Spatial variation in phenotypic selection on floral characteristics in an epiphytic orchid

Spatial variation in twelve floral characters was examined in an epiphytic orchidLepanthes rupestris to evaluate the strength and direction of phenotypic selection in seven riparian populations along two river basins in the Caribbean National Forest “El Yunque” for a range of 18–34 months. We evaluated selection on floral characters based on male (pollinaria removal) and female fitness (fruit set). Simple linear and quadratic regressions were used to evaluate the strength of directional, disruptive and stabilizing selections. Univariate and multivariate analyses were used to estimate the total strength of the selection acting on a character. Phenotypic selection was inconsistent among characters and populations. Few of the characters appeared to be under selection and none of them was found to be consistent throughout all populations. Inconsistency in selection coefficients among populations could suggest that selection is spatially variable. We only noted one character (column length) which had some consistency in differential selection coefficients among populations. Previous studies have shown that effective population sizes inL. rupestris are small and the observed “fitness differences” among populations could as easily be explained as stochastic events at play. We argue that the observed “fitness differences” in most characters and inconsistency among populations are likely from stochastic noise and not phenotypic selection. Consequently, we propose that random selection on character state support the hypothesis of genetic drift in small orchid populations.     

RESPONSE TO SELECTION IN PARTIALLY SELF-FERTILIZING POPULATIONS. I. SELECTION ON A SINGLE TRAIT

Self-fertilization is a common form of reproduction in plants and it has important implications for quantitative trait evolution. Here, I present a model of selection on quantitative traits that can accommodate any level of self-fertilization. The “structured linear model” (SLM) predicts the evolution of the mean phenotype as a function of three distinct quantities: the mean additive genetic value, the directional dominance, and the mean inbreeding coefficient. Stochastic simulations of truncation selection demonstrate the accuracy of the SLM in predicting changes in the mean and variance of a quantitative trait over the full range of selfing rates. They also illustrate how complex interactions between selection and mating system determine the population distribution of inbreeding coefficients and also the amount of linkage disequilibrium. Changes in the genetic variance due to linkage disequilibria, which are commonly referred to as the “Bulmer effect,” are greatly magnified by selfing. This complicates the relationship between selfing rate and response to selection. Like the random mating theory, the parameters of the SLM can be estimated from phenotypic data.     

VIABILITY SELECTION ON SEASONALLY POLYPHENIC TRAITS: WING MELANIN PATTERN IN WESTERN WHITE BUTTERFLIES

Wing melanin pattern varies seasonally among generations in many populations of the butterfly Pontia occidentalis, leading to distinctly different wing phenotypes during spring and summer generations. Estimates of directional selection on wing pattern can therefore quantify the imperfection of this phenotypically plastic (polyphenic) response in generating “optimal” phenotypes for each seasonal generation. Mark-release-recapture (MRR) studies were used to estimate directional selection on six wing traits in a natural population of P. occidentalis during both spring and summer weather conditions. Estimated survival and recapture probabilities varied substantially among the four MRR studies. When differences between males and females were detected, the survival and recapture probabilities were higher for males than for females. Estimated selection coefficients suggested that the direction of selection on one wing trait important for thermoregulation, melanin on the base of the dorsal hindwings (trait hb), fluctuated seasonally; there was evidence of directional selection for increased hb in the spring studies and for decreased hb in the summer studies. Such fluctuating seasonal selection on hb implies that the seasonal polyphenic response may not be sufficient to eliminate selection on this trait; the slope of the reaction-norm mapping hb onto seasonal environmental cues is too shallow, resulting in further selection on the reaction norm. Adaptive evolution of the reaction norm may be constrained by phenotypic and genetic correlations with other wing traits that experience different patterns of selection and by variable weather conditions within seasons and among years.     

