QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. I. RATE TESTS FOR RANDOM CHANGE VERSUS SELECTION IN DIFFERENTIATION OF LIVING SPECIES

The possible roles of random genetic change and natural selection in bryozoan speciation were analyzed using quantitative genetic methods on breeding data for traits of skeletal morphology in two closely related species of the cheilostome Stylopoma. The hypothesis that morphologic differences between the species are caused entirely by mutation and genetic drift could not be rejected for reasonable rates of mutation maintained for as few as 10³ to 10⁴ generations. Divergence times this short or shorter are consistent with the abrupt appearances of many invertebrate species in the fossil record, commonly followed by millions of years of morphologic stasis. To produce these differences over 10³ generations or fewer, directional selection acting alone would require unrealistically high levels of minimum selective mortality throughout divergence. Thus, selection is unnecessary to explain the divergence of these species, except as a means of accelerating the effects of random genetic change on shorter time scales (directional selection), or decelerating them over longer ones (stabilizing selection). These results are consistent with a variety of models of phenotypic evolution involving random shifts between multiple adaptive peaks. Similar results were obtained by substituting trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance in place of the values based on breeding data. Quantitative genetic analysis of speciation in fossil bryozoan lineages is thus justified.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. II. ANALYSIS OF SELECTION AND RANDOM CHANGE IN FOSSIL SPECIES USING RECONSTRUCTED GENETIC PARAMETERS

The roles of natural selection and random genetic change in the punctuated phenotypic evolution of eight Miocene-Pliocene tropical American species of the cheilostome bryozoan Metrarabdotos are analyzed by quantitative genetic methods. Trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance are similar to those previously obtained for living species of the cheilostome Stylopoma using breeding data. The hypothesis that differences in skeletal morphology between species of Metrarabdotos are entirely due to mutation and genetic drift cannot be rejected for reasonable rates of mutation maintained for periods brief enough to account for the geologically abrupt appearances of these species in the fossil record. Except for one pair of species, separated by the largest morphologic distance, directional selection acting alone would require unrealistically high rates of selective mortality to be maintained for these periods. Thus, directional selection is not strongly implicated in the divergence of Metrarabdotos species. Within species, rates of net phenotypic change are slow enough to require stabilizing selection, but mask large, relatively rapid fluctuations, all of which, however, can be attributed to chance departures from the mean phenotype by mutation and genetic drift, rather than to tracking environmental fluctuation by directional selection. The results are consistent with genetic models involving shifts between multiple adaptive peaks on which phenotypes remain more or less static through long-term stabilizing selection. Regardless of the degree to which directional selection may be involved in peak shifts, phenotypic differentiation is thus related to processes different than the pervasive stabilizing selection acting within species.     

THE GENETICS OF PHENOTYPIC PLASTICITY. VIII. THE COST OF PLASTICITY IN DAPHNIA PULEX

In a heterogeneous world, the optimal strategy for an individual is to continually change its phenotype to match the optimal type. However, in the real world, organisms do not behave in this fashion. One potential reason why is that phenotypic plasticity is costly. We measured production and maintenance costs of plasticity in the freshwater crustacean Daphnia pulex (Cladocera: Crustacea) in response to the presence of chemical signals from a predator, the insect Chaoborus americanus. We looked at three changes in juvenile body size and shape: body length, body depth, and tailspine length. Fitness costs were measured as changes in adult growth and fecundity, and summarized as the intrinsic rate of increase (r) for individuals reared in the presence or absence of Chaoborus extract. The cost of plasticity was measured as a multiple regression of mean clone fitness against trait and trait plasticity. We found scant evidence for either production or maintenance costs of plasticity. We also failed to find direct costs of these juvenile structures, which is surprising, as others have found such costs. We attribute the lack of measurable direct or plasticity costs to a decrease in metabolic rates in the presence of the Chaoborus extract. This decrease in metabolic rate may have compensated for any cost increases. We call for more extensive measures of the costs of plasticity, especially under natural conditions, and the incorporation of costs into evolutionary models.     

