Neophenogenesis: a developmental theory of phenotypic evolution

An important task for evolutionary biology is to explain how phenotypes change over evolutionary time. Neo-Darwinian theory explains phenotypic change as the outcome of genetic change brought about by natural selection. In the neo-Darwinian account, genetic change is primary; phenotypic change is a secondary outcome that is often given no explicit consideration at all. In this article, we introduce the concept of neophenogenesis: a persistent, transgenerational change in phenotypes over evolutionary time. A theory of neophenogenesis must encompass all sources of such phenotypic change, not just genetic ones. Both genetic and extra-genetic contributions to neophenogenesis have their effect through the mechanisms of development, and developmental considerations, particularly a rejection of the commonly held distinction between inherited and acquired traits, occupy a central place in neophenogenetic theory. New phenotypes arise because of a change in the patterns of organism-environment interaction that produce development in members of a population. So long as these new patterns of developmental interaction persist, the new phenotype(s) will also persist. Although the developmental mechanisms that produce the novel phenotype may change, as in the process known as "genetic assimilation", such changes are not necessary in order for neophenogenesis to occur, because neophenogenetic theory is a theory of phenotypic, not genetic, change.     

Genetic analysis of life-history constraint and evolution in a wild ungulate population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.     

Evolution of adaptive phenotypic variation patterns by direct selection for evolvability

A basic assumption of the Darwinian theory of evolution is that heritable variation arises randomly. In this context, randomness means that mutations arise irrespective of the current adaptive needs imposed by the environment. It is broadly accepted, however, that phenotypic variation is not uniformly distributed among phenotypic traits, some traits tend to covary, while others vary independently, and again others barely vary at all. Furthermore, it is well established that patterns of trait variation differ among species. Specifically, traits that serve different functions tend to be less correlated, as for instance forelimbs and hind limbs in bats and humans, compared with the limbs of quadrupedal mammals. Recently, a novel class of genetic elements has been identified in mouse gene-mapping studies that modify correlations among quantitative traits. These loci are called relationship loci, or relationship Quantitative Trait Loci (rQTL), and affect trait correlations by changing the expression of the existing genetic variation through gene interaction. Here, we present a population genetic model of how natural selection acts on rQTL. Contrary to the usual neo-Darwinian theory, in this model, new heritable phenotypic variation is produced along the selected dimension in response to directional selection. The results predict that selection on rQTL leads to higher correlations among traits that are simultaneously under directional selection. On the other hand, traits that are not simultaneously under directional selection are predicted to evolve lower correlations. These results and the previously demonstrated existence of rQTL variation, show a mechanism by which natural selection can directly enhance the evolvability of complex organisms along lines of adaptive change.     

Selective and genetic constraints on the evolution of body size in a stream-dwelling salmonid fish

To examine constraints on evolution of larger body size in two stunted populations of brook charr (Salvelinus fontinalis) from a single river in Cape Race, Newfoundland, Canada, we measured viability selection acting on length-at-age traits, and estimated quantitative genetic parameters in situ (following reconstruction of pedigree information from microsatellite data). Furthermore we tested for phenotypic differentiation between the populations, and for association of high juvenile growth with early maturity that is predicted by life history theory. Within each population, selection differentials and estimates of heritabilities for length-at-age traits suggested that evolution of larger size is prevented by both selective and genetic constraints. Between the populations, phenotypic differentiation was found in length-at-age and age of maturation traits, whereas early maturation was associated with increased juvenile growth (relative to adult growth) both within and between populations. The results suggest an adaptive plastic response in age of maturation to juvenile growth rates that have a largely environmental basis of determination.     