The estimation of heritability of some developmental characters in natural populations ofArabidopsis thaliana (L.)Heynh

The investigation concerns to what extent the phenotypic variability of some characters connected with the developmental rate inArabidopsis thaliana (L.)Heynh. is of genetic nature. For this reason, in a variable natural populationSt? the values of coefficients of heritability were estimated by means of offspring-parent regression coefficients and of intraclass correlation coefficients for the three following characters: “number of days to appearance of the flower primordia”, “number of rosette leaves” and “number of rosette leaves per day”. The regression coefficients were calculated (1) by using simple progeny means, (2) the maternal data were repeated with each individual offspring value, and (3) the weighted regression coefficients were used. It has been found that about a half of phenotypic differences in developmental characters studied is determined genetically. The question is discussed whether such heritability estimates can be influenced by dominance or interactions, as it results from considerations about the population structure inArabidopsis. There are no substantial differences between the methods used, and in the given case, the estimation of heritability with the aid of the intraclass correlation coefficient appears to be very advantageous.     

Using path analysis to measure natural selection

We expand current methods for calculating selection coefficients using path analysis and demonstrate how to analyse nonlinear selection. While this incorporation is a straightforward extension of current procedures, the rules for combining these traits to calculate selection coefficients can be complex. We demonstrate our method with an analysis of selection in an experimental population of Arabidopsis thaliana consisting of 289 individuals. Multiple regression analyses found positive directional selection and positive nonlinear selection only for inflorescence height. In contrast, the path analyses also revealed positive directional selection for number of rosette leaves and positive nonlinear selection for leaf number and time of inflorescence initiation. These changes in conclusions came about because indirect selection was converted into direct selection with the change in causal structure. Path analysis has great promise for improving our understanding of natural selection but must be used with caution since coefficient estimates depend on the assumed causal structure.     

VISUALIZING MULTIVARIATE SELECTION

Recent developments in quantitative-genetic theory have shown that natural selection can be viewed as the multivariate relationship between fitness and phenotype. This relationship can be described by a multidimensional surface depicting fitness as a function of phenotypic traits. We examine the connection between this surface and the coefficients of phenotypic selection that can be estimated by multiple regression and show how the interpretation of multivariate selection can be facilitated through the use of the method of canonical analysis. The results from this analysis can be used to visualize the surface implied by a set of selection coefficients. Such a visualization provides a compact summary of selection coefficients, can aid in the comparison of selection surfaces, and can help generate testable hypotheses as to the adaptive significance of the traits under study. Further, we discuss traditional definitions of directional, stabilizing, and disruptive selection and conclude that selection may be more usefully classified into two general modes, directional and nonlinear selection, with stabilizing and disruptive selection as special cases of nonlinear selection.     

Differences in locomotor behavior correspond to different patterns of morphological selection in two species of waterfall-climbing gobiid fishes

Behavior plays an important role in mediating relationships between morphology and performance in animals and, thus, can influence how selection operates. However, to what extent can the use of specific behaviors be associated with particular types of selection on morphological traits? Laboratory selection analyses on waterfall-climbing gobiid fishes were performed to investigate how behavioral variations in locomotion can affect patterns of linear and nonlinear morphological selection. Species from sister genera (Sicyopterus stimpsoni and Sicydium punctatum) that use different climbing behaviors were exposed to similar artificial waterfalls to simulate a controlled selective regime involving the climbing of a nearly vertical slope against flowing water. Juvenile S. stimpsoni “inch up” waterfalls by alternate attachment of oral and pelvic suckers with little axial or fin movement, leading to straightforward expectations that climbing selection should favor morphologies that improve drag reduction and substrate adhesion. In contrast, juvenile S. punctatum climb using substantial axial and fin movements, complicating expectations for selection patterns and potentially promoting correlational selection. Comparisons of directional, quadratic and correlational selection coefficients for various morphological traits and trait interactions indicated that these species showed different selection patterns that generally fit these predictions. Both directional and correlational selection patterns were different between the species, and on average were stronger in S. punctatum compared to S. stimpsoni. Stronger selection in S. punctatum may be related to its climbing style that requires more integrated movement of the fins and body axis than S. stimpsoni, promoting dynamic interactions among body regions within a complicated hydrodynamic environment.     

