a fission-fusion society

Nonrandom patterns of mating and dispersal create fine-scale genetic structure in natural populations — especially of social mammals — with important evolutionary and conservation genetic consequences. Such structure is well-characterized for typical mammalian societies; that is, societies where social group composition is stable, dispersal is male-biased, and males form permanent breeding associations in just one or a few social groups over the course of their lives. However, genetic structure is not well understood for social mammals that differ from this pattern, including elephants. In elephant societies, social groups fission and fuse, and males never form permanent breeding associations with female groups. Here, we combine 33 years of behavioural observations with genetic information for 545 African elephants ( Loxodonta africana ), to investigate how mating and dispersal behaviours structure genetic variation between social groups and across age classes. We found that, like most social mammals, female matrilocality in elephants creates co-ancestry within core social groups and significant genetic differentiation between groups (Φ_ST = 0.058). However, unlike typical social mammals, male elephants do not bias reproduction towards a limited subset of social groups, and instead breed randomly across the population. As a result, reproductively dominant males mediate gene flow between core groups, which creates cohorts of similar-aged paternal relatives across the population. Because poaching tends to eliminate the oldest elephants from populations, illegal hunting and poaching are likely to erode fine-scale genetic structure. We discuss our results and their evolutionary and conservation genetic implications in the context of other social mammals.     

Runaway sexual selection without genetic correlations: social environments and flexible mate choice initiate and enhance the fisher process

Female mating preferences are often flexible, reflecting the social environment in which they are expressed. Associated indirect genetic effects (IGEs) can affect the rate and direction of evolutionary change, but sexual selection models do not capture these dynamics. We incorporate IGEs into quantitative genetic models to explore how variation in social environments and mate choice flexibility influence Fisherian sexual selection. The importance of IGEs is that runaway sexual selection can occur in the absence of a genetic correlation between male traits and female preferences. Social influences can facilitate the initiation of the runaway process and increase the rate of trait elaboration. Incorporating costs to choice do not alter the main findings. Our model provides testable predictions: (1) genetic covariances between male traits and female preferences may not exist, (2) social flexibility in female choice will be common in populations experiencing strong sexual selection, (3) variation in social environments should be associated with rapid sexual trait divergence, and (4) secondary sexual traits will be more elaborate than previously predicted. Allowing feedback from the social environment resolves discrepancies between theoretical predictions and empirical data, such as why indirect selection on female preferences, theoretically weak, might be sufficient for preferences to become elaborated.     

Evolution in response to social selection: the importance of interactive effects of traits on fitness

Social interactions have a powerful effect on the evolutionary process. Recent attempts to synthesize models of social selection with equations for indirect genetic effects (McGlothlin et al. 2010) provide a broad theoretical base from which to study selection and evolutionary response in the context of social interactions. However, this framework concludes that social selection will lead to evolution only if the traits carried by social partners are nonrandomly associated. I suggest this conclusion is incomplete, and that traits that do not covary between social partners can nevertheless lead to evolution via interactive effects on fitness. Such effects occur when there are functional interactions between traits, and as an example I use the interplay in water striders (Gerridae) between grasping appendages carried by males and spines by females. Functional interactive effects between traits can be incorporated into both the equations for social selection and the general model of social evolution proposed by McGlothlin et al. These expanded equations would accommodate adaptive coevolution in social interactions, integrate the quantitative genetic approach to social evolution with game theoretical approaches, and stimulate some new questions about the process of social evolution.     

Coevolution of senders and receivers of sexual signals: Genetic coupling and genetic correlations

The parallel evolution of senders and receivers of sexual signals has been a topic of research in both neuroethology and evolutionary quantitative genetics. Neuroethologists have debated whether the same physiological mechanism underlies both production and reception of a signal, and whether the same genes affect the physiology of communication in each sex. Quantitative geneticists have discussed the possibility that particular types of signals, and preferences for those types, are inherited together. Studies of communication by a variety of insect species do not provide strong support for a common physiological mechanism, but do not rule out the genetic effect. The neuroethological perspective may be of assistance in understanding the evolution of sexual communication because it offers a way to subdivide communication into units for genetic analysis.     

A major evolutionary transition to more than two sexes?

Two recently discovered cases of genetic caste determination in social insects might provide the first example of a major evolutionary transition from two to more than two sexes. I argue here that the system can be interpreted as comprising primarily individuals requiring gametes from three parental types and having four sexes from the perspective of demographic extinction. Additionally, I show how this mating system can be seen as a major evolutionary transition. For these populations, it is apparent that the mechanism for a three- or four-sex system does not lie within the myriad of possible arrangements of chromosomes within individuals, but at the next level of evolutionary complexity, with the arrangement of chromosomes among individuals within a social system.     

Assembling networks of microbial genomes using linear programming

Background  

Microbial genomes exhibit complex sets of genetic affinities due to lateral genetic transfer. Assessing the relative contributions of parent-to-offspring inheritance and gene sharing is a vital step in understanding the evolutionary origins and modern-day function of an organism, but recovering and showing these relationships is a challenging problem.     

Genetics of human aggressive behaviour

A consideration of the evolutionary, physiological and anthropological aspects of aggression suggests that individual differences in such behaviour will have important genetic as well as environmental underpinning. Surveys of the likely pathways controlling the physiological and neuronal processes involved highlight, as obvious targets to investigate, genes implicated in sexual differentiation, anxiety, stress response and the serotonin neurotransmitter pathway. To date, however, association studies on single candidates have provided little evidence for any such loci with a major effect size. This may be because genes do not operate independently, but function against a background in which other genetic and environmental factors are crucial. Indeed, a series of recent studies, particularly concentrating on the serotonin and norepinephrine metabolising enzyme, monoamine oxidase A, has emphasised the necessity of examining gene by environmental interactions if the contributions of individual loci are to be understood. These findings will have major significance for the interpretation and analysis of data from detailed whole genome association studies. Functional imaging studies of genetic variants affecting serotonin pathways have also provided valuable insights into potential links between genes, brain and aggressive behaviour.     