PHENOTYPIC PLASTICITY IN POLYGONUM PERSICARIA. II. NORMS OF REACTION TO SOIL MOISTURE AND THE MAINTENANCE OF GENETIC DIVERSITY

Adaptive phenotypic plasticity is the predicted evolutionary response to fine-grained fluctuation in major environmental factors, such as soil moisture in plant habitats. This study examines genotypes from two natural populations of Polygonum persicaria, one from a relatively homogeneous, moderately moist site, and one from a site in which severe drought and root flooding occur within single growth seasons. Norms of reaction (phenotypic response curves) were determined for a random sample of eight and ten cloned genotypes, respectively, from each of the populations over a controlled moisture gradient ranging from drought to flooding.     

THE MIXED-MODEL ANALYSIS OF VARIANCE APPLIED TO QUANTITATIVE GENETICS: BIOLOGICAL MEANING OF THE PARAMETERS

The mixed-model factorial analysis of variance has been used in many recent studies in evolutionary quantitative genetics. Two competing formulations of the mixed-model ANOVA are commonly used, the “Scheffe” model and the “SAS” model; these models differ in both their assumptions and in the way in which variance components due to the main effect of random factors are defined. The biological meanings of the two variance component definitions have often been unappreciated, however. A full understanding of these meanings leads to the conclusion that the mixed-model ANOVA could have been used to much greater effect by many recent authors. The variance component due to the random main effect under the two-way SAS model is the covariance in true means associated with a level of the random factor (e.g., families) across levels of the fixed factor (e.g., environments). Therefore the SAS model has a natural application for estimating the genetic correlation between a character expressed in different environments and testing whether it differs from zero. The variance component due to the random main effect under the two-way Scheffe model is the variance in marginal means (i.e., means over levels of the fixed factor) among levels of the random factor. Therefore the Scheffe model has a natural application for estimating genetic variances and heritabilities in populations using a defined mixture of environments. Procedures and assumptions necessary for these applications of the models are discussed. While exact significance tests under the SAS model require balanced data and the assumptions that family effects are normally distributed with equal variances in the different environments, the model can be useful even when these conditions are not met (e.g., for providing an unbiased estimate of the across-environment genetic covariance). Contrary to statements in a recent paper, exact significance tests regarding the variance in marginal means as well as unbiased estimates can be readily obtained from unbalanced designs with no restrictive assumptions about the distributions or variance-covariance structure of family effects.     

GENETIC VARIATION AND POLYMORPHISM IN THE INDUCIBLE SPINES OF A MARINE BRYOZOAN

Of particular value in understanding the evolution of genotypes with broad phenotypic ranges (phenotypic plasticity) are the few examples of organisms with adaptive plasticity, such as those that develop a defensive morphology in response to cues from predators. We know little about the heritability of inducible defensive characters or the range of phenotypes available for selection to act on in the field. Membranipora membranacea is a colonial marine bryozoan that produces spines within two days of exposure to waterborne predator extracts. Surveys done in 1993 and 1995 showed that the population at Friday Harbor Labs, Washington, was polymorphic for inducible spine type and was composed of a constitutively spined type that produced spines in the absence of a predator stimulus, an unspined phenotype that did not produce spines irrespective of a stimulus, and an inducibly spined phenotype that would produce spines if exposed to the appropriate cue. In 1995, the frequencies of these types were determined through a laboratory common-garden experiment; 178 colonies were cultured from metamorphosis through approximately 30 days and then exposed to the cue. The inducible type was the dominant, comprising 80.3% of the population. The constitutive type made up 6.2% of the population, and the remaining 13.4 % was the unspined type. The frequency of the three types was similar to a preliminary trial of the experiment run in 1993. Experiments also showed that the lengths of the spines of the inducible type varied continuously among genotypes. To assess causes of variation in the inducible spine response and its clonal heritability, 16 clones were subdivided and grown in a common environment and exposed to a single dosage of spine inducing substance (SIS). Spine length showed high clonal heritability. The range of colony responses from a single environment varied from relatively unresponsive to highly responsive colonies with a very low threshold of response. Norms of reaction were quantified for spine lengths of inducible genotypes originating from two field environments by testing them in a concentration series of SIS. Both spine length and spine type varied with concentration of inducer. Within a clone, colonies were more likely to produce membranous spines than corner spines at higher concentrations. At low concentrations, only straight spines were produced. This study showed that populations of M. membranacea at Friday Harbor are a mix of inducible, nonspined and constitutively spined individuals. Even the inducible individuals showed high heritable variation in the length of spine activated, suggesting that there is considerable scope for the evolution of this character. A norm-of-reaction experiment further showed that the type of spine produced, membranous or corner, varied with the concentration of the cue. Factors maintaining the polymorphism and the broad range of genotypes could include high costs of defending the spined types coupled with a shifting biotic regime.     

