Genetic Canalization Research Articles

A Dynamical Theory of Speciation on Holey Adaptive Landscapes.

A holey adaptive landscape is an adaptive landscape where relatively infrequent well-fit combinations of genes form a contiguous set that expands throughout the genotype space. I formulate and study a series of simple models describing the dynamics of speciation on holey adaptive landscapes driven by mutation and random genetic drift. Unlike most previous models that concentrate only on some stages of speciation, the models studied here describe the complete process of speciation from initiation until completion. The evolutionary factors included are selection (reproductive isolation), random genetic drift, mutation, recombination, and migration. In these models, pre- and postmating reproductive isolation is a consequence of cumulative genetic change. I study possibilities for speciation according to allopatric, parapatric, peripatric, and vicariance scenarios. The results presented here, together with earlier numerical simulations, strongly suggest that rapid speciation, including simultaneous emergence of several new species, is a plausible outcome of the evolutionary dynamics of subdivided populations. Rapid speciation is most likely for populations that are subdivided into a large number of small subpopulations. Speciation is possible even when subpopulations exchange several individuals per generation. Selection for local adaptation is not necessary for rapid speciation. I briefly discuss implications of the dynamics on holey adaptive landscapes for the nearly neutral theory of molecular evolution and for the theory of evolution of genetic canalization.

Redundant Gene Functions and Natural Selection

Redundant gene functions are ubiquitous, and they are a potentially important source of evolutionary innovations on the biochemical level. It is therefore highly desirable to understand the mechanisms governing their evolution. Gene duplication is clearly a prominent mechanism generating redundant genes. However, because redundancy provides a protective effect against deleterious mutations, natural selection might be involved in generating and maintaining partial redundancy. Although much experimental data on redundant genes has been accumulated, no data is available that could elucidate what role selection has in their evolution. As a first step towards answering this question, a conceptually simple mathematical model for the evolution of redundancy is introduced. Its main result is that selection can not only maintain, but also increase redundancy among genes in a population provided (i) that mutation generates sufficient variation in redundancy, and (ii) that populations are large. The population biological process at work is somewhat unusual. Selection does not act on the (nonexisting) differential fitness between individuals with different degrees of redundancy. Rather, it acts through the low number of offspring with deleterious mutations that individuals with redundant genes will generate. Moreover, even if populations are small and variation in redundancy is low, selection will substantially slow the ``decay'' of redundancy caused by mutation and genetic drift. Methodological problems in determining degrees of redundancy experimentally are discussed, as well as issues concerning the relation of redundancy to genetic canalization. The latter two phenomena necessitate a differentiated view of neutral mutations necessary, where some neutral mutations are only neutral because their effects on gene products are absorbed by the epigenetic system.

A Dynamical Theory of Speciation on Holey Adaptive Landscapes

A holey adaptive landscape is an adaptive landscape where relatively infrequent well‐fit combinations of genes form a contiguous set that expands throughout the genotype space. I formulate and study a series of simple models describing the dynamics of speciation on holey adaptive landscapes driven by mutation and random genetic drift. Unlike most previous models that concentrate only on some stages of speciation, the models studied here describe the complete process of speciation from initiation until completion. The evolutionary factors included are selection (reproductive isolation), random genetic drift, mutation, recombination, and migration. In these models, pre‐ and postmating reproductive isolation is a consequence of cumulative genetic change. I study possibilities for speciation according to allopatric, parapatric, peripatric, and vicariance scenarios. The results presented here, together with earlier numerical simulations, strongly suggest that rapid speciation, including simultaneous emergence of several new species, is a plausible outcome of the evolutionary dynamics of subdivided populations. Rapid speciation is most likely for populations that are subdivided into a large number of small subpopulations. Speciation is possible even when subpopulations exchange several individuals per generation. Selection for local adaptation is not necessary for rapid speciation. I briefly discuss implications of the dynamics on holey adaptive landscapes for the nearly neutral theory of molecular evolution and for the theory of evolution of genetic canalization.

A POPULATION GENETIC THEORY OF CANALIZATION.

