Charles J. Goodnight

Epistasis and the effect of founder events on the additive genetic variance

Models of founder events have focused on the reduction in the genetic variation following a founder event. However, recent work (Bryant et al., 1986; Goodnight, 1987) suggests that when there is epistatic genetic variance in a population, the total genetic variance within demes may actually increase following a founder event. Since the additive genetic variance is a statistical property of a population and can change with the level of inbreeding, some of the epistatic genetic variance may be converted to additive genetic variance during a founder event. The model presented here demonstrates that some of the additive‐by‐additive epistatic genetic variance is converted to additive genetic variance following a founder event. Furthermore, the amount of epistasis converted to additive genetic variance is a function of the recombination rate and the propagule size. For a single founder event of two individuals, as much as 75% of the epistatic variance in the ancestral population may become additive genetic variance following the founder event. For founder events involving two individuals with free recombination, the relative contribution of epistasis to the additive genetic variance following a founder event is equal to its proportion of the total genetic variance prior to the founder event. Traits closely related to fitness are expected to have relatively little additive genetic variance but may have substantial nonadditive genetic variance. Founder events may be important in the evolution of fitness traits, not because they lead to a reduction in the genetic variance, but rather because they lead to an increase in the additive genetic variance.

PERSPECTIVE: THE THEORIES OF FISHER AND WRIGHT IN THE CONTEXT OF METAPOPULATIONS: WHEN NATURE DOES MANY SMALL EXPERIMENTS

We critically review the two major theories of adaptive evolution developed early in this century, Wrights shifting balance theory and Fishers large population size theory, in light of novel findings from field observations, laboratory experiments, and theoretical research conducted over the past 15 years. Ecological studies of metapopulations have established that the processes of local extinction and colonization of demes are relatively common in natural populations of many species and theoretical population genetic models have shown that these ecological processes have genetic consequences within and among local demes. Within demes, random genetic drift converts nonadditive genetic variance into additive genetic variance, increasing, rather than limiting, the potential for adaptation to local environments. For this reason, the genetic differences that arise by drift among demes, can be augmented by local selection. The resulting adaptive differences in gene combinations potentially contribute to the genetic origin of new species. These and other recent findings were not discussed by either Wright or Fisher. For example, although Wright emphasized epistatic genetic variance, he did not discuss the conversion process. Similarly, Fisher did not discuss how the average additive effect of a gene varies among demes across a metapopulation whenever there is epistasis. We discuss the implications of such recent findings for the Wright‐Fisher controversy and identify some critical open questions that require additional empirical and theoretical study.

Contextual analysis of models of group selection, soft selection, hard selection, and the evolution of altruism

Contextual analysis is used to examine models of group, hard, and soft selection and the evolution of altruism. We extend the methodology for measuring phenotypic selection to multiple levels in structured populations by analyzing selection acting on a trait at the individual level and its mean at the group level. With contextual analysis, we partition phenotypic selection into group and individual components using partial regressions These analyses identify the level(s) at which selection is acting and distinguish indirect from direct selection acting at other levels Contextual analysis of group selection in the absence of individual selection indicates that indirect selection is acting on individuals Under soft selection, though all groups have the same relative fitness, contextual analysis detects equal and opposite levels of group and individual selection resulting from frequency-dependent selection acting within groups. Under hard selection, groups vary in relative fitness, but there is no group selection Instead, indirect selection acts on the group mean phenotype. Thus, contextual analysis reveals that group, kin, frequency-dependent, and soft selection are related phenomena. Finally, we rederive Hamiltons rule for the evolution of altruism and determine when group selection is expected to be more powerful than individual selection