PHENOTYPIC PLASTICITY IN POLYGONUM PERSICARIA. III. THE EVOLUTION OF ECOLOGICAL BREADTH FOR NUTRIENT ENVIRONMENT

Norms of reaction for a number of growth and reproductive characters were determined for 15 randomly sampled Polygonum persicaria genotypes, from two natural populations originating in sites with very different nutrient availabilities. Under severely limiting nutrient conditions, these genotypes shared not only plastic responses such as increased root-to-shoot ratio, but a surprising constancy in such functionally essential characters as leaf area ratio, leaf nitrogen concentration, and propagule nitrogen content. Because functional homeostasis depends on flexibility in underlying characters, similar homeostatic results can be achieved through different combinations of underlying plastic and fixed responses in genetically different entities. For example, plants in each population maintained a relatively constant propagule nitrogen content under extreme low-nitrogen conditions by varying either the size or the tissue nitrogen concentration of propagules. These genotypes also tolerated excessive nutrient levels toxic to many plants, evidently by storing excess nutrients in shoots. Although development was altered under such circumstances, reproductive fitness was maintained.     

GENOTYPE-ENVIRONMENT INTERACTION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY

Studies of spatial variation in the environment have primarily focused on how genetic variation can be maintained. Many one-locus genetic models have addressed this issue, but, for several reasons, these models are not directly applicable to quantitative (polygenic) traits. One reason is that for continuously varying characters, the evolution of the mean phenotype expressed in different environments (the norm of reaction) is also of interest. Our quantitative genetic models describe the evolution of phenotypic response to the environment, also known as phenotypic plasticity (Gause, 1947), and illustrate how the norm of reaction (Schmalhausen, 1949) can be shaped by selection. These models utilize the statistical relationship which exists between genotype-environment interaction and genetic correlation to describe evolution of the mean phenotype under soft and hard selection in coarse-grained environments. Just as genetic correlations among characters within a single environment can constrain the response to simultaneous selection, so can a genetic correlation between states of a character which are expressed in two environments. Unless the genetic correlation across environments is ± 1, polygenic variation is exhausted, or there is a cost to plasticity, panmictic populations under a bivariate fitness function will eventually attain the optimum mean phenotype for a given character in each environment. However, very high positive or negative correlations can substantially slow the rate of evolution and may produce temporary maladaptation in one environment before the optimum joint phenotype is finally attained. Evolutionary trajectories under hard and soft selection can differ: in hard selection, the environments with the highest initial mean fitness contribute most individuals to the mating pool. In both hard and soft selection, evolution toward the optimum in a rare environment is much slower than it is in a common one. A subdivided population model reveals that migration restriction can facilitate local adaptation. However, unless there is no migration or one of the special cases discussed for panmictic populations holds, no geographical variation in the norm of reaction will be maintained at equilibrium. Implications of these results for the interpretation of spatial patterns of phenotypic variation in natural populations are discussed.     

PRELIMINARY ANALYSIS OF QUANTITATIVE GENETICS AND PHENOTYPIC PLASTICITY IN AULACOSEIRA SUBARCTICA (BACILLAR-IOPHYTA)

Several clones of Aulacoseira subarctica were isolated from Yellowstone, Lewis, and East Rosebud Lakes (Montana, Wyoming). Two to four clones from each lake were grown in batch cultures under three light intensities, 2, 11.4 and 115 μE m⁻² s⁻¹. Clones were conditioned to their light environment for a three-week period. Inoculants from the conditioned clones taken during log phase of growth, were grown until in log phase, then samples were collected. Five randomly chosen valves for 2 replicates of each clone were examined using a scanning electron microscope and captured on film at a magnification of 20,000x. Each image was digitized and quantitative morphometric characters were measured. A preliminary quantitative genetic analysis was performed on selected characters within each light environment. Plasticity of characters within clones across the three light regimes were also examined. The amount of variability found within characters in A. subarctica will be discussed in terms of environmental, genetic, and microenvironmental sources.     