Migration-induced phenotypic divergence: the migration-selection balance of correlated traits

Genetically correlated traits are known to respond to indirect selection pressures caused by directional selection on other traits. It is however unclear how local adaptation in populations diverging along some phenotypic traits but not others is affected by the joint action of gene flow and genetic correlations among traits. This simulation study shows that although gene flow is a potent constraining mechanism of population adaptive divergence, it may induce phenotypic divergence in traits under homogeneous selection among habitats if they are genetically correlated with traits under divergent selection. This correlated phenotypic divergence is a nonmonotonous function of migration and increases with mutational correlation among traits. It also increases with the number of divergently selected traits provided their genetic autonomy relative to the uniformly selected trait is reduced by specific patterns of genetic covariances: populations with lower effective trait dimensionality are more likely to generate very large correlated divergence. The correlated divergence is likely to be picked up by Q(ST)-F(ST) analysis of population genetic differentiation and be erroneously ascribed to adaptive divergence under divergent selection. This study emphasizes the necessity to understand the interaction between selection and the genetic basis of adaptation in a multivariate rather than univariate context.     

Maize selection passes the century mark: a unique resource for 21st century genomics

The Illinois Long-Term Selection Experiment for grain protein and oil concentration in maize (Zea mays) is the longest continuous genetics experiment in higher plants. A total of 103 cycles of selection have produced nine related populations that exhibit phenotypic extremes for grain composition and a host of correlated traits. The use of functional genomics tools in this unique genetic resource provides exciting opportunities not only to discover the genes that contribute to phenotypic differences but also to investigate issues such as the response of plant genomes to artificial selection, the genetic architecture of quantitative traits and the source of continued genetic variation within domesticated crop genomes.     

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.     

A test for selection employing quantitative trait locus and mutation accumulation data

Evolutionary biologists attribute much of the phenotypic diversity observed in nature to the action of natural selection. However, for many phenotypic traits, especially quantitative phenotypic traits, it has been challenging to test for the historical action of selection. An important challenge for biologists studying quantitative traits, therefore, is to distinguish between traits that have evolved under the influence of strong selection and those that have evolved neutrally. Most existing tests for selection employ molecular data, but selection also leaves a mark on the genetic architecture underlying a trait. In particular, the distribution of quantitative trait locus (QTL) effect sizes and the distribution of mutational effects together provide information regarding the history of selection. Despite the increasing availability of QTL and mutation accumulation data, such data have not yet been effectively exploited for this purpose. We present a model of the evolution of QTL and employ it to formulate a test for historical selection. To provide a baseline for neutral evolution of the trait, we estimate the distribution of mutational effects from mutation accumulation experiments. We then apply a maximum-likelihood-based method of inference to estimate the range of selection strengths under which such a distribution of mutations could generate the observed QTL. Our test thus represents the first integration of population genetic theory and QTL data to measure the historical influence of selection.     

Evolution of the environmental component of the phenotypic variance: stabilizing selection in changing environments and the cost of homogeneity

Quantitative traits show abundant genetic, environmental, and phenotypic variance, yet if they are subject to stabilizing selection for an optimal phenotype, both the genetic and environmental components are expected to decline. The mechanisms that determine the level and maintenance of phenotypic variance are not yet fully understood. While there has been extensive study of mechanisms maintaining genetic variability, it has generally been assumed that environmental variance is not dependent on the genotype and therefore not subject to change. However, accumulating data suggest that the environmental variance is under some degree of genetic control. In this study, it is assumed accordingly that both the genotypic value (i.e., mean phenotypic value) and the variance of phenotypic value given genotypic value depend on the genotype. Two models are investigated as potentially able to explain the protected maintenance of environmental variance of quantitative traits under stabilizing selection. One is varying environment among generations, such that both the optimal phenotype and the strength of the stabilizing selection vary between generations. The other is the cost of homogeneity, which is based on an assumption of an engineering cost of minimizing variability in development. It is shown that a small homogeneity cost is enough to maintain the observed levels of environmental variance, whereas a large amount of temporal variation in the optimal phenotype and the strength of selection would be necessary.     