On the effect of founder events on epistatic genetic variance

Mayr (1963) proposed that small isolated propagules from a large panmictic population would occasionally undergo a genetic revolution due to loss of genetic variability. More recently Templeton (1980a) has suggested that founder events may be much more important in systems that have strong epistasis. Because of the work of these and other authors it becomes an interesting theoretical problem to study the distribution of epistatic variance in a population following a founder event. In the model presented here measures of coancestry (Cockerham, 1967, 1984; Cockerham and Weir, 1973; Weir and Cockerham, 1973, 1977; Tachida and Cockerham, unpubl.) are used to examine the effect of founder events on additive‐by‐additive epistasis. Using this approach, the coancestries, or intraclass correlations, within individuals and within demes, together with the genetic variance components in the ancestral population are used to obtain the variance within and among demes following a founder event. Examples are analyzed for single founder events of 1–25 individuals and multiple founder events of two individuals. Following a single founder event, the contribution of the additive variance to the variance within demes relative to the additive variance in the ancestral population is always less than one. However, the contribution of epistatic variance to the variance within demes relative to the epistatic variance in the ancestral population is always greater than one. Thus, while a founder event decreases the contribution of additive variance to the variance within demes, it increases the contribution of epistatic variance to the variance within demes. The contribution of epistatic variance to the variance among demes following a single founder event is not qualitatively different from the contribution of additive variance to the variance among demes. These results indicate that epistatic variance is less likely than additive variance to cause a genetic revolution following a single founder event. When populations undergo multiple founder events the situation changes considerably. Epistatic variance may contribute as much as four times its original value to the variance among demes, while additive variance can contribute maximally twice its original value to the variance among demes. Thus, epistasis, which is relatively unimportant following a single founder event, may have major evolutionary implications if drift is allowed to continue for several generations.

THE COMPARISON OF PHENOTYPIC PLASTICITY AND GENETIC VARIATION IN POPULATIONS OF THE GRASS DANTHONIA SPICATA

A species can persist in a heterogeneous environment either if individuals of that species are phenotypically flexible or if there is genetic variation among individuals (Thoday, 1953; Baker, 1965; Bradshaw, 1965; Jain, 1979). Phenotypic flexibility may be defined as the extent to which an organism can grow and reproduce in a range of environments either by varying its phenotype (plasticity) or by maintaining a constant phenotype (homeostasis or stability) (sensu Thoday, 1953; Hume and Cavers, 1982). Bradshaw (1965) recognized that phenotypic plasticity could itself be under genetic control and would therefore be subject to selective pressures. Bradshaw (1965) and others (Thoday, 1953; Levins, 1963; Marshall and Jain, 1968; Jain, 1979) have postulated that selection for phenotypic flexibility and genetic variation would be antagonistic, that there would be selection for a population to be either phenotypically flexible or genetically variable. Several studies comparing congeneric species (Cumming, 1959; Marshall and Jain, 1968; Jain, 1979) have found evidence that one of the species is more genetically variable and the other more phenotypically plastic. One study (Grant, 1974) has found differences in genetic variation and phenotypic plasticity among adjacent populations of a single species. The purpose of this paper is two-fold. First, we present mathematical definitions for plastic variation and plasticity. Second, we compare plastic vari-

Experimental Studies of Group Selection: What Do They Tell US About Group Selection in Nature?

The study of group selection has developed along two autonomous lines. One approach, which we refer to as the adaptationist school, seeks to understand the evolution of existing traits by examining plausible mechanisms for their evolution and persistence. The other approach, which we refer to as the genetic school, seeks to examine how currently acting artificial or natural selection changes traits within populations and focuses on current evolutionary change. The levels of selection debate lies mainly within the adaptationist school, whereas the experimental studies of group selection lie within the genetic school. Because of the very different traditions and goals of these two schools, the experimental studies of group selection have not had a major impact on the group selection debate. We review the experimental results of the genetic school in the context of the group selection controversy and address the following questions: Under what conditions is group selection effective? What is the genetic basis of a response to group selection? How common is group selection in nature?

