Natural selection on gall size: variable contributions of individual host plants to population-wide patterns

Studies that provide estimates of the form and magnitude of selection on herbivore traits at the level of individual plants in natural populations represent a vital step in understanding the interaction of selection and gene flow among host-affiliated insect populations when individual plants equate to differing selective regimes. We analyzed phenotypic selection on the trait gall size for a host-specific gall former at both the individual host plant and population level (across host plants) in each of two years. Linear and nonlinear selection and the fitness function relating gall size to the probability of survivorship in the absence of natural enemies were estimated for each level and year. Selection imposed by the host plant was observed in 19 of the 22 subpopulations monitored. At the population level, linear and nonlinear selection were evident each year. However, population-level estimates masked the significant heterogeneity in the form and direction of selection evident among plants each year. Heterogeneity among gall-former subpopulations is emphasized by our findings that selection varied from directional to stabilizing among plants and the majority of selection gradients estimated for individual plants did not fall within the 95% CIs of the population-level estimates.     

Impacts of environmental heterogeneity on natural selection in a wild bird population*

Natural selection has been studied for several decades, resulting in the computation of thousands of selection estimates. Although the importance of environmental conditions on selection has often been suggested, published estimates rarely take into account the effects of environmental heterogeneity on selection patterns. Here, we estimated linear and nonlinear viability selection gradients on morphological traits of 12-day old nestlings in a wild population of tree swallows (Tachycineta bicolor) across a large-scale heterogeneous study system in southern Québec, Canada. We assessed the environmental drivers of nestling survival and evaluated their effects on strength and direction of selection gradients. Separate analyses of environmental variables showed that high temperatures and heavy rainfall caused stronger positive linear selection on morphological traits. Weaker linear selection was also measured in more extensively cultivated areas. Both strength and shape of nonlinear quadratic and correlational components of selection were modified by environmental variables. Considering all environmental variables revealed that precipitation since hatching affected patterns of linear selection on traits, while temperatures since hatching shaped nonlinear selection patterns. Our study underlines the importance of quantifying linear and nonlinear natural selection under various environmental conditions and how the evolutionary response of traits may be affected by ongoing human-induced environmental changes.     

An analysis of continent-wide patterns of sexual selection in a passerine bird

Patterns of selection are widely believed to differ geographically, causing adaptation to local environmental conditions. However, few studies have investigated patterns of phenotypic selection across large spatial scales. We quantified the intensity of selection on morphology in a monogamous passerine bird, the barn swallow Hirundo rustica, using 6495 adults from 22 populations distributed across Europe and North Africa. According to the classical Darwin-Fisher mechanism of sexual selection in monogamous species, two important components of fitness due to sexual selection are the advantages that the most attractive males acquire by starting to breed early and their high annual fecundity. We estimated directional selection differentials on tail length (a secondary sexual character) and directional selection gradients after controlling for correlated selection on wing length and tarsus length with respect to these two fitness components. Phenotype and fitness components differed significantly among populations for which estimates were available for more than a single year. Likewise, selection differentials and selection gradients differed significantly among populations for tail length, but not for the other two characters. Sexual selection differentials differed significantly from zero across populations for tail length, particularly in males. Controlling statistically for the effects of age reduced the intensity of selection by 60 to 81%, although corrected and uncorrected estimates were strongly positively correlated. Selection differentials and gradients for tail length were positively correlated between the sexes among populations for selection acting on breeding date, but not for fecundity selection. The intensity of selection with respect to breeding date and fecundity were significantly correlated for tail length across populations. Sexual size dimorphism in tail length was significantly correlated with selection differentials with respect to breeding date for tail length in male barn swallows across populations. These findings suggest that patterns of sexual selection are consistent across large geographical scales, but also that they vary among populations. In addition, geographical patterns of phenotypic selection predict current patterns of phenotypic variation among populations, suggesting that consistent patterns of selection have been present for considerable amounts of time.     