家蚕二化性杂交品种部分数量性状遗传参数的初步评估

采用完全随机设计法根据10头老熟幼虫体重、全茧重、茧层量、茧层率（%）、存活率、万蚕茧层量和茧丝长等指标,对两对二化性家蚕Bombyx mori L. 杂交品系（SH6×NB₄D₂和CSR₂×CSR₄）杂交一代的22个子代个体进行了遗传参数估算,以缩小优质蚕品种的候选范围,并且计算出直接筛选的参数,如遗传力和遗传进度等,使这些信息可用于以筛选高产新品种为目的的育种和选择过程中。杂交子代2, 4, 5, 6, 7, 10, 14, 16, 19和20号个体在这几个指标中表现出显著的优越性。全茧重、万蚕茧层量和茧丝长的遗传力和遗传进度较大,可以简单地从表现型的差异对这些性状进行选择并取得遗传性状改良。其他几个指标(10头老熟幼虫体重、茧层量、茧层率(%)和存活率)的遗传力和遗传进度较低,对这些性状进行直接选择来改良品种的效果较差。     

Artificial selection on phenotypically plastic traits

Many phenotypes respond physiologically or developmentally to continuously distributed environmental variables such as temperature and nutritional quality. Information about phenotypic plasticity can be used to improve the efficiency of artificial selection. Here we show that the quantitative genetic theory for 'infinite-dimensional' traits such as reaction norms provides a natural framework to accomplish this goal. It is expected to improve selection responses by making more efficient use of information about environmental effects than do conventional methods. The approach is illustrated by deriving an index for mass selection of a phenotypically plastic trait. We suggest that the same approach could be extended directly to more general and efficient breeding schemes, such as those based on general best linear unbiased prediction. Methods for estimating genetic covariance functions are reviewed.     

Competition can maintain genetic but not environmental variance in the presence of stabilizing selection

A population in which there is stabilizing selection acting on quantitative traits toward an intermediate optimum becomes monomorphic in the absence of mutation. Further, genotypes that show least environmental variation are also favored, such that selection is likely to reduce both genetic and environmental components of phenotypic variance. In contrast, intraspecific competition for resources is more severe between phenotypically similar individuals, such that those deviating from prevailing phenotypes have a selective advantage. It has been shown previously that polymorphism and phenotypic variance can be maintained if competition between individuals is "effectively" stronger than stabilizing selection. Environmental variance is generally observed in quantitative traits, so mechanisms to explain its maintenance are sought, but the impact of competition on its magnitude has not previously been studied. Here we assume that a quantitative trait is subject to selection for an optimal value and to selection due to competition. Further, we assume that both the mean and variance of the phenotypic value depend on genotype, such that both may be affected by selection. Theoretical analysis and numerical simulations reveal that environmental variance can be maintained only when the genetic variance (in mean phenotypic value) is constrained to a very low level. Environmental variance will be replaced entirely by genotypic variance if a range of genotypes that vary widely in mean phenotype are present or become so by mutation. The distribution of mean phenotypic values is discrete when competition is strong relative to stabilizing selection; but more genotypes segregate and the distribution can approach continuity as competition becomes extremely strong. If the magnitude of the environmental variance is not under genetic control, there is a complementary relationship between the levels of environmental and genetic variance such that the level of phenotypic variance is little affected.     

A test for the genetic basis of natural selection: an individual-based longitudinal study in a stream-dwelling fish

In addition to the well-studied evolutionary parameters of (1) phenotype-fitness covariance and (2) the genetic basis of phenotypic variation, adaptive evolution by natural selection requires that (3) fitness variation is effected by heritable genetic differences among individuals and (4) phenotype-fitness covariances must be, at least in part, underlain by genetic covariances. These latter two requirements for adaptive evolutionary change are relatively unstudied in natural populations. Absence of the latter requirements could explain stasis of apparently directionally selected heritable traits. We provide complementary analyses of selection and variation at phenotypic and genetic levels for juvenile growth rate in brook charr Salvelinus fontinalis in Freshwater River, Newfoundland, Canada. Contrary to the vast majority of reports in fish, we found very little viability selection of juvenile body size. Large body size appears nonetheless to be selectively advantageous via a relationship with early maturity. Genetic patterns in evolutionary parameters largely reflected phenotypic patterns. We have provided inference of selection based on longitudinal data, which are uncommon in high fecundity organisms. Furthermore we have provided a practicable framework for further studies of the genetic basis of natural selection.     