Inbreeding: One word, several meanings

The way geneticists use the word “inbreeding” can be somewhat puzzling. How can the same word be applied to situations as different as the presence of commong ancestors in the pedigrees of two individuals, on one hand, and the attitude towards marriage in a population, on the other? How can the same parameter, i.e., the “inbreeding coefficient F,” be used both, to measure the degree of genetic resemblance between individuals within a single population and also to measure the degree of genetic differences between groups of individuals.It will be useful for the sake of translation as well as for that of clarity, to delineate the various situations in which geneticists are led to refer to “inbreeding.”We shall see that this one word is used in, at least, five concepts: relationship between relatives; genetic drift; departure from panmixia of mating behaviour; subdivision of a population into several isolated groups; and divergence between the actual genotypic structure of a population and the reference “Hardy-Weinberg Structure.”     

Rudimentary, “functionless” first metapodials of Canis latrans: Variation and association in length with longer,functional metapodials

A tenet of evolutionary theory is that phenotypic variation of a trait is inversely related to the intensity of stabilizing selection pressure. Among homologous bones, such as metapodials, a rudimentary, “nonfunctional” bone is expected to be more variable in length than nonrudimentary bones. This study compares variation and association in length among metapodials using 277 adult skeletons of Canis latrans. Canis latrans has a short, “functionless” first metacarpal (mc1) and “rudimentary, vestigial” first metatarsal (mt1). Results show that among the 10 metapodials, mt1 has the highest variation in length; other metapodials do not differ significantly from one another in their variation. Correlation coefficients for length of mc1 and mt1 with their ipsilateral metapodials 2-5 are significantly lower than coefficients for all other ipsilateral pairs. The correlation coefficient between left and right mt1 is significantly the lowest among all bilateral pairs of metapodials. Results are interpreted as follows. Mt1's high variation and low association in length are the outcome of less intense stabilizing selection pressure compared with other metapodials. The nonsignificant difference for variation in length between mc1 and metapodials 2-5 may be that mc1 is functional for development of a pollical dewclaw that helps restrain small prey.     

Sifaka positional behavior: ontogenetic and quantitative genetic approaches

In many primate species, hands and feet are large relative to neonatal body weight, and they subsequently exhibit negative allometric growth during ontogeny. Here, data are presented showing that this pattern holds for a wild population of lemur, Verreaux's sifaka (Propithecus verreauxi verreauxi). Using morphometric data collected on this population, it is shown that younger animals possess relatively large hands and feet. This ontogenetic pattern suggests a simple behavioral test: do juvenile animals with their larger, almost adult‐sized hands and feet locomote on similarly sized substrates as adult animals? Using locomotor bout sampling, this question was tested by collecting positional behavior data on this population. Results from this test find no differences in locomotor behaviors or substrate use between yearlings and adult animals. To place these results in a broader evolutionary context, heritabilities and selection gradients of hands, feet, and other limb elements for animals in this population were estimated. Among limb elements, heritabilities range from 0.16–0.44, with the foot having the lowest value. Positive directional selection acts most strongly on the foot (directional selection gradient = 0.119). The low heritability and positive selection coefficient indicate that selection has acted, and continues to act, on foot size in young animals. These results are interpreted within a functional context with respect to the development of locomotor coordination: larger feet enable young animals to use “adult‐sized” substrates when they move through their habitat. It is suggested that the widespread pattern of negative allometry of the extremities in sifaka and other primates is maintained by selection, and does not simply reflect a primitive developmental pathway that has no adaptive basis. Am J Phys Anthropol 131:261–271, 2006. © 2006 Wiley‐Liss, Inc.     