Canalization is the suppression of phenotypic variation. Depending on the causes of phenotypic variation, one speaks either of genetic or environmental canalization. Genetic canalization describes insensitivity of a character to mutations, and the insensitivity to environmental factors is called environmental canalization. Genetic canalization is of interest because it influences the availability of heritable phenotypic variation to natural selection, and is thus potentially important in determining the pattern of phenotypic evolution. In this paper a number of population genetic models are considered of a quantitative character under stabilizing selection. The main purpose of this study is to define the population genetic conditions and constraints for the evolution of canalization. Environmental canalization is modeled as genotype specific environmental variance. It is shown that stabilizing selection favors genes that decrease environmental variance of quantitative characters. However, the theoretical limit of zero environmental variance has never been observed. Of the many ways to explain this fact, two are addressed by our model. It is shown that a "canalization limit" is reached if canalizing effects of mutations are correlated with direct effects on the same character. This canalization limit is predicted to be independent of the strength of stabilizing selection, which is inconsistent with recent experimental data (Sterns et al. 1995). The second model assumes that the canalizing genes have deleterious pleiotropic effects. If these deleterious effects are of the same magnitude as all the other mutations affecting fitness very strong stabilizing selection is required to allow the evolution of environmental canalization. Genetic canalization is modeled as an influence on the average effect of mutations at a locus of other genes. It is found that the selection for genetic canalization critically depends on the amount of genetic variation present in the population. The more genetic variation, the stronger the selection for canalizing effects. All factors that increase genetic variation favor the evolution of genetic canalization (large population size, high mutation rate, large number of genes). If genetic variation is maintained by mutation-selection balance, strong stabilizing selection can inhibit the evolution of genetic canalization. Strong stabilizing selection eliminates genetic variation to a level where selection for canalization does not work anymore. It is predicted that the most important characters (in terms of fitness) are not necessarily the most canalized ones, if they are under very strong stabilizing selection (k > 0.2Ve ). The rate of decrease of mutational variance Vm is found to be less than 10% of the initial Vm . From this result it is concluded that characters with typical mutational variances of about 10-3 Ve are in a metastable state where further evolution of genetic canalization is too slow to be of importance at a microevolutionary time scale. The implications for the explanation of macroevolutionary patterns are discussed.

Canalization: A molecular genetic perspective

The phenomenon of canalization--the genetic capacity to buffer developmental pathways against mutational or environmental perturbations--was first characterized in the late 1930s and early 1940s. Despite enormous subsequent progress in understanding the nature of the genetic material and the molecular basis of gene expression, there have been few attempts to interpret the classical work on canalization in molecular genetic terms. Some recent findings, however, bear on one form of canalization, 'genetic canalization', the stabilization of development against mutational effects. These data indicate that co-expressed paralogous genes can function as mutual 'back-up' elements in developmental processes. Paralogues, however, are far from the only basis of canalization: other genetic sources can be readily envisaged and some of these are described here. The evolutionary questions about genetic canalization and the mechanistic questions about developmental instability that still need to be addressed are also briefly discussed.

PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY.

The problem of complex adaptations is studied in two largely disconnected research traditions: evolutionary biology and evolutionary computer science. This paper summarizes the results from both areas and compares their implications. In evolutionary computer science it was found that the Darwinian process of mutation, recombination and selection is not universally effective in improving complex systems like computer programs or chip designs. For adaptation to occur, these systems must possess "evolvability," i.e., the ability of random variations to sometimes produce improvement. It was found that evolvability critically depends on the way genetic variation maps onto phenotypic variation, an issue known as the representation problem. The genotype-phenotype map determines the variability of characters, which is the propensity to vary. Variability needs to be distinguished from variations, which are the actually realized differences between individuals. The genotype-phenotype map is the common theme underlying such varied biological phenomena as genetic canalization, developmental constraints, biological versatility, developmental dissociability, and morphological integration. For evolutionary biology the representation problem has important implications: how is it that extant species acquired a genotype-phenotype map which allows improvement by mutation and selection? Is the genotype-phenotype map able to change in evolution? What are the selective forces, if any, that shape the genotype-phenotype map? We propose that the genotype-phenotype map can evolve by two main routes: epistatic mutations, or the creation of new genes. A common result for organismic design is modularity. By modularity we mean a genotype-phenotype map in which there are few pleiotropic effects among characters serving different functions, with pleiotropic effects falling mainly among characters that are part of a single functional complex. Such a design is expected to improve evolvability by limiting the interference between the adaptation of different functions. Several population genetic models are reviewed that are intended to explain the evolutionary origin of a modular design. While our current knowledge is insufficient to assess the plausibility of these models, they form the beginning of a framework for understanding the evolution of the genotype-phenotype map.

The differential genetic and environmental canalization of fitness components in Drosophila melanogaster

AbstractCanalization describes the process by which phenotypic variation is reduced by developmental mechanisms. A trait can be canalized against environmental or genetic perturbations. Stabilizing selelction should favor improved canalization, and the degree of a trait's canalization should be positively correlated with its impact on fitness. Here we report, for Drosophila melanogaster, measurements of environmental canalization for five fitness components. We compare them with measurements of genetic canalization, and we discuss the impact of inbreeding on both. In three experiments we measured the variation of fitness components within lines nested within temperature, treatment, and experiment. Lines differed in the position of a P element insert or in genetic background. Within lines flies were genetically nearly identical. We designated trait variation within lines as environmental canalization. The canalization of the traits increased with their impact on fitness, and the pattern was similar to that found for the canalization of fitness components against genetic differences, measured as the variation among lines nested within temperature, treatment, and experiment. This suggests that developmental mechanisms buffer the phenotype against both genetic and environmental disturbance. The results also suggest, less strongly, that inbreeding weakens canalization.

FITNESS SENSITIVITY AND THE CANALIZATION OF LIFE-HISTORY TRAITS.