Accuracy of marker-assisted selection with auxiliary traits

Genetic information on molecular markers is increasingly being used in plant and animal improvement programmes particularly as indirect means to improve a metric trait by selection either on an individual basis or on the basis of an index incorporating such information. This paper examines the utility of an index of selection that not only combines phenotypic and molecular information on the trait under improvement but also combines similar information on one or more auxiliary traits. The accuracy of such a selection procedure has been theoretically studied for sufficiently large populations so that the effects of detected quantitative trait loci can be perfectly estimated. The theory is illustrated numerically by considering one auxiliary trait. It is shown that the use of an auxiliary trait improves the selection accuracy; and, hence, the relative efficiency of index selection compared to individual selection which is based on the same intensity of selection. This is particularly so for higher magnitudes of residual genetic correlation and environmental correlation having opposite signs, lower values of the proportion of genetic variation in the main trait associated with the markers, negligible proportion of genetic variation in the auxiliary trait associated with the markers, and lower values of the heritability of the main trait but higher values of the heritability of the auxiliary trait.     

SASQuant: a SAS software program to estimate genetic effects and heritabilities of quantitative traits in populations consisting of 6 related generations

Plant breeders are interested in the analysis of phenotypic data to measure genetic effects and heritability of quantitative traits and predict gain from selection. Measurement of phenotypic values of 6 related generations (parents, F(1), F(2), and backcrosses) allows for the simultaneous analysis of both Mendelian and quantitative traits. In 1997, Liu et al. released a SAS software based program (SASGENE) for the analysis of inheritance and linkage of qualitative traits. We have developed a new program (SASQuant) that estimates gene effects (Hayman's model), genetic variances, heritability, predicted gain from selection (Wright's and Warner's models), and number of effective factors (Wright's, Mather's, and Lande's models). SASQuant makes use of traditional genetic models and allows for their easy application to complex data sets. SASQuant is freely available and is intended for scientists studying quantitative traits in plant populations.     

A general model of the relation between phenotypic selection and genetic response

The phenotypic view of selection assumes that genetic responses can be predicted from selective forces and heritability — or in the classical quantitative genetic equation: R = h²S. However, data on selection in bird populations show that often no selection responses is found, despite consistent selective forces on phenotypes and significant heritable variation. Such discrepancies may arise due to the assumption that selection only acts on observed phenotypes. We derive a general selection equation that takes into account the possibility that some relevant (internal or external) traits are not measured. This equation shows that the classic equation applies if selection directly acts on the measured, phenotypic traits. This is not the case when, for instance, there are unknown internal genetic trade-offs, or unknown common environmental factors affecting both trait and fitness. In such cases, any relationship between phenotypic selection and genetic response is possible. Fortunately, the classical model can be tested by comparing phenotypic and genetic covariances between traits and fitness; an indication that important internal or external traits are missing can thus be obtained. Such an analysis was indeed found in the literature; for selection on fledging weight in Great Tits it yielded valuable extra information.     

Genetic components of variation in Nemophila menziesii undergoing inbreeding: morphology and flowering time.

The standard approaches to estimation of quantitative genetic parameters and prediction of response to selection on quantitative traits are based on theory derived for populations undergoing random mating. Many studies demonstrate, however, that mating systems in natural populations often involve inbreeding in various degrees (i.e. , self matings and matings between relatives). Here we apply theory developed for estimating quantitative genetic parameters for partially inbreeding populations to a population of Nemophila menziesii recently obtained from nature and experimentally inbred. Two measures of overall plant size and two of floral size expressed highly significant inbreeding depression. Of three dominance components of phenotypic variance that are defined under partial inbreeding, one was found to contribute significantly to phenotypic variance in flower size and flowering time, while the remaining two components contributed only negligibly to variation in each of the five traits considered. Computer simulations investigating selection response under the more complete genetic model for populations undergoing mixed mating indicate that, for parameter values estimated in this study, selection response can be substantially slowed relative to predictions for a random mating population. Moreover, inbreeding depression alone does not generally account for the reduction in selection response.     

