PEAK SHIFTS AND POLYMORPHISM DURING PHASE THREE OF WRIGHT'S SHIFTING-BALANCE PROCESS

The third phase of Wright's shifting-balance theory involves the export of adaptive gene combinations from one subpopulation to another. Previous results have demonstrated that this can occur at very low migration rates, but it has been argued that this simply reflects the ability of migration to overcome selection and fix any (even deleterious) alleles. Here, previous analyses are extended by concentrating on the critical balance between forward and reverse migration rates that still allows phase III to proceed. It is shown that selective advantage, dominance, recombination rate, and the number of loci all affect the ability of a genotype to invade and become fixed in a new subpopulation, but it is unlikely that phase III will occur in the absence of differential migration unless the invading genotype consists of a few dominant loci with a large selection advantage, spreading into a few populations of lower fitness. Therefore, as was envisioned by Wright, differential migration from more to less fit populations will be necessary for phase III to occur under most circumstances.     

PHASE III OF WRIGHT'S SHIFTING BALANCE PROCESS AND THE VARIANCE AMONG DEMES IN MIGRATION RATE

Interdemic selection by the differential migration of individuals out from demes of high fitness and into demes of low fitness (Phase III) is one of the most controversial aspects of Wright's Shifting Balance Theory. I derive a relationship between Phase III migration and the interdemic selection differential, S, and show its potential effect on F_ST. The relationship reveals a diversifying effect of interdemic selection by Phase III migration on the genetic structure of a metapopulation. Using experimental metapopulations, I explored the effect of Phase III migration on F_ST by comparing the genetic variance among demes for two different patterns of migration: (1) island model migration and (2) Wright's Phase III migration. Although mean migration rates were the same, I found that the variance among demes in migration rate was significantly higher with Phase III than with island model migration. As a result, F_ST for the frequency of a neutral marker locus was higher with Phase III than it was with island model migration. By increasing F_ST, Phase III enhanced the genetic differentiation among demes for traits not subject to interdemic selection. This feature makes Wright's process different from individual selection which, by reducing effective population size, decreases the genetic variance within demes for all other traits. I discussed this finding in relation to the efficacy of Phase III and random migration for effecting peak shifts, and the contribution of genes with indirect effects to among‐deme variation.     

A SIMULATION OF WRIGHT'S SHIFTING-BALANCE PROCESS: MIGRATION AND THE THREE PHASES

Wright partitioned the shifting-balance process into three phases. Phase one is the shift of a deme within a population to the domain of a higher adaptive peak from that of the historical peak. Phase two is mass selection within a deme towards that higher peak. Phase three is the conversion of additional demes to the higher peak. The migration rate between demes is critical for the existence of phases one and three. Phase one requires small effective population sizes, hence low migration rates. Phase three is optimal under high migration rates that spread the most-fit genotype from deme to deme. Thus, a population-wide peak shift requires intermediate levels of migration. By altering the rates of phases one and three, migration affects the predominant direction of mass selection within a population. This study examines the degree to which migration, through its effects on phases one and three, determines the probability of a simulated population arriving at its genotypic optimum after 12,000 generations. These simulations reveal that there is a range of migration rates for which an entire population might be expected to shift to a higher peak. Below m = 0.001 peak shifts occur frequently (phases I and II) but are not successfully exported out of subpopulations (phase III), and above 0.01 peak shifts within demes (phase I and II), required to initiate phase III, become increasingly uncommon. Because it is unlikely that real populations will have uniform migration rates from generation to generation, the probable effects of varying migration rates on broadening the range of conditions producing peak shifts are discussed.     

FIXATION OF MUTATORS IN ASEXUAL POPULATIONS: THE ROLE OF GENETIC DRIFT AND EPISTASIS

We study the evolutionary dynamics of an asexual population of nonmutators and mutators on a class of epistatic fitness landscapes. We consider the situation in which all mutations are deleterious and mutators are produced from nonmutators continually at a constant rate. We find that in an infinitely large population, a minimum nonmutator‐to‐mutator conversion rate is required to fix the mutators but an arbitrarily small conversion rate results in the fixation of mutators in a finite population. We calculate analytical expressions for the mutator fraction at mutation‐selection balance and fixation time for mutators in a finite population when the difference between the mutation rate for mutator and nonmutator is smaller (regime I) and larger (regime II) than the selection coefficient. Our main result is that in regime I, the mutator fraction and the fixation time are independent of epistasis but in regime II, mutators are rarer and take longer to fix when the decrease in fitness with the number of deleterious mutations occurs at an accelerating rate (synergistic epistasis) than at a diminishing rate (antagonistic epistasis). Our analytical results are compared with numerics and their implications are discussed.     

