Michael J. Wade

On the measurement of natural and sexual selection : theory

The aim of this paper is to illustrate an approach to the empirical measurement of selection that is directly related to formal evolutionary theory. Recent field studies have demonstrated that it is feasible to measure fitness in natural populations. The most successful studies have yielded accurate tallies of survivorship, mating success and fertility (e.g., Tinkle, 1965; Howard, 1979; Downhower and Brown, 1980; Lennington, 1980; Kluge, 1981; Clutton-Brock et al., 1982). Despite this success, no concensus has been reached on how to analyze the data and relate them to evolutionary theory. We present here a mode of data analysis that describes selection in useful, theoretical terms, so that field or experimental results will have a tangible relationship to equations for evolutionary change. Multivariate, polygenic theory (Lande, 1979, 1980, 1981; Bulmer, 1980) is particularly useful as a conceptual framework because it is concerned with the evolution of continuously distributed traits such as those commonly studied in laboratory and field situations. Multivariate equations have been used for many years by plant and animal breeders in order to impose selection and predict its impact (Smith, 1936; Hazel, 1943; Dickerson et al., 1954, 1974; Yamada, 1977), but this quantitative genetic theory has only recently been applied to evolutionary problems. Definitions and Aims. -It is critical to distinguish between selection and evolutionary response to selection (Fisher, 1930; Haldane, 1954). Selection causes observable changes within a generation in the means, variances and covariances of phenotypic distributions. Thus selection can be described in purely phenotypic terms without recourse to the inheritance of characters. In contrast, evolutionary response to selection, for example, the change in phenotypic mean from one generation to the next, certainly does depend on inheritance. In the following sections we show how knowledge of inheritance can be combined with purely phenotypic measures of selection to predict evolutionary response to selection. By distinguishing between selection and response to selection we can measure selection on characters whose mode of inheritance may be unknown and make prediction of evolutionary response a separate issue. Thus knowledge of inheritance is essential for complete

On the measurement of natural and sexual selection: applications

In this paper, we use measures of selection developed by quantitative geneticists and some new results (Arnold and Wade, 1984) to analyze multiple episodes of selection in natural populations of amphibians, reptiles, and insects. These examples show how different methods of data collection influence the potential for relating field observations to formal evolutionary theory. We adhere to the Darwinian tradition of distinguishing between natural and sexual selection (Darwin, 1859, 1871; Ghiselin, 1974). We view sexual selection as selection arising from variance in mating success and natural selection as arising from variance in other components of fitness. The justification for this formal distinction is developed by Wade (1979), Lande (1980), Wade and Arnold (1980), Arnold and Houck (1982) and Arnold (1 983 a). (We define mating success as the number of mates that bear progeny given survival of the mating organsim to sexual maturity. We do not equate mating success with mere copulatory success.) The utility of the distinction between sexual and natural selection is that the two forms of selection may often act in opposite directions on particular characters (Darwin, 1859, 1871). While we find the distinction between these two forms of selection useful, the difference is not crucial to our analysis. The essential point is that the recognition of selection episodes permits analysis of selection that may change in magnitude and direction during the life cycle. Defining Fitness Components. -The key first step in the analysis of data is to define multiplicative components of fitness so that selection can be partitioned into parts corresponding to these components or episodes of selection. Using an animal example, if the number of offspring zygotes is taken as total fitness, we can define the following components of fitness: viability (survivorship to sexual maturity), mating success (the number of mates) and fertility per mate (the average number of zygotes produced per mate). These components of fitness are defined so that their product gives total fitness. As a second example, consider the components of fitness in a plant in which yield (seeds/plant) is taken as the measure of total fitness (Primack and Antonovics, 1981). We might define the following components of fitness: number of stems per plant, average number of inflorescences per stem, average number of seed capsules per inflorescence, and average number of seeds per capsule. Again, these four fitness components are defined so that their product gives total fitness. We will need to measure each component of fitness and each character on each individual in order to partition selection into parts corresponding to the separate episodes of selection or to the separate components of fitness. Thus in the animal example, we need to measure the viability, mating success and fertility of each individual. With this accomplished we can estimate the separate forces of viability, sexual and fertility selection on each phenotypic character. In addition we can calculate the opportunities of selection corresponding to these three episodes and covariances between the different kinds of selection. In the plant example, we might begin with the intuition that larger plants have a greater yield. Using our methodology we can reword and extend this intuition. We can not only test the proposition of

Evolutionary consequences of indirect genetic effects

Indirect genetic effects (IGEs) are environmental influences on the phenotype of one individual that are due to the expression of genes in a different, conspecific, individual. Historically, work has focused on the influence of parents on offspring but recent advances have extended this perspective to interactions among other relatives and even unrelated individuals. IGEs lead to complicated pathways of inheritance, where environmental sources of variation can be transmitted across generations and therefore contribute to evolutionary change. The existence of IGEs alters the genotype-phenotype relationship, changing the evolutionary process in some dramatic and non-intuitive ways.