Drosophila melanogaster females change mating behaviour and offspring production based on social context

In Drosophila melanogaster, biological rhythms, aggression and mating are modulated by group size and composition. However, the fitness significance of this group effect is unknown. By varying the composition of groups of males and females, we show that social context affects reproductive behaviour and offspring genetic diversity. Firstly, females mating with males from the same strain in the presence of males from a different strain are infecund, analogous to the Bruce effect in rodents, suggesting a social context-dependent inbreeding avoidance mechanism. Secondly, females mate more frequently in groups composed of males from more than one strain; this mitigates last male sperm precedence and increases offspring genetic diversity. However, smell-impaired Orco mutant females do not increase mating frequency according to group composition; this indicates that social context-dependent changes in reproductive behaviour depend on female olfaction, rather than direct male-male interactions. Further, variation in mating frequency in wild-type strains depends on females and not males. The data show that group composition can affect variance in the reproductive success of its members, and that females play a central role in this process. Social environment can thus influence the evolutionary process.     

Models to estimate maternally controlled genetic variation in quantitative seed characters

Summary Estimating quantitative contributions to specific traits can be accomplished from a variety of genetic models (Mather 1949; Mather and Jinks 1971; Falconer 1981). Residual genetic effects, those beyond main and interaction effects of the embryo genotype, are often pooled under a single classification, termed maternal effects. Maternal contributions to seed-related traits can originate from various maternal sources (e.g., endosperm, testa and cytoplasm). Quantitative contributions of a maternal nature are not predictable from parental performance and effects are largely non-persistent over generations (Jinks et al. 1972). The methods used to determine maternal effects in quantitative traits often do not measure quantitative genetic parameters, while those that do are either complex or partially resolve potential contributions of individual sources of maternal effects. We present simple genetic models for estimating quantitative genetic parameters which take into account maternal effects expressed in the major seed tissues of higher plants.     

Indirect Genetic Effects and the Dynamics of Social Interactions

BackgroundIndirect genetic effects (IGEs) occur when genes expressed in one individual alter the expression of traits in social partners. Previous studies focused on the evolutionary consequences and evolutionary dynamics of IGEs, using equilibrium solutions to predict phenotypes in subsequent generations. However, whether or not such steady states may be reached may depend on the dynamics of interactions themselves.ResultsIn our study, we focus on the dynamics of social interactions and indirect genetic effects and investigate how they modify phenotypes over time. Unlike previous IGE studies, we do not analyse evolutionary dynamics; rather we consider within-individual phenotypic changes, also referred to as phenotypic plasticity. We analyse iterative interactions, when individuals interact in a series of discontinuous events, and investigate the stability of steady state solutions and the dependence on model parameters, such as population size, strength, and the nature of interactions. We show that for interactions where a feedback loop occurs, the possible parameter space of interaction strength is fairly limited, affecting the evolutionary consequences of IGEs. We discuss the implications of our results for current IGE model predictions and their limitations.     

Kin selection and the evolution of sexual conflict

Males and females do not always share the same evolutionary interests. This is particularly true in the case of multiple mating, where male–male competition can often lead to adaptations that are harmful to the female, and females can evolve counter adaptations to reduce the benefits males gain from such traits. Although social evolution has made substantial progress from kin selection theory, most studies of sexual conflict have ignored the effects of genetic relatedness. Here, I use a model of male harm and female resistance to investigate how kin selection affects the evolution of sexual conflict. Building on models of social evolution, I show that relatedness inhibits sexual conflict, in terms of male harm, whereas it has no effect on the evolution female resistance. This study examines a previously neglected mechanism that can potentially help to resolve sexual conflict over mating and highlights the potential importance of considering relatedness in empirical studies of sexual conflict.     

Evolution of specificity in the eukaryotic endomembrane system

Two hundred years after Darwin's birth, our understanding of genetic mechanisms and cell biology has advanced to a level unimaginable in the 19th century. We now know that eukaryotic cells contain a huge variety of internal compartments, each with their own function, identity and history. For the compartments that together form the membrane-trafficking system, one of the central questions is how that identity is encoded and how it evolved. Here we review the key components involved in membrane-trafficking events, including SNAREs, Rabs, vesicle coats, and tethers and what is known about their evolutionary history. Our current understanding suggests a possible common mechanism by which the membrane-trafficking organelles might have evolved. This model of increased organellar complexity by gene duplication and co-evolution of multiple, interacting, specificity-encoding proteins could well be applicable to other non-endosymbiotic organelles as well. The application of basic evolutionary principles well beyond their original scope has been exceedingly powerful not only in reconstructing the history of cellular compartments, but for medical and applied research as well, and underlines the contributions of Darwin's ideas in modern biology.     

The logic of Ménage à Trois.

Recent studies of socially monogamous species have shown that in many cases females do not copulate exclusively with their pair mates, but are also receptive to other males. The explanation usually given for unfaithful female behavior is that most females are unable to bond with a male they would prefer as genetic father to their offspring. To secure male assistance the female therefore pairs with an available male but also copulates with males of supposedly higher genetic quality. Here we offer an alternative evolutionary explanation for female infidelity, which does not rely upon this ''Good Genes hypothesis of female choice. We show with a simple model that in an evolutionary game between three players, a male, a female and a male lover, solutions exist in which the female can secure more assistance from her mate by being receptive to other males. We conclude that female sexuality can have a decisive role in regulating social behaviour, in which the fertile female is the driving force.