Spatiotemporal fluctuations in natural selection acting on the gall‐parasitic aphid Tetraneura sorini

The measurement of the selection gradient is crucial for understanding the magnitude of selection acting directly on a trait and predicting the evolutionary trajectory of that trait. This study evaluated the selection gradient acting on the morphology of the gall‐parasitic aphid Tetraneura sorini during the galling process and compared the strength among populations. Gall formers (first instars) frequently fight with conspecifics or heterospecifics for usurping incipient galls using their well‐developed hind legs. First instars that successfully acquired galls were found within galls, whereas those that failed were found dead on leaf surfaces. Selection gradients were estimated using logistic stepwise regression and partial least square (PLS) regression. Calculated selection differentials indicated that first instars that secured galls were larger in body size than failed individuals through all populations. However, selection gradients on weapon traits varied largely among populations or among years in the same population. We confirmed microevolutionary changes in the relationship between traits, which accorded with the expectation from changes in the selection gradients. When gall formers were transferred onto developing buds individually, individuals that successfully induced galls had smaller body size than failed individuals. Available evidence suggests that the selection gradient on body size becomes higher with an increasing proportion of T. sorini in the Tetraneura species community. Thus, we concluded that more intense fighting with conspecifics leads to stronger selective pressure on body size, but that selective pressure for each trait is variable depending on differences in the tactics and species composition among populations.     

Quantifying selection on standard metabolic rate and body mass in Drosophila melanogaster

Standard metabolic rate (SMR), defined as the minimal energy expenditure required for self‐maintenance, is a key physiological trait. Few studies have estimated its relationship with fitness, most notably in insects. This is presumably due to the difficulty of measuring SMR in a large number of very small individuals. Using high‐throughput flow‐through respirometry and a Drosophila melanogaster laboratory population adapted to a life cycle that facilitates fitness measures, we quantified SMR, body mass, and fitness in 515 female and 522 male adults. We used a novel multivariate approach to estimate linear and nonlinear selection differentials and gradients from the variance‐covariance matrix of fitness, SMR, and body mass, allowing traits specific covariates to be accommodated within a single model. In males, linear selection differentials for mass and SMR were positive and individually significant. Selection gradients were also positive but, despite substantial sample sizes, were nonsignificant due to increased uncertainty given strong SMR‐mass collinearity. In females, only nonlinear selection was detected and it appeared to act primarily on body size, although the individual gradients were again nonsignificant. Selection did not differ significantly between sexes although differences in the fitness surfaces suggest sex‐specific selection as an important topic for further study.     

Comparing complex fitness surfaces: among-population variation in mutual sexual selection in Drosophila serrata

Despite a dramatic increase in empirical estimates of phenotypic selection over the past two decades, we remain remarkably ignorant about variation in the multivariate fitness surfaces that shape the adaptive landscape. We develop a novel approach for quantifying patterns of spatial and/or temporal variation in multivariate selection that directly compares vectors of linear selection gradients (beta) and matrices of nonlinear selection gradients (gamma) that describe the multivariate fitness surface in each population. We apply this approach to estimates of sexual selection on a suite of cuticular hydrocarbons (CHCs) in males and females from nine geographic populations of Drosophila serrata. In males, variation in linear sexual selection was associated with the presence of the related species Drosophila birchii, suggesting that female mate preferences for male CHCs differ between sympatry and allopatry. This is consistent with previous experimental results suggesting that reproductive character displacement of male CHCs has resulted from selection caused by the presence of D. birchii. No significant associations were found for nonlinear sexual selection in males. In females, large-scale variation in both linear and nonlinear sexual selection was negatively associated with assumed-neutral population genetic structure, suggesting a key role for chance events in male mate preference divergence.     

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

The role of sexual selection in fuelling genital evolution is becoming increasingly apparent from comparative studies revealing interspecific divergence in male genitalia and evolutionary associations between male and female genital traits. Despite this, we know little about intraspecific variance in male genital morphology, or how male and female reproductive traits covary among divergent populations. Here we address both topics using natural populations of the guppy, Poecilia reticulata, a livebearing fish that exhibits divergent patterns of male sexual behaviour among populations. Initially, we performed a series of mating trials on a single population to examine the relationship between the morphology of the male's copulatory organ (the gonopodium) and the success of forced matings. Using a combination of linear measurements and geometric morphometrics, we found that variation in the length and shape of the gonopodium predicted the success of forced matings in terms of the rate of genital contacts and insemination success, respectively. We then looked for geographical divergence in these traits, since the relative frequency of forced matings tends to be greater in high-predation populations. We found consistent patterns of variation in male genital size and shape in relation to the level of predation, and corresponding patterns of (co)variation in female genital morphology. Together, these data enable us to draw tentative conclusions about the underlying selective pressures causing correlated patterns of divergence in male and female genital traits, which point to a role for sexually antagonistic selection.     

