Donald A. Levin

Gene Flow in Seed Plants

Gene dispersal (flow, or migration) within and between plant populations has been of continuous interest to plant breeders and seed producers for many decades. Economic considerations have stimulated studies of gene flow as a function of distance, breeding system, pollinating agent, and planting design in numerous domestic plants. Only during the past two decades have a large body of plant evolutionists become interested in information accruing from these studies, and in the rates of gene flow in wild populations. Their efforts have concentrated primarily on related problems such as adaptations for and mechanics of pollen and seed (or fruit) dispersal, plant-pollinator coevolution, adaptive radiation in pollination and seed dispersal mechanisms, and colonization and the alteration of species boundaries. Early in this century, anecdoctal evidence on the movement of pollen and seed vectors, dispersal of pollen by wind, and the range extensions of weed species led to the casual assumption that gene flow must be extensive, and that it must play a major role in the cohesion of populations and population systems. This view eroded as more information became available and was more critically interpreted (e.g., Grant, 1958, 1971; Ehrlich and Raven, 1969; Stebbins, 1970a; Bradshaw, 1972).

Evolutionary Consequences of Seed Pools

The annual habit in plants is often accompanied by specialized physiological mechanisms which permit seeds to remain dormant for a few years to decades. This results in the establishment of a seed pool from which germinating individuals are drawn. The seed pool causes an overlapping of generations in a population which would otherwise be subdivided into discrete generations. Others have examined seed pools per se as evolutionary strategies, but we are examining the constraints a seed pool imposes on the evolution of loci controlling seedling and adult characters not directly related to seed dormancy. Since a seed pool introduces genetic constraints for all loci simultaneously, there is not one evolutionary impact of seed pools upon an annual population, but many. For those loci that yield constant fitness effects, the presence of a seed pool retards the annual rate of allele frequency change, but does not alter the final equilibrium. However, for those loci interacting with variable features of the environment in producing their fitness effects, the seed pool can alter the ultimate genetic outcome. In a cyclical environment, the seed pool can dampen fitness cycles with a short period (with respect to the extent of the seed pool over past years) and accentuate long cycles. More importantly, the seed pool may serve as an evolutionary filter that causes only a few years from the cycle to have any true evolutionary impact and to effectively eliminate the selective impact of other years. This evolutionary filter also operates for those loci interacting with environmental elements that fluctuate randomly from year to year. Hence, seed pools can greatly reduce the fitness uncertainty generated by cyclical or random environments and free the plant population from having to respond genetically to the fitness conditions realized in every year. Moreover, the seed pool allows the absolute quality of a given years environment to influence allele frequency changes and not just the relative fitnesses of the genotypes at that locus. Finally, we examined the selectively analogous situation of seedling and juvenile selection in perennial plants lacking a seed pool. In this case, the standing crop replaces the seed pool as the agent causing an overlapping of generations. Most of the conclusions about the evolutionary effects of seed pools in annuals carry over to the evolutionary effects of standing crops on seedling and juvenile selection in perennials. However, the evolutionary filter caused by a standing crop is less effective in filtering random seedling and juvenile fitness fluctuations in perennials than the filter caused by a seed pool with respect to random fitness fluctuations in annuals.

Competition for Pollinators between Simultaneously Flowering Species

Species with similar floral structures and with similar flowering periods and time of pollen and nectar presentation may compete for the service of the same pollinators. The outcome of interspecific competition was analyzed with a simple two-species model. The reproductive success of a species depends on its relative frequency. The minority species will be at a reproductive handicap because it suffers a larger percentage of heterospecific pollinations. The reproductive handicap of the minority species leads to a smaller standing crop in the next generation, which in turn enhances the minority disadvantage. This should lead to rapid exclusion of the minority species from the immediate flora. An increase in pollinator constancy to a given plant species retards the elimination of the rarer species. Pollinator preference for a given plant species may enhance or retard this progression depending on whether the minority species is preferred, since preference alters the effective frequencies of the two species. The minority disadvantage is reduced if the competing species have different habitat requirements or if they form large patches of regular size.

