Marcy K. Uyenoyama

Theories of kin and group selection: A population genetics perspective☆

The elucidation of the evolution of altruism has been described as “the central theoretical problem of sociobiology” (Wilson, 1975, p. 3). While altruistic “socially valuable but individually disadvantageous” (Haldane, 1932), traits are by definition necessary for the functioning of semisocial and eusocial insect societies in which workers exhibit reduced fertility (E. 0. Wilson, 1971, p. 4), the significance of altruism to the evolution of social systems in general may be questioned. Nevertheless, if one accepts Wilson’s (1975, p. 7) definition of a society as a group of cooperating individuals of the same species, it is useful to consider the general problem of the evolution of cooperation from the perspective of the “worst” case, in which cooperative individuals incur a cost in fitness in order to benefit other members of the group. The purpose of this paper is to review the major hypotheses which have been advanced for the evolution of altruism under kin selection and group selection, and to attempt to relate the various verbal and mathematical arguments which have been applied to the problem. The theoretical context will be a population genetic one. In this view, the model of evolution is one of gene frequency change; strategy arguments based outside of the dynamical theory of genotype frequency change are not addressed. First, mathematical models of kin selection are surveyed and the results compared to the qualitative predictions proposed by Haldane (1955) and Hamilton (1964a,b). Second, various definitions of group

INBREEDING AND THE COST OF MEIOSIS: THE EVOLUTION OF SELFING IN POPULATIONS PRACTICING BIPARENTAL INBREEDING

The effect of biparental inbreeding on the conditions governing the evolution of selfing is examined using recursions in mating‐type frequencies. Sibmating in combination with random outcrossing influences two key determinants of the adaptive value of selfing: 1) the meiotic cost of biparental reproduction and 2) the level of inbreeding depression due to deleterious mutations. Biparental inbreeding serves to maintain biparental reproduction by increasing relatedness between parents and their biparentally derived offspring and introduces the possibility of an optimal mating system that incorporates both modes of reproduction. Biparental inbreeding serves to promote uniparental reproduction by reducing the relative inbreeding depression suffered by uniparental offspring. The net effect of these two antagonistic trends depends upon the extent to which mutational load accounts for differences in the numbers of the two types of offspring. A brief summary of the empirical literature suggests that: 1) biparental inbreeding may occur in populations exhibiting mixed mating systems; 2) while inbreeding depression represents an important factor, it does not account entirely for differences in offspring number between the two modes of reproduction.

On relatedness and adaptive topography in kin selection

Hamilton (1964a, b) constructed the verbal theoretical basis of modern kin selection theory which states that potentially “altruistic” individuals evolve to value their relatives according to the closeness of their genetic relatedness. In those fundamental papers, Hamilton restructed the brood selection models of Haldane (1932, 1955) and Williams and Williams (1957), and proposed the following criterion under which a gene for altruism may be expected to increase,

Coevolution of self-fertilization and inbreeding depression II. Symmetric overdominance in viability

We describe the evolutionary dynamics of a modifier of selfing coevolving with a locus subject to symmetric overdominance in viability under general levels of reduction in pollination success as a consequence of self-fertilization (pollen discounting). Simple models of the evolution of breeding systems that represent inbreeding depression as a constant parameter do not admit the possibility of stable mixed mating systems involving both inbreeding and random mating. Contrary to this expectation, we find that coevolution between a modifier of selfing and a single overdominant locus situated anywhere in the genome can generate evolutionarily attracting mixed mating systems. Two forms of association between the modifier locus and the viability locus promote the evolution of outcrossing. The favored heterozygous genotype at the viability locus develops positive associations with modifier alleles that enhance outcrossing and with the heterozygous genotype at the modifier locus. Associations between outcrossing and high viability evolve immediately upon the introduction of a rare modifier allele, even in the absence of linkage.

S -allele sequence diversity in natural populations of Solanum carolinense (Horsenettle)

S-allele diversity in Solanum carolinense was surveyed in two natural populations, located in Tennessee and North Carolina, with a molecular assay to determine the genotype of individual plants. A total of 13 different S-alleles were identified and sequenced. There is high overlap between the two populations sampled, with 10 alleles shared in common, one allele found only in Tennessee, and two found only in North Carolina. The number of alleles in this species appears to be extremely low compared with other species with gametophytic self-incompatibility. Sequence comparisons show that most alleles are extremely different one from another in their primary sequence and a phylogenetic analysis indicates extensive trans-specific evolution of S-lineages. In addition, some alleles appear to be derived much more recently. The implications of these observations are discussed in the light of recent theoretical results on S-allele population diversity and persistence.