EPISTASIS AND THE EVOLUTION OF ADDITIVE GENETIC VARIANCE IN POPULATIONS THAT PASS THROUGH A BOTTLENECK

Traditional models of genetic drift predict a linear decrease in additive genetic variance for populations passing through a bottleneck. This perceived lack of heritable variance limits the scope of founder-effect models of speciation. We produced 55 replicate bottleneck populations maintained at two male-female pairs through four generations of inbreeding (average F = 0.39). These populations were formed from an F₂ intercross of the LG/J and SM/J inbred mouse strains. Two contemporaneous control strains maintained with more than 60 mating pairs per generation were formed from this same source population. The average level of within-strain additive genetic variance for adult body weight was compared between the control and experimental lines. Additive genetic variance for adult body weight within experimental bottleneck strains was significantly higher than expected under an additive genetic model This enhancement of additive genetic variance under inbreeding is likely to be due to epistasis, which retards or reverses the loss of additive genetic variance under inbreeding for adult body weight in this population. Therefore, founder-effect speciation processes may not be constrained by a loss of heritable variance due to population bottlenecks.     

EPISTASIS AS A SOURCE OF INCREASED ADDITIVE GENETIC VARIANCE AT POPULATION BOTTLENECKS

The role of epistasis in evolution and speciation has remained controversial. We use a new parameterization of physiological epistasis to examine the effects of epistasis on levels of additive genetic variance during a population bottleneck. We found that all forms of epistasis increase average additive genetic variance in finite populations derived from initial populations with intermediate allele frequencies. Average additive variance continues to increase over many generations, especially at larger population sizes (N = 32 to 64). Additive-by-additive epistasis is the most potent source of additive genetic variance in this situation, whereas dominance-by-dominance epistasis contributes smaller amounts of additive genetic variance. With additive-by-dominance epistasis, additive genetic variance decreases at a relatively high rate immediately after a population bottleneck, rebounding to higher levels after several generations. Empirical examples of epistasis for murine adult body weight based on measured genotypes are provided illustrating the varying effects of epistasis on additive genetic variance during population bottlenecks.     

THE ACTION OF STABILIZING SELECTION,MUTATION, AND DRIFT ON EPISTATIC QUANTITATIVE TRAITS

For a quantitative trait under stabilizing selection, the effect of epistasis on its genetic architecture and on the changes of genetic variance caused by bottlenecking were investigated using theory and simulation. Assuming empirical estimates of the rate and effects of mutations and the intensity of selection, we assessed the impact of two‐locus epistasis (synergistic/antagonistic) among linked or unlinked loci on the distribution of effects and frequencies of segregating loci in populations at the mutation‐selection‐drift balance. Strong pervasive epistasis did not modify substantially the genetic properties of the trait and, therefore, the most likely explanation for the low amount of variation usually accounted by the loci detected in genome‐wide association analyses is that many causal loci will pass undetected. We investigated the impact of epistasis on the changes in genetic variance components when large populations were subjected to successive bottlenecks of different sizes, considering the action of genetic drift, operating singly (D), or jointly with mutation (MD) and selection (MSD). An initial increase of the different components of the genetic variance, as well as a dramatic acceleration of the between‐line divergence, were always associated with synergistic epistasis but were strongly constrained by selection.     