Genetic and phenotypic correlations in a natural population of song sparrows

We estimated heritabilities, and genetic and phenotypic correlations between beak and body traits in the song sparrow ( Melospiza melodia ). We compared these estimates to values for the same traits in the Galápagos finches, Geospiza (Boag, 1983; Grant, 1983). Morphological variance is low in the song sparrow, and our results show that genetic and phenotypic correlations are considerably lower than correlations in the morphologically more variable Geospiza. Comparison using a larger sample of Galapagos populations confirms the existence of an association between variance and correlation for phenotypic values. We suggest two possible explanations for this association. First, most traits studied are functionally related, and the joint evolution of variance and correlation may have resulted from stabilizing selection about a line of optimal allometry between traits. Alternatively, introgression between populations and species could have caused correlation and variance to evolve jointly. Both selection and introgression were probably influential in producing the observed pattern, but it is not possible to estimate their relative importance with current data. Genetic and phenotypic correlations were correlated in the song sparrow, but heritabilities of traits varied greatly. As a result, the genetic variance-covariance matrix for traits is not simply a constant multiple of the phenotypic matrix. Evolutionary response to natural selection cannot, therefore, be predicted from the measurement of phenotypic characteristics alone.     

Quantitative analysis of correlations among flower traits in Gerbera hybrida, Compositae. III. Genetic variability and structure of principal component traits

 A sample of 36 flower traits consisting of six morphological categories in the Davis population of gerbera was restructured into phenotypic and genetic principal component traits. The first 5 phenotypic principal component traits accounted for 62% of the total phenotypic variance of the 36 traits and have moderate to high heritablities. The first 5 genetic principal component traits account for 97% of total genetic variance and all have high heritability. Morphological structure of these component traits suggest an underlying process identified by the first genetic principal component involving largely trans and disk floret traits. The results of this study indicate that the quantitative genetic structure of the gerbera flower is controlled by a few independent components and that principal component analysis is a useful tool to reveal variation in this structure. These composite traits are heritable and are expected to respond to selection. Received: 20 September 1997 / Accepted: 19 January 1998     

Quantitative genetics of growth and cryptic evolution of body size in an island population

While evolution occurs when selection acts on a heritable trait, empirical studies of natural systems have frequently reported phenotypic stasis under these conditions. We performed quantitative genetic analyses of weight and hindleg length in a free-living population of Soay sheep (Ovis aries) to test whether genetic constraints can explain previously reported stasis in body size despite evidence for strong positive directional selection. Genetic, maternal and environmental covariance structures were estimated across ontogeny using random regression animal models. Heritability increased with age for weight and hindleg length, though both measures of size were highly heritable across ontogeny. Genetic correlations among ages were generally strong and uniformly positive, and the covariance structures were also highly integrated across ontogeny. Consequently, we found no constraint to the evolution of larger size itself. Rather we expect size at all ages to increase in response to positive selection acting at any age. Consistent with expectation, predicted breeding values for age-specific size traits have increased over a twenty-year period, while maternal performance for offspring size has declined. Re-examination of the phenotypic data confirmed that sheep are not getting larger, but also showed that there are significant negative trends in size at all ages. The genetic evolution is therefore cryptic, with the response to selection presumably being masked at the phenotypic level by a plastic response to changing environmental conditions. Density-dependence, coupled with systematically increasing population size, may contribute to declining body size but is insufficient to completely explain it. Our results demonstrate that an increased understanding of the genetic basis of quantitative traits, and of how plasticity and microevolution can occur simultaneously, is necessary for developing predictive models of phenotypic change in nature.