Ancestral Population Genomics: The Coalescent Hidden Markov Model Approach

With incomplete lineage sorting (ILS), the genealogy of closely related species differs along their genomes. The amount of ILS depends on population parameters such as the ancestral effective population sizes and the recombination rate, but also on the number of generations between speciation events. We use a hidden Markov model parameterized according to coalescent theory to infer the genealogy along a four-species genome alignment of closely related species and estimate population parameters. We analyze a basic, panmictic demographic model and study its properties using an extensive set of coalescent simulations. We assess the effect of the model assumptions and demonstrate that the Markov property provides a good approximation to the ancestral recombination graph. Using a too restricted set of possible genealogies, necessary to reduce the computational load, can bias parameter estimates. We propose a simple correction for this bias and suggest directions for future extensions of the model. We show that the patterns of ILS along a sequence alignment can be recovered efficiently together with the ancestral recombination rate. Finally, we introduce an extension of the basic model that allows for mutation rate heterogeneity and reanalyze human–chimpanzee–gorilla–orangutan alignments, using the new models. We expect that this framework will prove useful for population genomics and provide exciting insights into genome evolution.

Coevolution of self-fertilization and inbreeding depression. III : Homozygous lethal mutations at multiple loci

We study the evolution of the rate of self-fertilization in response to deleterious mutations at multiple loci. Although partial selfing induces associations among loci even in the absence of linkage, associations among mutations at different loci are of a smaller order of magnitude than the mutation rate. Genotypes that carry homozygous lethal mutations in heterozygous form at i loci occur in frequencies of the order (Ti) mu i, in which T denotes the number of viability loci and mu the mutation rate. While associations between mutations at different loci remain small even under inbreeding, each viability locus develops an association with the modifier of the rate of self-fertilization that substantially affects the evolution of the breeding system. Positive associations between enhancers of selfing and haplotypes carrying multiple wild-type alleles and positive associations in heterozygosity between the modifier locus and the viability loci promote evolutionary increases in the rate of self-fertilization.

ON THE EVOLUTIONARY COSTS OF SELF-INCOMPATIBILITY: INCOMPLETE REPRODUCTIVE COMPENSATION DUE TO POLLEN LIMITATION

Abstract . Pollen limitation affects plants with diverse reproductive systems and ecologies. In self‐incompatible (SI) species, pollen limitation may preclude full reproductive compensation for prezygotic rejection of pollen. We present a model designed to explore the effects of incomplete reproductive compensation on evolutionary changes at a modifier locus that regulates the level of SI expression. Our results indicate that incomplete reproductive compensation greatly increases the evolutionary costs of SI, particularly in populations with low S‐allele diversity. The evolutionary fate of modifiers of SI expression depends on the rate at which they are transmitted to future generations as well as the effects of SI on offspring number and quality. Partial SI expression can represent a stable condition rather than an evolutionarily transient state between full expression and full suppression. This unanticipated result provides the first theoretical support for the evolutionary stability of such mixed mating systems, the existence of which has recently been documented.

Evolution of altruism under group selection in large and small populations in fluctuating environments

Abstract A continuous, graded form of group selection which does not involve extinction of demes can effectively oppose selection on the individual level against an altruistic allele under fluctuating environments in infinitely large demes among which uniform mixing occurs every generation. Although group selection cannot alter the conditions necessary for the initial increase of altruistic alleles, group selection can significantly influence the stationary distribution of gene frequency which is attained once stochastic forces have allowed theirintroduction. Drift is a more effective source of variation than fluctuations in selection when the variance in selection is moderate to small. High numbers of demes promote polymorphism under both graded group selection and extinction group selection.

Frequency-Dependent Disease Transmission and the Dynamics of the Silene-Ustilago Host-Pathogen System

Models incorporating density-dependent disease transmission functions generally provide a good fit for airborne and directly transmitted bacterial or viral diseases. However, the transmission dynamics of sexually transmitted and vector-borne diseases are likely to be frequency- rather than density-dependent, which results in qualitatively different dynamics. Here, we present analyses of a basic epidemiological model in which the transmission process is represented as a function of the population disease frequency. In an extension of the basic model, we consider disease transmission as a probability function that assumes that the chance of becoming infected increases with the number of vector contacts. Stability analyses show that host-pathogen coexistence is possible in vector-transmitted and sexually transmitted disease systems in which transmission is likely to be frequency-dependent; the potential for stable coexistence is greatest for intermediate rates of disease spread and weak density dependence of host growth rate. Extension of the basic frequency-dependent model to allow for multiple contacts among hosts indicates that parameter ranges within which coexistence is predicted are thereby broadened.