David C. Krakauer

PERSPECTIVE:EVOLUTION AND DETECTION OF GENETIC ROBUSTNESS

Abstract Robustness is the invariance of phenotypes in the face of perturbation. The robustness of phenotypes appears at various levels of biological organization, including gene expression, protein folding, metabolic flux, physiological homeostasis, development, and even organismal fitness. The mechanisms underlying robustness are diverse, ranging from thermodynamic stability at the RNA and protein level to behavior at the organismal level. Phenotypes can be robust either against heritable perturbations (e.g., mutations) or nonheritable perturbations (e.g., the weather). Here we primarily focus on the first kind of robustness—genetic robustness—and survey three growing avenues of research: (1) measuring genetic robustness in nature and in the laboratory; (2) understanding the evolution of genetic robustness; and (3) exploring the implications of genetic robustness for future evolution.

Policing stabilizes construction of social niches in primates.

All organisms interact with their environment, and in doing so shape it, modifying resource availability. Termed niche construction, this process has been studied primarily at the ecological level with an emphasis on the consequences of construction across generations. We focus on the behavioural process of construction within a single generation, identifying the role a robustness mechanism—conflict management—has in promoting interactions that build social resource networks or social niches. Using ‘knockout’ experiments on a large, captive group of pigtailed macaques (Macaca nemestrina), we show that a policing function, performed infrequently by a small subset of individuals, significantly contributes to maintaining stable resource networks in the face of chronic perturbations that arise through conflict. When policing is absent, social niches destabilize, with group members building smaller, less diverse, and less integrated grooming, play, proximity and contact-sitting networks. Instability is quantified in terms of reduced mean degree, increased clustering, reduced reach, and increased assortativity. Policing not only controls conflict, we find it significantly influences the structure of networks that constitute essential social resources in gregarious primate societies. The structure of such networks plays a critical role in infant survivorship, emergence and spread of cooperative behaviour, social learning and cultural traditions.

Redundancy, antiredundancy, and the robustness of genomes

Genetic mutations that lead to undetectable or minimal changes in phenotypes are said to reveal redundant functions. Redundancy is common among phenotypes of higher organisms that experience low mutation rates and small population sizes. Redundancy is less common among organisms with high mutation rates and large populations, or among the rapidly dividing cells of multicellular organisms. In these cases, one even observes the opposite tendency: a hypersensitivity to mutation, which we refer to as antiredundancy. In this paper we analyze the evolutionary dynamics of redundancy and antiredundancy. Assuming a cost of redundancy, we find that large populations will evolve antiredundant mechanisms for removing mutants and thereby bolster the robustness of wild-type genomes; whereas small populations will evolve redundancy to ensure that all individuals have a high chance of survival. We propose that antiredundancy is as important for developmental robustness as redundancy, and is an essential mechanism for ensuring tissue-level stability in complex multicellular organisms. We suggest that antiredundancy deserves greater attention in relation to cancer, mitochondrial disease, and virus infection.

SEXUAL SELECTION, SPACE, AND SPECIATION

A Fisherian model of sexual selection is combined with a diffusion model of mate dispersal to investigate the evolution of assortative mating in a sympatric population. Females mate with one of two types of polygynous males according to a males display of one of two sex‐limited, autosomal traits; these male traits may be associated with differential phenotypic mortalities. Through a Fisherian runaway process, female preferences and male traits can become associated in linkage disequilibrium, leading to patterns of assortative mating. Dispersing males, whose rate of movement is dependent on mating success, carry female preference genes with them, and displaced males thereby produce daughters with preference genes for their respective traits in locally higher than average frequencies. The reduced diffusion of the more preferred males permits the success of other male types in adjacent areas. Thus, mating‐success dependent diffusion, when coupled with the rapid divergence in phenotypes possible under the Fisher process, can lead to the coexistence of two female preferences and two male traits in sympatry. We argue that many existing approaches to sympatric speciation fail to explain observed male polymorphisms because they exclude explicit spatial structure from their speciation models.

Groups confuse predators by exploiting perceptual bottlenecks: a connectionist model of the confusion effect

Aggregation is a well documented behaviour in a number of animal groups. The “confusion effect” is one mechanism thought to mitigate the success of predators feeding on gregarious prey and hence favour aggregation. An artificial neural network model of prey targeting is developed to explore the advantages prey species might derive through a tendency to group. The network illustrates how an abstract model of the computational mechanisms mediating the perception of prey position is able to show a degradation in performance as group size increases. The relationship between group size and predator confusion has a characteristic decreasing decelerating shape. Prey “oddity” is shown to reduce the impact of the confusion effect, thereby allowing predators to target prey more accurately. Hence shoaling behaviour is most profitable to the prey when prey phenotypes are visually indistinguishable to a predator. Futhermore it is shown that prey “oddity” is relatively more costly in large groups than in small groups and the implications for assortative schooling are discussed. Both the model and the results are intended to make the general point that cognitive constraints will limit the information that a nervous system can process at a number of different levels of neural organization.