THE OCCURRENCE AND SIGNIFICANCE OF EPISTATIC VARIANCE FOR QUANTITATIVE CHARACTERS AND ITS MEASUREMENT IN HAPLOIDS

Epistatic genetic variance for quantitative traits may play an important role in evolution, but detecting epistasis in diploid organisms is difficult and requires complex breeding programs and very large sample sizes. We develop a model for detecting epistasis in organisms with a free-living haploid stage in their life cycles. We show that epistasis is indicated by greater variance among families of haploid progeny derived from individual diploids than among clonally replicated haploid sibs from the same sporophyte. Simulations show that the power to detect epistasis is linearly related to the number of sporophytes and the number of haploids per sporophyte in the dataset. We illustrate the model with data from growth variation among gametophytes of the moss, Ceratodon purpureus. The experiment failed to detect epistatic variance for biomass production, although there was evidence of additive variance.     

THE EFFECTS OF SELECTION AND GENETIC DRIFT ON THE GENOMIC DISTRIBUTION OF SEXUALLY ANTAGONISTIC ALLELES

Sexual antagonism (SA) occurs when an allele that is beneficial to one sex, is detrimental to the other. This conflict can result in balancing, directional, or disruptive selection acting on SA alleles. A body of theory predicts the conditions under which sexually antagonistic mutants will invade and be maintained in stable polymorphism under balancing selection. There remains, however, considerable debate over the distribution of SA genetic variation across autosomes and sex chromosomes, with contradictory evidence coming from data and theory. In this article, we investigate how the interplay between selection and genetic drift will affect the genomic distribution of sexually antagonistic alleles. The effective population sizes can differ between the autosomes and the sex chromosomes due to a number of ecological factors and, consequently, the distribution of SA genetic variation in genomes. In general, we predict the interplay of SA selection and genetic drift should lead to the accumulation of SA alleles on the X in male heterogametic (XY) species and, on the autosomes in female heterogametic (ZW) species, especially when sexual competition is strong among males.     

A LIFE-HISTORY BASED STUDY OF POPULATION GENETIC STRUCTURE: SEED BANK TO ADULTS IN PLANTAGO LANCEOLATA

We explored the extent to which the soil seed bank differed genetically and spatially in comparison to two actively growing stages in a natural population of Plantago lanceolata. All seed-bank seeds, seedlings, and adults of P. lanceolata within eight subunits in a larger population were mapped, subjected to starch gel electrophoresis, and allozyme analysis in 1988. Gel electrophoresis was also used to estimate the mating system in two years, 1986 and 1988. The spatial distributions of seeds, seedlings, and adults were highly coincident. Allele frequencies of the dormant seeds differed significantly from those of the adults for four of the five polymorphic loci. In addition, a comparison of the genotype frequencies of the three life-history stages indicated that the seed bank had an excess of homozygotes. Homozygosity, relative to Hardy-Weinberg expectations, decreased during the life cycle (for seed bank, seedlings, and adults respectively: F_it = 0.19, 0.09, 0.01; F_is = 0.14, 0.04, -0.12). Spatial genetic differentiation increased sixfold during the life cycle: (for seed bank, seedling and adults: F_s1??? = 0.02, 0.05, 0.12). The apparent selfing rate was 0.01 in 1986 and 0.09 in 1988. These selfing rates are not large enough to account for the elevated homozygosity of the seed bank. Inbreeding depression, overdominance for fitness, and a “temporal Wahlund's effect” are discussed as possible mechanisms that could generate high homozygosity in the seed bank, relative to later life-history stages. In Plantago lanceolata, the influence of the mating system and the “genetic memory” of the seed bank are obscured by the time plants reach the reproductive stage.     

CORRELATION OF PAIRWISE GENETIC AND GEOGRAPHIC DISTANCE MEASURES: INFERRING THE RELATIVE INFLUENCES OF GENE FLOW AND DRIFT ON THE DISTRIBUTION OF GENETIC VARIABILITY

Attempts to relate estimates of regional F_ST to gene flow and drift via Wright's (1931) equation F_ST ≈ 1/ (4Nm + 1) are often inappropriate because most natural sets of populations probably are not at equilibrium (McCauley 1993), as assumed by the island model upon which the equation is based, or ineffective because the influences of gene flow and drift are confounded in the product Nm. Evaluations of the association between genetic (F_ST) and geographic distances separating all pairwise populations combinations in a region allows one to test for regional equilibrium, to evaluate the relative influences of gene flow and drift on population structure both within and between regions, and to visualize the behavior of the association across all degrees of geographic separation. Tests of the model using microsatellite data from 51 populations of eastern collared lizards (Crotaphytus collaris collaris) collected from four distinct geographical regions gave results highly consistent with predicted patterns of association based on regional differences in various historical and ecological factors that affect the amount of drift and gene flow. The model provides a prerequisite for and an alternative to regional F_ST analyses, which often simply assume regional equilibrium, thus potentially leading to erroneous and misleading inferences regarding regional population structure.     