The strength of phenotypic selection in natural populations

How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for studies that estimated the strength of linear and quadratic selection in terms of standardized selection gradients or differentials on natural variation in quantitative traits for field populations. We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. The absolute values of linear selection gradients |beta| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon. The values of |beta| for selection on morphological and on life-history/phenological traits were significantly different: on average, selection on morphology was stronger than selection on phenology/life history. Similarly, the values of |beta| for selection via aspects of survival, fecundity, and mating success were significantly different: on average, selection on mating success was stronger than on survival. Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. The absolute values of quadratic selection gradients |gamma| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. The distribution of gamma values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature.     

VARIABLE SELECTION ON EUROSTA'S GALL SIZE,I: THE EXTENT AND NATURE OF VARIATION IN PHENOTYPIC SELECTION

Natural fluctuations in environmental conditions are likely to induce variation in the intensity or direction of natural selection. A long-term study of the insect, Eurosta solidaginins Fitch (Diptera; Tephritidae), which induces stem galls on the perennial herb Solidago altissima (Asteraceae) was performed to explore the patterns of variation in phenotypic selection. The intensity of selection imposed by parasitoids and predators on gallmaking larvae, for gall size, was measured across 16 populations over the course of 4 generations, for a total of 64 population-generations. Directional selection was quantified by i, the selection intensity, and variance selection by j‘, a measure of the intensity of selection on phenotypic variance. Size-dependent attack by parasitoids caused upward directional selection (mean i_p = 0.42; SE = 0.023), while size-dependent bird attack favored larvae that induced smaller galls (mean i_b = -0.07; SE = 0.013. The mean net directional selection intensity was 0.35 (SE = 0.030), which indicates that insects inducing larger galls are generally favored by selection. The opposing patterns of size-dependent attack resulted in stabilizing selection in half the population generations, with an overall average. j‘ of -0.11 (SE = 0.078). The magnitude of directional selection was strongly influenced by the population mean gall size and weakly by the optimal gall size. The intensity of variance selection was strongly influenced by the shape of the fitness function, with sigmoidal and Gaussian-like shapes causing greater depletion of phenotypic variance.     

MEASURING SELECTION ON REACTION NORMS: AN EXPLORATION OF THE EUROSTA-SOLIDAGO SYSTEM

The sensitivity of genotypic expression to the environment can be depicted as the reaction norm, which is defined as the array of phenotypes produced by a single genotype over a range of environments. We studied selection on reaction norms of the gall-inducing insect Eurosta solidaginis (Diptera; Tephritidae), which attacks tall goldenrod Solidago altissima (Compositae). Gall size was treated as a component of insect phenotype and attributes of the host plant as environmental influences on gall development. Genetic differences in the response of gall size to plant lag time (the number of days before a plant responds to the gall maker) were examined. Reaction norms for full-sib families of flies were quantified as linear functions; the elevation of the function denoted gall size produced by the family averaged across all plants, and the function's slope denoted family sensitivity to lag time. Expected fitness of each family was regressed over reaction norm elevation and slope to yield selection gradients on these reaction norm parameters. Directional selection on gall size averaged across environments is four times stronger than selection on sensitivity. Yet, genetic variation for sensitivity contributes more than twice as much to gall phenotypic variance as family mean gall size. Our results suggest that selection on environmental sensitivity will be weak for populations restricted to a narrow segment of an environmental gradient, but strong for broadly distributed species.     