ADAPTIVE RADIATION ALONG GENETIC LINES OF LEAST RESISTANCE

Are measurements of quantitative genetic variation useful for predicting long-term adaptive evolution? To answer this question, I focus on g_max, the multivariate direction of greatest additive genetic variance within populations. Original data on threespine sticklebacks, together with published genetic measurements from other vertebrates, show that morphological differentiation between species has been biased in the direction of g_max for at least four million years, despite evidence that natural selection is the cause of differentiation. This bias toward the direction of evolution tends to decay with time. Rate of morphological divergence between species is inversely proportional to θ, the angle between the direction of divergence and the direction of greatest genetic variation. The direction of greatest phenotypic variance is not identical with g_max, but for these data is nearly as successful at predicting the direction of species divergence. I interpret the findings to mean that genetic variances and covariances constrain adaptive change in quantitative traits for reasonably long spans of time. An alternative hypothesis, however, cannot be ruled out: that morphological differentiation is biased in the direction g_max because divergence and g_max are both shaped by the same natural selection pressures. Either way, the results reveal that adaptive differentiation occurs principally along “genetic lines of least resistance.”     

The interpretation of selection coefficients

Evolutionary biologists have an array of powerful theoretical techniques that can accurately predict changes in the genetic composition of populations. Changes in gene frequencies and genetic associations between loci can be tracked as they respond to a wide variety of evolutionary forces. However, it is often less clear how to decompose these various forces into components that accurately reflect the underlying biology. Here, we present several issues that arise in the definition and interpretation of selection and selection coefficients, focusing on insights gained through the examination of selection coefficients in multilocus notation. Using this notation, we discuss how its flexibility—which allows different biological units to be identified as targets of selection—is reflected in the interpretation of the coefficients that the notation generates. In many situations, it can be difficult to agree on whether loci can be considered to be under “direct” versus “indirect” selection, or to quantify this selection. We present arguments for what the terms direct and indirect selection might best encompass, considering a range of issues, from viability and sexual selection to kin selection. We show how multilocus notation can discriminate between direct and indirect selection, and describe when it can do so.     

Genetic correlations and sex‐specific adaptation in changing environments

Females and males have conflicting evolutionary interests. Selection favors the evolution of different phenotypes within each sex, yet divergence between the sexes is constrained by the shared genetic basis of female and male traits. Current theory predicts that such “sexual antagonism” should be common: manifesting rapidly during the process of adaptation, and slow in its resolution. However, these predictions apply in temporally stable environments. Environmental change has been shown empirically to realign the direction of selection acting on shared traits and thereby alleviate signals of sexually antagonistic selection. Yet there remains no theory for how common sexual antagonism should be in changing environments. Here, we analyze models of sex‐specific evolutionary divergence under directional and cyclic environmental change, and consider the impact of genetic correlations on long‐run patterns of sex‐specific adaptation. We find that environmental change often aligns directional selection between the sexes, even when they have divergent phenotypic optima. Nevertheless, some forms of environmental change generate persistent sexually antagonistic selection that is difficult to resolve. Our results reinforce recent empirical observations that changing environmental conditions alleviate conflict between males and females. They also generate new predictions regarding the scope for sexually antagonistic selection and its resolution in changing environments.     

Genetical aspects of kin selection: effects of inbreeding

Hamilton's c/b < “r” rule is an important tool in sociobiological research and clearly functions as a “positive heuristic”, sensu Lakatos (1970). This paper examines the theoretical underpinnings of this rule in population genetics when inbreeding is taken into account. The model used is an extension of Charnov (1977) and assumes that the altruistic gene codes for a behavior between inbred individuals of a fixed genetic relationship. No consideration is given to the population or mating system processes which give rise to this relationship. It is shown that in inbred populations with weak selection the right-hand side of Hamilton's rule depends upon gene frequency and dominance as well as the degree of genetic relationship between the individuals involved. Because of this dependence, stable polymorphisms in altruistic and non-altruistic alleles are possible for certain ranges of c/b ratios. Another consequence is that the more dominant the altruistic gene, the easier it is for it to invade a population, but the harder it is for it to increase to high frequencies. In the special case when the individuals involved are inbred to the same extent and gene effects are additive, the RHS of the rule is independent of gene frequency and equals b_YX and r_YX: respectively Hamilton's regression coefficient of relatedness and Wright's correlation coefficient of relationship.     