NEUTRAL THEORY OF QUANTITATIVE GENETIC VARIANCE IN AN ISLAND MODEL WITH LOCAL EXTINCTION AND COLONIZATION

Additive genetic variance maintained by mutation in a selectively neutral quantitative character is analyzed for an ideal population distributed on n islands, each with local effective size N, that exchange migrants at a small rate, m. In a stable population structure, the expected genetic variance maintained within islands is identical to that in a panmictic population of the same total size, regardless of the migration rate (m > 0). This result contrasts with Wright's classical conclusion, based on inbreeding coefficients, that at least one immigrant per island every other generation (Nm > ½) is necessary for the genetic variance within local populations to approach that under panmixia. The expected genetic variance maintained among islands is inversely proportional to m and increases with the number of islands, but is independent of N. Local extinction and colonization diminish the genetic variance maintained within islands by reducing the effective size of island populations through the founder effect, although the expected genetic variance within islands is nearly as large as that in a panmictic population of the same total effective size. If the founders of new colonies originate from more than one island, rates of local extinction and colonization larger than about twice the migration rate will substantially reduce the genetic variance maintained among islands. These results indicate the importance of mutation and migration in maintaining quantitative genetic variance within small local populations.     

SEX-SPECIFIC GENETIC VARIANCE AND THE EVOLUTION OF SEXUAL DIMORPHISM: A SYSTEMATIC REVIEW OF CROSS-SEX GENETIC CORRELATIONS

The independent evolution of the sexes may often be constrained if male and female homologous traits share a similar genetic architecture. Thus, cross-sex genetic covariance is assumed to play a key role in the evolution of sexual dimorphism (SD) with consequent impacts on sexual selection, population dynamics, and speciation processes. We compiled cross-sex genetic correlations ( r _MF) estimates from 114 sources to assess the extent to which the evolution of SD is typically constrained and test several specific hypotheses. First, we tested if r _MF differed among trait types and especially between fitness components and other traits. We also tested the theoretical prediction of a negative relationship between r _MF and SD based on the expectation that increases in SD should be facilitated by sex-specific genetic variance. We show that r _MF is usually large and positive but that it is typically smaller for fitness components. This demonstrates that the evolution of SD is typically genetically constrained and that sex-specific selection coefficients may often be opposite in sign due to sub-optimal levels of SD. Most importantly, we confirm that sex-specific genetic variance is an important contributor to the evolution of SD by validating the prediction of a negative correlation between r _MF and SD.     

SEXUAL SELECTION CAN INCREASE THE EFFECT OF RANDOM GENETIC DRIFT—A QUANTITATIVE GENETIC MODEL OF POLYMORPHISM IN OOPHAGA PUMILIO,THE STRAWBERRY POISON‐DART FROG

The variation in color pattern between populations of the poison‐dart frog Oophaga pumilio across the Bocas del Toro archipelago in Panama is suggested to be due to sexual selection, as two other nonsexually selecting Dendrobatid species found in the same habitat and range do not exhibit this variation. We theoretically test this assertion using a quantitative genetic sexual selection model incorporating aposematic coloration and random drift. We find that sexual selection could cause the observed variation via a novel process we call “coupled drift.” Within our model, for certain parameter values, sexual selection forces frog color to closely follow the evolution of female preference. Any between‐population variation in preference due to genetic drift is passed on to color. If female preference in O. pumilio is strongly affected by drift, whereas color in the nonsexually selecting Dendrobatid species is not, coupled drift will cause increased between‐population phenotypic variation. However, with different parameter values, coupled drift will result in between‐population variation in color being suppressed compared to its neutral value, or in little or no effect. We suggest that coupled drift is a novel theoretical process that could have a role linking sexual selection with speciation both in O. pumilio, and perhaps more generally.     