Selection on female behaviour fluctuates with offspring environment

Temporal variation in selection has long been proposed as a mechanism by which genetic variation could be maintained despite short‐term strong directional selection and has been invoked to explain the maintenance of consistent individual differences in behaviour. We tested the hypothesis that ecological changes through time lead to fluctuating selection, which could promote the maintenance of variation in female behavioural traits in a wild population of North American red squirrels. As predicted, linear selection gradients on female aggression and activity significantly fluctuated across years depending on the level of competition among juveniles for vacant territories. This selection acted primarily through juvenile overwinter survival rather than maternal fecundity. Incorporating uncertainty in individual measures of behaviour reduced the magnitude of annual selection gradients and increased uncertainty in these estimates, but did not affect the overall pattern of temporal fluctuations in natural selection that coincided with the intensity of competition for vacant territories. These temporal fluctuations in selection might, therefore, promote the maintenance of heritable individual differences in behaviour in this wild red squirrel population.     

Leaf size, specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses

We examined variation in leaf size and specific leaf area (SLA) in relation to the distribution of 22 chaparral shrub species on small-scale gradients of aspect and elevation. Potential incident solar radiation (insolation) was estimated from a geographic information system to quantify microclimate affinities of these species across north- and south-facing slopes. At the community level, leaf size and SLA both declined with increasing insolation, based on average trait values for the species found in plots along the gradient. However, leaf size and SLA were not significantly correlated across species, suggesting that these two traits are decoupled and associated with different aspects of performance along this environmental gradient. For individual species, SLA was negatively correlated with species distributions along the insolation gradient, and was significantly lower in evergreen versus deciduous species. Leaf size exhibited a negative but non-significant trend in relation to insolation distribution of individual species. At the community level, variance in leaf size increased with increasing insolation. For individual species, there was a greater range of leaf size on south-facing slopes, while there was an absence of small-leaved species on north-facing slopes. These results demonstrate that analyses of plant functional traits along environmental gradients based on community level averages may obscure important aspects of trait variation and distribution among the constituent species.     

A geographic mosaic of trophic interactions and selection: trees, aphids and birds

Genetic variation in plants is known to influence arthropod assemblages and species interactions. However, these influences may be contingent upon local environmental conditions. Here, we examine how plant genotype-based trophic interactions and patterns of natural selection change across environments. Studying the cottonwood tree, Populus angustifolia, the galling aphid, Pemphigus betae and its avian predators, we used three common gardens across an environmental gradient to examine the effects of plant genotype on gall abundance, gall size, aphid fecundity and predation rate on galls. Three patterns emerged: (i) plant genotype explained variation in gall abundance and predation, (ii) G×E explained variation in aphid fecundity, and environment explained variation in gall abundance and gall size, (iii) natural selection on gall size changed from directional to stabilizing across environments.     

Nonlinear selection and the evolution of variances and covariances for continuous characters in an anole

The pattern of genetic variances and covariances among characters, summarized in the additive genetic variance‐covariance matrix, G , determines how a population will respond to linear natural selection. However, G itself also evolves in response to selection. In particular, we expect that, over time, G will evolve correspondence with the pattern of multivariate nonlinear natural selection. In this study, we substitute the phenotypic variance‐covariance matrix ( P ) for G to determine if the pattern of multivariate nonlinear selection in a natural population of Anolis cristatellus, an arboreal lizard from Puerto Rico, has influenced the evolution of genetic variances and covariances in this species. Although results varied among our estimates of P and fitness, and among our analytic techniques, we find significant evidence for congruence between nonlinear selection and P , suggesting that natural selection may have influenced the evolution of genetic constraint in this species.     

Changes in the selection differential exerted on a marine snail during the ontogeny of a predatory shore crab

Empirical estimates of selection gradients caused by predators are common, yet no one has quantified how these estimates vary with predator ontogeny. We used logistic regression to investigate how selection on gastropod shell thickness changed with predator size. Only small and medium purple shore crabs (Hemigrapsus nudus) exerted a linear selection gradient for increased shell‐thickness within a single population of the intertidal snail (Littorina subrotundata). The shape of the fitness function for shell thickness was confirmed to be linear for small and medium crabs but was humped for large male crabs, suggesting no directional selection. A second experiment using two prey species to amplify shell thickness differences established that the selection differential on adult snails decreased linearly as crab size increased. We observed differences in size distribution and sex ratios among three natural shore crab populations that may cause spatial and temporal variation in predator‐mediated selection on local snail populations.     