Mitochondria and germ-cell death.

In birds and mammals, most of the female germ cells are destroyed before fertilization in a process known as atresia, reducing the population of cells to a small fraction of that present in early fetal life. We suggest that this death of germ cells can be interpreted as a developmental solution to the accumulation of mutations (Müllers ratchet) in mitochondria, an idea that is supported by comparative analysis. Atresia in effect therefore removes oocytes carrying mutant mitochondria.

Social Structure, Robustness, and Policing Cost in a Cognitively Sophisticated Species

Conflict management is one of the primary requirements for social complexity. Of the many forms of conflict management, one of the rarest and most interesting is third‐party policing, or intervening impartially to control conflict. Third‐party policing should be hard to evolve because policers personally pay a cost for intervening, while the benefits are diffused over the whole group. In this study we investigate the incidence and costs of policing in a primate society. We report quantitative evidence of non–kin policing in the nonhuman primate, the pigtailed macaque. We find that policing is effective at reducing the intensity of or terminating conflict when performed by the most powerful individuals. We define a measure, social power consensus, that predicts effective low‐cost interventions by powerful individuals and ineffective, relatively costly interventions by low‐power individuals. Finally, we develop a simple probabilistic model to explore whether the degree to which policing can effectively reduce the societal cost of conflict is dependent on variance in the distribution of power. Our data and simple model suggest that third‐party policing effectiveness and cost are dependent on power structure and might emerge only in societies with high variance in power.

STABILITY AND EVOLUTION OF OVERLAPPING GENES

Abstract.— When the same sequence of nucleotides codes for regions of more than one functional polypeptide, this sequence contains overlapping genes. Overlap is most common in rapidly evolving genomes with high mutation rates such as viruses, bacteria, and mitochondria. Overlap is thought to be important as: (1) a means of compressing a maximum amount of information into short sequences of structural genes; and (2) as a mechanism for regulating gene expression through translational coupling of functionally related polypeptides. The stability of overlapping codes is examined in relation to the information cost of overlap and the mutation rate of the genome. The degree of overlap in a given population will tend to become monomorphic. Evolution toward partial overlap of genes is shown to depend on a convex cost function of overlap. Overlap does not evolve when expression of overlapping genes is mutually exclusive and produced by rare mutations to the wild‐type genome. Assuming overlap increases coupling between functionally related genes, the conditions favoring overlap are explored in relation to the kinetics of gene activation and decay. Coupling is most effective for genes in which the gene overlapping at its 5’end (leading gene) decays rapidly, while the gene overlapping at the 3’end (induced gene) decays slowly. If gene expression can feedback on itself (autocatalysis), then high rates of activation favor overlap.

Robustness mechanisms in primate societies: a perturbation study

Conflict management mechanisms have a direct, critical effect on system robustness because they mitigate conflict intensity and help repair damaged relationships. However, robustness mechanisms can also have indirect effects on system integrity by facilitating interactions among components. We explore the indirect role that conflict management mechanisms play in the maintenance of social system robustness, using a perturbation technique to ‘knockout’ components responsible for effective conflict management. We explore the effects of knockout on pigtailed macaque (Macaca nemestrina) social organization, using a captive group of 84 individuals. This system is ideal in addressing this question because there is heterogeneity in performance of conflict management. Consequently, conflict managers can be easily removed without disrupting other control structures. We find that powerful conflict managers are essential in maintaining social order for the benefit of all members of society. We show that knockout of components responsible for conflict management results in system destabilization by significantly increasing mean levels of conflict and aggression, decreasing socio-positive interaction and decreasing the operation of repair mechanisms.

An error limit for the evolution of language

On the evolutionary trajectory that led to human language there must have been a transition from a fairly limited to an essentially unlimited communication system. The structure of modern human languages reveals at least two steps that are required for such a transition: in all languages (i) a small number of phonemes are used to generate a large number of words; and (ii) a large number of words are used to a produce an unlimited number of sentences. The first (and simpler) step is the topic of the current paper. We study the evolution of communication in the presence of errorsand show that this limits the number of objects (or concepts) that can be described by a simple communication system. The evolutionary optimum is achieved by using only a small number of signals to describe a few valuable concepts. Adding more signals does not increase the fitness of a language. This represents an error–limit for the evolution of communication. We show that this error limit can be overcome by combining signals (phonemes) into words. The transition from an analog to a digital system was a necessary step toward theevolution of human language.