EVOLUTION IN FLUCTUATING ENVIRONMENTS: DECOMPOSING SELECTION INTO ADDITIVE COMPONENTS OF THE ROBERTSON–PRICE EQUATION

We analyze the stochastic components of the Robertson–Price equation for the evolution of quantitative characters that enables decomposition of the selection differential into components due to demographic and environmental stochasticity. We show how these two types of stochasticity affect the evolution of multivariate quantitative characters by defining demographic and environmental variances as components of individual fitness. The exact covariance formula for selection is decomposed into three components, the deterministic mean value, as well as stochastic demographic and environmental components. We show that demographic and environmental stochasticity generate random genetic drift and fluctuating selection, respectively. This provides a common theoretical framework for linking ecological and evolutionary processes. Demographic stochasticity can cause random variation in selection differentials independent of fluctuating selection caused by environmental variation. We use this model of selection to illustrate that the effect on the expected selection differential of random variation in individual fitness is dependent on population size, and that the strength of fluctuating selection is affected by how environmental variation affects the covariance in Malthusian fitness between individuals with different phenotypes. Thus, our approach enables us to partition out the effects of fluctuating selection from the effects of selection due to random variation in individual fitness caused by demographic stochasticity.     

HIERARCHICAL GENETIC STRUCTURE AND GENE FLOW IN MACROGEOGRAPHIC POPULATIONS OF THE EASTERN TENT CATERPILLAR (MALACOSOMA AMERICANUM)

Genetic structure and inferred rates of gene flow in macrogeographic populations of the eastern tent caterpillar Malacosoma americanum were analyzed at two hierarchical scales: local demes and regional subpopulations. Wright's F-statistics were used to estimate population genetic structure using multilocus genotypic data generated electrophoretically. Estimated values of F_ST and the distribution of private alleles were then used to obtain indirect estimates of gene flow. We found modest, though significant, genetic structure at both spatial scales, a pattern consistent with high rates of gene flow over the large distances involved. Modest values obtained for Nei's genetic distance also suggested high levels of gene flow across the range of this species, although some gene-flow restriction resulting from isolation by distance was suggested by a positive regression of genetic distance on geographic distance. The observed homogeneity at enzyme loci across the range of M. americanum parallels the reported uniformity in morphology, suggesting a general absence of local genetic differentiation in this widely distributed species. The genetic homogeneity observed in this wide-ranging insect is discussed in terms of organism-specific environmental experience at different spatial scales. Some organisms occupying apparently heterogeneous environments may ameliorate unsuitable local conditions through microhabitat selection or behavioral modification of their microenvironment. This may be accomplished in M. americanum through group shelter construction and behavioral thermoregulation, closely tying thermoregulation to social biology in this species. If in this way the tent helps produce an effectively homogeneous environment for this species across its extensive range, this system may provide a unique example of how social behavior can influence the distribution of genetic variation in a population.     

SLOWER TEMPO OF MICROEVOLUTION IN ISLAND BIRDS: IMPLICATIONS FOR CONSERVATION BIOLOGY

Whether microevolution on small islands differs from that on larger landmasses is a key question in biology with substantial implications for species conservation. However, due to the difficulties faced in producing adequately replicated samples and in controlling for confounding variables, prior attempts to examine evolutionary questions relating to habitat area and population size have produced equivocal results. Here we show, using experimental design criteria that reduce the potential for such confounding, that bird species on larger landmasses have higher rates of molecular evolution. The study involves a global dataset of 48 independent contrasts for the cytochrome b gene encompassing all possible paired sister species comparisons (from seven orders and 17 families) that were available at the time of dataset assembly. A more rapid evolutionary tempo in larger areas has important ramifications for biodiversity conservation because it indicates a new imperative, beyond that of simply maintaining preexisting genetic diversity, for securing large areas for threatened species. This result suggests that the trend of confining species to limited refugia is likely to be slowing the tempo of microevolution. That effect might constrain the potential for adaptive shifts in response to changing environments such as those associated with global warming.