QUANTITATIVE GENETIC MODELS FOR DEVELOPMENT,EPIGENETIC SELECTION,AND PHENOTYPIC EVOLUTION

Herein we describe a general multivariate quantitative genetic model that incorporates two potentially important developmental phenomena, maternal effects and epigenetic effects. Maternal and epigenetic effects are defined as partial regression coefficients and phenotypic variances are derived in terms of age-specific genetic and environmental variances. As a starting point, the traditional quantitative genetic model of additive gene effects and random environmental effects is cast in a developmental time framework. From this framework, we first extend a maternal effects model to include multiple developmental ages for the occurrence of maternal effects. An example of maternal effects occurring at multiple developmental ages is prenatal and postnatal maternal effects in mammals. Subsequently, a model of intrinsic and epigenetic effects in the absence of maternal effects is described. It is shown that genetic correlations can arise through epigenetic effects, and in the absence of other developmental effects, epigenetic effects are in general confounded with age-specific intrinsic genetic effects. Finally, the two effects are incorporated into the basic quantitative genetic model. For this more biologically realistic model combining maternal and epigenetic effects, it is shown that the phenotypic regressions of offspring on mother and offspring on father can be used in some cases to estimate simultaneously maternal effects and epigenetic effects.     

GENETIC VARIATION FOR PHENOTYPIC PLASTICITY IN THE LARVAL LIFE HISTORY OF SPADEFOOT TOADS (SCAPHIOPUS COUCHII)

Phenotypic plasticity in life-history traits is common. The relationship between phenotype and environment, or reaction norm, associated with life-history plasticity can evolve by natural selection if there is genetic variation within a population for the reaction norm and if the traits involved affect fitness. As with other traits, selection on plasticity in a particular trait or in response to a particular environmental factor may be constrained by trade-offs with other traits that affect fitness. In this paper, I experimentally evaluated broad-sense genetic variation in the reaction norms of age and size at metamorphosis in response to two environmental factors, food level and temperature. Differences among full-sib families in one or both traits were evident in all treatments. However, variation among families in their responses to each treatment (genotype-environment interaction) resulted in variation among treatments in estimated heritabilities and genetic correlations. Age at metamorphosis was equally sensitive to temperature in all families, but size at metamorphosis was more sensitive to temperature in some families than in others. Size at metamorphosis was equally sensitive to food level in all families, but age at metamorphosis was sensitive to food in some families but not in others. At high temperature or low food, the genetic correlation between age and size at metamorphosis was positive, generating a potential trade-off between metamorphosing early to attain higher larval survival and metamorphosing later to achieve larger size. This trade-off extends across treatments: families with the largest average size at metamorphosis achieved larger size with the longest average and greatest plasticity in age at metamorphosis. Other families achieved shorter average larval periods by exhibiting greater plasticity in size at metamorphosis but had the smallest average size at metamorphosis. This trade-off may reflect an underlying functional constraint on the ability to respond optimally to all environments, resulting in persistent genetic variation in reaction norms.     

QUANTITATIVE GENETICS AND THE EVOLUTION OF REACTION NORMS

We extend methods of quantitative genetics to studies of the evolution of reaction norms defined over continuous environments. Our models consider both spatial variation (hard and soft selection) and temporal variation (within a generation and between generations). These different forms of environmental variation can produce different evolutionary trajectories even when they favor the same optimal reaction norm. When genetic constraints limit the types of evolutionary changes available to a reaction norm, different forms of environmental variation can also produce different evolutionary equilibria. The methods and models presented here provide a framework in which empiricists may determine whether a reaction norm is optimal and, if it is not, to evaluate hypotheses for why it is not.     