Extinction and recolonization : Their effects on the genetic differentiation of local populations

In this paper, we use a model by Slatkin (1977) to investigate the genetic effects of extinction and recolonization for a species whose population structure consists of an array of local demes with some migration among them. In particular, we consider the conditions under which extinction and recolonization might enhance or diminish gene flow and increase or decrease the rate of genetic differentiation relative to the static case with no extinctions. We explicitly take into account the age‐structure that is established within the array of populations by the extinction and colonization process. We also consider two different models of the colonization process, the so‐called “migrant pool” and “propagule pool” models. Our theoretical studies indicate that the genetic effects of extinction and colonization depend upon the relative magnitudes of K, the number of individuals founding new colonies, and 2Nm, twice the number of migrants moving into extant populations. We find that these genetic effects are surprisingly insensitive to the extinction rate. We conclude that, in order to assess the genetic effects of the population dynamics, we must first answer an important empirical question that is essentially ecological: is colonization a behavior distinct from migration?

A Critical Review of the Models of Group Selection

Group selection is defined as that process of genetic change which is caused by the differential extinction or proliferation of groups of organisms. A very large proportion of the literature pertaining to group selection consists of theoretical papers; the genetic problems of group selection have been addressed from many different mathematical viewpoints. The general conclusion has been that, although group selection is possible, it cannot override the effects of individual selection within populations except for a highly restricted set of parameter values. Since it is unlikely that conditions in natural populations would fall within the bounds imposed by the models, group selection, by and large, has been considered an insignificant force for evolutionary change. These theoretical conclusions and the assumptions from which they have been derived are reexamined in the light of recent empirical studies of group selection with laboratory populations of the flour beetle, Tribolium (Wade, 1976, 1977). It is shown that the models have a number of assumptions in common which are inherently unfavorable to the operation of group selection. Alternative assumptions derived from the empirical results are suggested and discussed in the hope that they will stimulate further theoretical and empirical study of this controversial subject.

The causes of natural selection.

We discuss the necessary and sufficient conditions for identifying the cause of natural selection on a phenotypic trait. We reexamine the observational methods recently proposed for measuring selection in natural populations and illustrate why the multivariate analysis of selection is insufficient for identifying the causal agents of selection. We discuss how the observational approach of multivariate selection analysis can be complemented by experimental manipulations of the phenotypic distribution and the environment to identify not only how selection is operating on the phenotypic distribution but also why it operates in the observed manner. A significant point of departure of our work from recent discussions is in regard to the role of the environment in the study of natural selection. Instead of viewing the environment as a source of unwanted variation that obscures the relationship between phenotype and fitness, we view fitness as arising from the interaction of the phenotype with the environment. The biotic and abiotic environment is the context that gives rise to the relationship between phenotype and fitness (selection). The analysis of the causes of selection is in essence a problem in ecology. The experimental study of the association between selection gradients and environmental characteristics is necessary to identify the agents of natural selection. We recommend research methods for identifying the agency of selection that depend upon a reciprocity between the observational approach of multivariate selection analysis and the manipulative approach of field experiments in evolutionary ecology.

The intensity of sexual selection in relation to male sexual behaviour, female choice, and sperm precedence.

Abstract In this paper we define sexual selection on males as the variance in numbers of mates per male and show how the intensity of this selection is affected by male sexual behaviour, female choice, sex ratio, and modes of sperm precedence. This definition coincides with Darwins conception of sexual selection but differs from some post-Darwinian views. For systems of single-male paternity, we show that the intensity of total selection on male reproductive success equals the intensity of natural selection on female fertility, times the sex ratio, plus the intensity of sexual selection on males. The absolute intensity of sexual selection is unaffected by the system of sperm precedence. The application of the results to field studies is discussed.

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.

What are maternal effects (and what are they not)

Maternal effects can play an important role in a diversity of ecological and evolutionary processes such as population dynamics, phenotypic plasticity, niche construction, life-history evolution and the evolutionary response to selection. However, although maternal effects were defined by quantitative geneticists well over half a century ago, there remains some confusion over exactly what phenomena should be characterized as maternal effects and, more importantly, why it matters and how they are defined. We suggest a definition of maternal effects as the causal influence of the maternal genotype or phenotype on the offspring phenotype. This definition differs from some definitions in that it treats maternal effects as a phenomenon, not as a statistical construct. The causal link to maternal genotype or phenotype is the critical component of this definition providing the link between maternal effects and evolutionary and ecological processes. We show why phenomena such as maternal cytoplasmic inheritance and genomic imprinting are distinct genetically from and have different evolutionary consequences than true maternal effects. We also argue that one should consider cases where the maternal effect is conditional on offspring genotype as a class of maternal effects.

The evolutionary ecology of metacommunities.

Research on the interactions between evolutionary and ecological dynamics has largely focused on local spatial scales and on relatively simple ecological communities. However, recent work demonstrates that dispersal can drastically alter the interplay between ecological and evolutionary dynamics, often in unexpected ways. We argue that a dispersal-centered synthesis of metacommunity ecology and evolution is necessary to make further progress in this important area of research. We demonstrate that such an approach generates several novel outcomes and substantially enhances understanding of both ecological and evolutionary phenomena in three core research areas at the interface of ecology and evolution.