Pest Pressure and Recombination Systems in Plants

An open recombination system would be of immediate and manifest value to plant species experiencing pathogen and pest pressures which are intense, systematic, and capable of redirection in the event the host alters its defensive posture. These pressures are most important in climax communities, well exemplified in the tropics and on ancient islands, where open recombination prevails and is promoted. The simple genetic bases for host resistance and pathogen or pest virulence, the vulnerability of species with restricted recombinations to disease epidemics and pest outbreaks, and the ability of pathogens and pests to rapidly evolve resistance to new natural or synthetic biocides provide the empirical superstructure for postulating why the genomes of K-selected species do not congeal.

Plant Phenolics: An Ecological Perspective

Plant phenolics are a structurally diverse group of compounds synthesized by all higher plants. The toxicity of phenolics and the products of their hydrolysis and oxidation has long been appreciated, and has implicated this group of natural products with plant defense. Unfortunately, much of the literature relating phenolics to plant defense is published in sources rarely consulted by evolutionists or ecologists. The purpose of this paper is to make a case for plant phenolics as defensive substances by considering their structural diversity, concentration, alteration upon infection, and mode of action. Correlations between ecogeographical and ecological parameters and phenolic profiles are discussed in light of the putative defensive role of phenolics, and additional correlations are predicted.

INBREEDING DEPRESSION AND PROXIMITY-DEPENDENT CROSSING SUCCESS IN PHLOX DRUMMONDII

Viability depression is a typical consequence of inbreeding in cross-fertilizing species. In some populations of Homo sapiens (Schull and Neel, 1965; FreireMaia and Azevedo, 1971; Schull et al., 1970) and Drosophila (Dobzhansky et al., 1963; Stone et al., 1963; MalogolowkinCohen et al., 1964; Mettler et al., 1966), the level of viability depression is linearly dependent on the inbreeding coefficient of an individual. If extrapolated to the maximum level (F = 1) from sib and cousin values, mortality due to homozygosity for detrimental genes would exceed 50% in most Homo and Drosophila populations. In most populations of Homo and Drosophila, the mean number of lethal equivalents per zygote is between 1 and 4. Populations of Tribolium also fall within this range (Levene et al., 1965). Viability depression following inbreeding in angiosperms is similar to that in the aforementioned animals. The mean numbers of lethal equivalents per zygote are as follows: Secale cereale, 2.7 (Landes, 1939); Medicago sativa, 1.2-4.5 (Cooper and Brink, 1940; Sayers and Murphy, 1966); Fagopyrum esculentum, 1.3-5.2 (Komaki, 1982); and Stylidium spathulatum, 3.4 (James, 1979). Among conifer species, the mean number of lethal equivalents per zygote varies from 1 to 10, values exceeding 8 in Pinus and Pseudotsuga (Sorensen, 1969; Franklin, 1972; Koski, 1973). Ferns are similar to conifers in their range of lethal equivalents (Klekowski, 1970; Ganders, 1972; Lloyd, 1974; Saus and Lloyd, 1976). The magnitude of viability depression from inbreeding in plants is dependent upon genetic and environmental variables. The frequency of lethal and detrimental genes in populations is a prime factor. It exceeds .15 in several species (Apirion and Zohary, 1961; Crumpacker, 1967; Kiang and Libby, 1972; Ohnishi, 1979; Komaki, 1982). The level of viability depression also is governed by the tolerance of species to higher levels of homozygosity (Mayo, 1980). Species whose genetic systems are adapted to relatively high levels of homozygosity are likely to show the least viability depression with inbreeding. Finally, the viability differential between outcross and inbred progeny is influenced by environmental quality. Under conditions of drought, disease and other stresses, the relative viability of inbreds is much poorer than under favorable conditions (Allard and Hansche, 1964; Pawsey, 1964; Koski, 1973; Libby et al., 1981). Viability depression in plants is most pronounced during seed development. For example, in Pseudotsuga menziesii, about 95% of the lethality following inbreeding occurs prior to germination (Orr-Ewing, 1957). Seed abortion usually is 2 to 10 times greater following selffertilization than cross-fertilization in conifers (Sorensen, 1969; Koski, 1971, 1973; Franklin, 1972; Birshir and Pepper, 1977) and angiosperms (Brink and Cooper, 1947; Linck, 1961; Rowlands, 1960; Sayers and Murphy, 1966; James, 1979). If the products of self-fertilization or crosses among sibs have reduced viability relative to outcrosses, we may expect progeny from neighboring plants in natural populations to have lower viability than those from distant plants when plant relatedness declines with distance. This relationship between proximity and relatedness would be a consequence of restricted pollen and seed dispersal, and is