Canalization is an abstract term that describes unknown developmental mechanisms that reduce phenotypic variation. A trait can be canalized against environmental perturbations (e.g., changes in temperature or nutrient quality), or genetic perturbations (e.g., mutations or recombination); this paper is about genetic canalization. Stabilizing selection should improve the canalization of traits, and the degree of canalization should be positively correlated with the traits' impact on fitness. Experiments testing this idea should measure the canalization of a series of traits whose impact on fitness is known or can be inferred, exclude differences among traits in the number of loci and alleles segregating as an explanation for the pattern of variability found, and distinguish between canalization against genetic and environmental variation. These conditions were met by three experiments within which the variation of fitness components among Drosophila melanogaster lines was measured and among which the genetic contribution to the variation among lines was clearly different. The canalization of the traits increased with their impact on fitness and did not depend on the degree of genetic differences among lines. That the flies used had been transformed by a P-element insert suggests that canalization was also effective against novel genetic variation. The results reported here cannot be explained by the classical hypothesis of reduction in the number of loci segregating for traits with greater impact on fitness and confirm that traits with greater impact on fitness are more strongly canalized. This pattern of canalization reveals an underappreciated role for development in microevolution. There is differential genetic canalization of fitness components in D. melanogaster.

Adaptive Phenotypic Plasticity: Target or By-Product of Selection in a Variable Environment?

Adaptive Phenotypic Plasticity: Target or By-Product of Selection in a Variable Environment?

Early approach preferences of patterns and colours in quail: responses to artificial selection and imprinting

Abstract. Japanese quail, Coturnix coturnix japonica, were bidirectionally selected for early approach preferences between two achromatic patterns and two coloured stimuli. The pattern preference lines responded to selection by less robust and more asymmetrical progression than the colour preference lines, but F 2 segregation suggested relatively simple genetic influences in both selection studies. Selection effects were partially transferred across the two stimulus modalities. While imprinting to colours modified colour preferences in subjects from each genetic line of each study, imprinting to patterns did not modify pattern preferences in any of the lines. This was true regardless of the type and magnitude of selected preferences. Discussion focuses on the uses of these preparations in modelling the neural representation of stimulus information, and on the processes of genotype-environment interaction and genetic canalization of behavioural development.

Perceptual Imprinting: Stimulus Preferences, Age Effects, and Genetic Canalization

AbstractThe separate and interactive influences of genetically variable unconditional stimulus preference, age effects, and genetic canalization were studied in relation to perceptual imprinting in Japanese quail chicks (C. coturnix japonica). The chicks were drawn from populations subjected to 21 generations of bidirectional genetic selection for unconditional approach preference between blue and red stimuli. They were tested for age and stimulus effects in perceptual learning from synergistic and conflicting exposures to the genetically preferred and genetically unpreferred colours. Unselected quail chicks were tested as genetic controls, and the qualitative influences of exposures to colours were controlled by comparable exposures to white and other preference-wise neutral stimuli. The results indicate robust and developmentally stable gene effects in the quail's unconditional colour choices, developmentally persistent but episodically variable learning from exposures to colours of genetically variable preference values, and systematic genotype-environment interactions. Discussion focuses on the canalizing role of genetically variable unconditional stimulus preferences in the early developmental of behaviour.

Gene-culture coevolution of complex social behavior: human altruism and mate choice.

The hypothesis is examined that genes bias the development of complex social behavior in one direction over alternatives. Studies of altruism and political attitudes in twins estimate that approximately 50% of the variance is associated with direct genetic inheritance, virtually 0% with the twin's common family environment, and the remainder with each twin's specific environment. Studies of human marriages show that spouses choose each other on the basis of similarity, assorting on the most genetically influenced of a set of homogeneous attributes. These data imply a genetic canalization of social influences such that, within the constraints allowed by the total spectrum of cultural alternatives, people create environments maximally compatible with their genotypes.

The Whitehead Institute Symposium on Forces Molding the Genome

I. Many believe that sooner or later molecular biology will mechanistically provide the precise genotypic basis for phenotypic change. This in turn will provide the basis for attacking several major evolutionary problems posed by paleontology, including the following: —There are approximately 30 phylum-level taxa in the animal kingdom, and yet in the “fast” version of evolutionary history, many of then arose 600 Myr ago in a very short period of time (of order <30 Myr). In terms of basic body plan and inferred ecology, these sponges, clams, arthropods, etc. were seemingly as different then as they are now. It is as though the rate of morphologic change was much more rapid during that interval than during the nearly 600 Myr since then. Even the “slow” version of evolutionary history (which allows for an additional unfossilized record of about 500 Myr) demands an answer to what has controlled the development of major evolutionary Bauplans.—Some morphologic traits (though probably not individual species) persist for immense periods of geologic time—the general shape of the horseshoe crab, for example, or the bristle patterns of taxa of meiofaunal “worms” living among sand grains. What is the developmental rationale for these persistent traits? In short, what is the molecular basis for genetic and morphologic canalization?—The general pattern of species specialization proceeds unabated overtime, but every once in a while the developmental clock is reset. Organisms which are sexually mature but with simplified or “primitive” morphology arise de novo, and these lineages then form the stock of unspecialized forms from which future specializations evolve. What is the molecular basis for resetting the developmental clock?—Reproductive isolation may arise “accidentally” through genomic changes unrelated to changes in the local environment. To the extent this is true, speciation has a largely accidental component. Knowledge of the rate and type of genomic change is critical for an evaluation of this idea.