Wright's shifting balance theory: an experimental study

Experimental confirmation of Wrights shifting balance theory of evolution, one of the most comprehensive theories of adaptive evolution, is presented. The theory is regarded by many as a cornerstone of modern evolutionary thought, but there has been little direct empirical evidence supporting it. Some of its underlying assumptions are viewed as contradictory, and the existence and efficacy of the theorys fundamental adaptive process, interdemic selection, is the focus of controversy. Interdemic selection was imposed on large arrays of laboratory populations of the flour beetle Tribolium castaneum in the manner described by Wright: the differential dispersion of individuals from demes of high fitness into demes of low fitness. A significant increase in average fitness was observed in the experimental arrays when compared to control populations with equivalent but random migration rates. The response was not proportional to the selection differential: The largest response occurred with interdemic selection every two generations rather than every generation or every three generations. The results indicate that the interdemic phase of Wrights shifting balance theory can increase average fitness and suggest that gene interactions are involved in the observed response.

The influence of environmental variation on group and individual selection in a cress

An experimental study of group and individual selection for leaf area under different patterns of environmental variation is presented. This study, which uses the cress Arabidopsis thaliana, demonstrates that group selection can occur in plants. The response to group selection was always in the expected direction, but surprisingly, the response to individual selection was not. Furthermore the interaction between group and individual selection was significant. Individual selection interfered with the response to group selection whether the two forces were acting in concert or were opposed. The effects of the environmental variation treatments were detected mainly as three‐way interactions with group and individual selection. Group selection was more effective in environments that interfered with individual selection, as well as in environments that did not interfere with group selection. These results suggest that the ability of a character to respond to group selection, individual selection, or both will depend on a great many factors and that the relative importance of the different levels of selection can only be determined empirically.

GENETIC VARIATION IN INBREEDING DEPRESSION IN THE RED FLOUR BEETLE TRIBOLIUM CASTANEUM

Inbreeding depression varies among species and among populations within a species. Few studies, however, have considered the extent to which inbreeding depression varies within a single population. We report on two experiments to provide evidence that inbreeding depression is genetically variable, such that within a single population some lineages suffer severe inbreeding depression, others suffer only mild inbreeding depression, and some lineages actually increase in phenotypic value at higher levels of inbreeding. We examine the effects of population structure on inbreeding depression for two traits in the first experiment (adult dry weight and female relative fitness), and for seven traits in the second experiment (female and male adult dry weight, female and male relative fitness, female and male developmental time, and egg‐to‐adult viability). In the first experiment, we collected data from 4 families within each of 38 lineages derived from a single ancestral stock population and maintained for four generations of full‐sib mating. Both traits demonstrate significant inbreeding depression and provide evidence that even within a single lineage there is significant genetic variability in inbreeding depression. In the second experiment, we collected data from 5 replicates for each of 15 lineages derived from the same ancestral population used in the first experiment; these lineages were maintained for four generations of full‐sib mating. We also collected data on outbred control beetles in each generation and incorporated these data into the analyses to account for environmental effects in an unbiased manner. All traits except female and male developmental time show significant inbreeding depression. All traits showing inbreeding depression are genetically variable in inbreeding depression, as is evident from a significant linear lineage‐×‐f component. For both experiments, the effect of population structure on inbreeding depression is further evident from the increasing amount of variation that can be explained by the models used to measure inbreeding depression when additional levels of population structure are included. Genetic variation in inbreeding depression has important implications for conservation biology and may be an important factor in mating‐system evolution.

Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes

Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organization—what is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon. ABSTRACT Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organization—what is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon. For instance, critiquing the hologenome concept is not synonymous with critiquing coevolution, and arguing that an entity is not a primary unit of selection dismisses the fact that the hologenome concept has always embraced multilevel selection. Holobionts and hologenomes are incontrovertible, multipartite entities that result from ecological, evolutionary, and genetic processes at various levels. They are not restricted to one special process but constitute a wider vocabulary and framework for host biology in light of the microbiome.