Relative Selection Strength: Quantifying effect size in habitat‐ and step‐selection inference

Habitat‐selection analysis lacks an appropriate measure of the ecological significance of the statistical estimates—a practical interpretation of the magnitude of the selection coefficients. There is a need for a standard approach that allows relating the strength of selection to a change in habitat conditions across space, a quantification of the estimated effect size that can be compared both within and across studies. We offer a solution, based on the epidemiological risk ratio, which we term the relative selection strength (RSS ). For a “used‐available” design with an exponential selection function, the RSS provides an appropriate interpretation of the magnitude of the estimated selection coefficients, conditional on all other covariates being fixed. This is similar to the interpretation of the regression coefficients in any multivariable regression analysis. Although technically correct, the conditional interpretation may be inappropriate when attempting to predict habitat use across a given landscape. Hence, we also provide a simple graphical tool that communicates both the conditional and average effect of the change in one covariate. The average‐effect plot answers the question: What is the average change in the space use probability as we change the covariate of interest, while averaging over possible values of other covariates? We illustrate an application of the average‐effect plot for the average effect of distance to road on space use for elk (Cervus elaphus ) during the hunting season. We provide a list of potentially useful RSS expressions and discuss the utility of the RSS in the context of common ecological applications.     

Selection for costly sexual traits results in a vacant mating niche and male dimorphism

The expected strong directional selection for traits that increase a male's mating ability conflicts with the frequent observation that within species, males may show extreme variation in sexual traits. These male reproductive polymorphisms are usually attributed to direct male–male competition. It is currently unclear, however, how directional selection for sexually selected traits may convert into disruptive selection, and if female preference for elaborate traits may be an alternative mechanism driving the evolution of male polymorphism. Here, we explore this mechanism using the polyandric dwarf spider Oedothorax gibbosus as a model. We first show that males characterized by conspicuous cephalic structures serving as a nuptial feeding device (“gibbosus males”) significantly outperform other males in siring offspring of previously fertilized females. However, significant costs in terms of development time of gibbosus males open a mating niche for an alternative male type lacking expensive secondary sexual traits. These “tuberosus males” obtain virtually all fertilizations early in the breeding season. Individual‐based simulations demonstrate a hitherto unknown general principle, by which males selected for high investment to attract females suffer constrained mating opportunities. This creates a vacant mating niche of unmated females for noninvesting males and, consequently, disruptive selection on male secondary sexual traits.     

Causal mechanisms of evolution and the capacity for niche construction

Ernst Mayr proposed a distinction between “proximate”, mechanistic, and “ultimate”, evolutionary, causes of biological phenomena. This dichotomy has influenced the thinking of many biologists, but it is increasingly perceived as impeding modern studies of evolutionary processes, including study of “niche construction” in which organisms alter their environments in ways supportive of their evolutionary success. Some still find value for this dichotomy in its separation of answers to “how?” versus “why?”questions about evolution. But “why is A?” questions about evolution necessarily take the form “how does A occur?”, so this separation is illusory. Moreover, the dichotomy distorts our view of evolutionary causality, in that, contra Mayr, the action of natural selection, driven by genotype-phenotype-environment interactions which constitute adaptations, is no less “proximate” than the biological mechanisms which are altered by naturally selected genetic variants. Mayr’s dichotomy thus needs replacement by more realistic, mechanistic views of evolution. From a mechanistic viewpoint, there is a continuum of adaptations from those evolving as responses to unchanging environmental pressures to those evolving as the capacity for niche construction, and intermediate stages of this can be identified. Some biologists postulate an association of “phenotypic plasticity” (phenotype-environment covariation with genotype held constant) with capacity for niche construction. Both “plasticity” and niche construction comprise wide ranges of adaptive mechanisms, often fully heritable and resulting from case-specific evolution. Association of “plasticity” with niche construction is most likely to arise in systems wherein capacity for complex learning and behavioral flexibility have already evolved.