DEVELOPMENTAL QUANTITATIVE GENETICS AND THE EVOLUTION OF ONTOGENIES

A model is presented which permits integration of developmental information into genetic discussions about evolutionary change in morphology. Development of a trait is described in terms of an ontogenetic trajectory whose properties are defined by a small number of parameters. Some evolutionary aspects of development are examined from the perspective of this quantitative genetic model. Particular attention is given to the developmental origin of pleiotropic effects, developmental constraints, heterochrony, and the growth and morphogenesis of complex morphologies. The role of genetic maternal effects in mammalian development is briefly examined, particularly as it relates to selection on developmental traits.     

PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION

The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation.     

THE QUANTITATIVE GENETICS OF SEXUAL DIMORPHISM IN SILENE LATIFOLIA (CARYOPHYLLACEAE). I. GENETIC VARIATION

It is widely recognized that there are basic conflicts between the resource needs of a plant for paternal versus maternal functions. In dioecious species, these divergent demands, and the selection pressures they impose, can lead to the evolution of sexual dimorphism. The present study was conducted to assess the potential for the evolution of sexual dimorphism in Silene latifolia by evaluating the genetic variation and genetic correlation between characters and between the sexes for a range of growth and reproductive characters. Sexual dimorphism is largely restricted to reproductive characters, particularly flower number and flower size. A canonical correlation analysis revealed considerable intercorrelation between growth characters, such as germination date, height, and leaf size, and reproductive characters; plants that grow fast early on also flower earlier, and plants that produce big leaves also produce big flowers. There was genetic variation for several sexually dimorphic characters; much of the focus in this analysis was on flower size, particularly calyx diameter. Finally, genetic correlations within and between the sexes were found that limit the rate of evolutionary divergence between the sexes. The genetic results suggest that S. latifolia has been subject to divergent selection on the two sexes for a long period of time, bringing about a gradual fixation of sex-limited gene effects, so that the remaining genetic effects are expressed in both sexes. Genetic correlations between the sexes that arise from this residual variation impose limits on further evolutionary change.     

THE ECOLOGY AND GENETICS OF FITNESS IN CHLAMYDOMONAS III. GENOTYPE-BY-ENVIRONMENT INTERACTION WITHIN STRAINS

The fitness of genotypes created by crossing strains of Chlamydomonas reinhardtii was measured in axenic pure culture in a set of chemically defined environments. There was substantial and highly significant genotype-by-environment interaction, with genetic correlations between environments averaging only about +0.1 for both r and K. Higher-order interactions with combinations of environmental factors appeared to be no less important than simple interactions with single factors. The importance of genotype-by-environment interaction increased with the number of environmental factors manipulated. The linear reaction norms of genotypic score on environmental mean score varied substantially among genotypes and often intersected. There was also some evidence that nonallelic genetic interactions were present, and varied among environments. The genetic correlation of r with K also varied among environments, being significantly negative in some but not in others. These results are similar in all important respects to those previously obtained with different species, and suggest that genotype-by-environment interaction is important at all genetic scales. It is argued that they provide empirical support for a general theory of diversity, the “Tangled Bank,” based on the different response of genotypes to the range of conditions found in heterogeneous natural environments.     

LOCAL ADAPTATION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN TRINIDADIAN GUPPIES (POECILIA RETICULATA)

Divergent selection pressures across environments can result in phenotypic differentiation that is due to local adaptation, phenotypic plasticity, or both. Trinidadian guppies exhibit local adaptation to the presence or absence of predators, but the degree to which predator‐induced plasticity contributes to population differentiation is less clear. We conducted common garden experiments on guppies obtained from two drainages containing populations adapted to high‐ and low‐predation environments. We reared full‐siblings from all populations in treatments simulating the presumed ancestral (predator cues present) and derived (predator cues absent) conditions and measured water column use, head morphology, and size at maturity. When reared in presence of predator cues, all populations had phenotypes that were typical of a high‐predation ecotype. However, when reared in the absence of predator cues, guppies from high‐ and low‐predation regimes differed in head morphology and size at maturity; the qualitative nature of these differences corresponded to those that characterize adaptive phenotypes in high‐ versus low‐predation environments. Thus, divergence in plasticity is due to phenotypic differences between high‐ and low‐predation populations when reared in the absence of predator cues. These results suggest that plasticity might initially play an important role during colonization of novel environments, and then evolve as a by‐product of adaptation to the derived environment.