The Origin of Isolating Mechanisms in Flowering Plants

Genetically conditioned mechanisms which restrict or limit gene exchange between coexisting species or population systems permit the preservation of their genetic integrity, and afford evolutionary independence. In the absence of genetically controlled isolation, coexisting populations would fuse into a single variable population. The fact that biotically sympatric populations which differ in adaptive mode almost invariably maintain their identity is prima facie evidence for their genetic isolation. Genetic isolation is evident in some form in essentially every genus where it has been sought. The degree of isolation need not be a function of genetic divergence or taxonomic distance, although in most instances a positive correlation may be found.

Alkaloid-bearing plants: an ecogeographic perspective

The incidence of alkaloid-bearing plants is dependent upon their habit and ecogeographical distribution. Among annual species the incidence of alkaloids is nearly twice that of perennials, among tropical floras nearly twice that of temperate floras, and a latitudinal cline is evident. In New Guinea, disparate communities differ in the incidence of alkaloid-bearing species and in the amount of alkaloid contained in their vegetative tissues. Families primarily distributed in the tropics have a higher percentage of alkaloid-bearing species than do those of temperate regions or those with cosmopolitan distributions. The most primitive orders, Magnoliales and Ranales, have a higher percentage of alkaloid-bearing species than the remainder of the dicots. These findings are discussed from the vantage point of coevolutionary theory. It is suggested that the ecogeographic patterns may be the result of differences in pest pressure, the alkaloids playing a defensive role in plants.

THE DEPENDENCE OF BEE-MEDIATED POLLEN AND GENE DISPERSAL UPON PLANT DENSITY

Pollen dispersal and pollen-mediated gene dispersal in flowering plants are effected primarily by animals and air currents. It is generally accepted that the dispersal of pollen within a colony of a given species is under the control of these agents and beyond the control of the colony. This view may be valid in the case of anemophilous plants where alterations of colony parameters ostensibly would have no effect upon the characteristics of pollen flow, since these parameters would not affect the transferal agent. However, in entomophilous plants, pollen and associated gene movements are mediated by vectors which may be sensitive to stimuli emanating from the colony. If pollinators respond to such stimuli, permutations of which would alter foraging behavior, the colony, wittingly or unwittingly, would control the dispersal of its pollen and genes. A recent study on pollinator flight patterns in Liatris aspera (Levin and Kerster, 1969) has shown that plant density and spacing control the feeding-flight behavior of bees and the movement of pollen which they bear. The present investigation was undertaken to determine whether the dependence of bee-flight characteristics and bee-mediated pollen dispersal upon plant spacing is a general phenomenon. We will show that bees are highly responsive to plant spacing and that bee-mediated pollen dispersal and associated gene dispersal is strongly correlated with plant spacing, the plant species and floral mechanism notwithstanding.

Ecological Constraints on the Establishment of a Novel Polyploid in Competition with Its Diploid Progenitor

Competition between a newly formed polyploid and one of its diploid parental species has been modeled. Models were based on the Lotka-Volterra competition model, to which were added terms representing the positive frequency-dependent effect (minority disadvantage) as a result of lowered fertility caused by the receipt of inappropriate pollen from the other cytotype. A new polyploid may persist by replacing its diploid parent as a result of the combination of a very small diploid population, the existence of an unstable equilibrium between the two cytotypes, and chance events (probably the most common route); by coexisting with it as the result of niche separation; or by outcompeting and replacing it (probably very rare). However, the conditions for all of these possibilities are quite restrictive. The model and results are applicable in some degree to the establishment of other novel cytotypes, and also to pairs of species that compete for resources and also experience minority disadvantage (perhaps because of competition for pollinators) with respect to each other.