The spatial patterns of directional phenotypic selection

Local adaptation, adaptive population divergence and speciation are often expected to result from populations evolving in response to spatial variation in selection. Yet, we lack a comprehensive understanding of the major features that characterise the spatial patterns of selection, namely the extent of variation among populations in the strength and direction of selection. Here, we analyse a data set of spatially replicated studies of directional phenotypic selection from natural populations. The data set includes 60 studies, consisting of 3937 estimates of selection across an average of five populations. We performed meta‐analyses to explore features characterising spatial variation in directional selection. We found that selection tends to vary mainly in strength and less in direction among populations. Although differences in the direction of selection occur among populations they do so where selection is often weakest, which may limit the potential for ongoing adaptive population divergence. Overall, we also found that spatial variation in selection appears comparable to temporal (annual) variation in selection within populations; however, several deficiencies in available data currently complicate this comparison. We discuss future research needs to further advance our understanding of spatial variation in selection.     

Consumer‐resource interactions along urbanization gradients drive natural selection*

Urbanization is an important component of global change. Urbanization affects species interactions, but the evolutionary implications are rarely studied. We investigate the evolutionary consequences of a common pattern: the loss of high trophic‐level species in urban areas. Using a gall‐forming fly, Eurosta solidaginis, and its natural enemies that select for opposite gall sizes, we test for patterns of enemy loss, selection, and local adaptation along five urbanization gradients. Eurosta declined in urban areas, as did predation by birds, which preferentially consume gallmakers that induce large galls. These declines were linked to changes in habitat availability, namely reduced forest cover in urban areas. Conversely, a parasitoid that attacks gallmakers that induce small galls was unaffected by urbanization. Changes in patterns of attack by birds and parasitoids resulted in stronger directional selection, but loss of stabilizing selection in urban areas, a pattern which we suggest may be general. Despite divergent selective regimes, gall size did not very systematically with urbanization, suggesting but not conclusively demonstrating that environmental differences, gene flow, or drift, may have prevented the adaptive divergence of phenotypes. We argue that the evolutionary effects of urbanization will have predictable consequences for patterns of species interactions and natural selection.     

COMPARING STRENGTHS OF DIRECTIONAL SELECTION: HOW STRONG IS STRONG?

The fundamental equation in evolutionary quantitative genetics, the Lande equation, describes the response to directional selection as a product of the additive genetic variance and the selection gradient of trait value on relative fitness. Comparisons of both genetic variances and selection gradients across traits or populations require standardization, as both are scale dependent. The Lande equation can be standardized in two ways. Standardizing by the variance of the selected trait yields the response in units of standard deviation as the product of the heritability and the variance-standardized selection gradient. This standardization conflates selection and variation because the phenotypic variance is a function of the genetic variance. Alternatively, one can standardize the Lande equation using the trait mean, yielding the proportional response to selection as the product of the squared coefficient of additive genetic variance and the mean-standardized selection gradient. Mean-standardized selection gradients are particularly useful for summarizing the strength of selection because the mean-standardized gradient for fitness itself is one, a convenient benchmark for strong selection. We review published estimates of directional selection in natural populations using mean-standardized selection gradients. Only 38 published studies provided all the necessary information for calculation of mean-standardized gradients. The median absolute value of multivariate mean-standardized gradients shows that selection is on average 54% as strong as selection on fitness. Correcting for the upward bias introduced by taking absolute values lowers the median to 31%, still very strong selection. Such large estimates clearly cannot be representative of selection on all traits. Some possible sources of overestimation of the strength of selection include confounding environmental and genotypic effects on fitness, the use of fitness components as proxies for fitness, and biases in publication or choice of traits to study.     

Duplication and population dynamics shape historic patterns of selection and genetic variation at the major histocompatibility complex in rodents

Genetic variation at the major histocompatibility complex (MHC) is vitally important for wildlife populations to respond to pathogen threats. As natural populations can fluctuate greatly in size, a key issue concerns how population cycles and bottlenecks that could reduce genetic diversity will influence MHC genes. Using 454 sequencing, we characterized genetic diversity at the DRB Class II locus in montane voles (Microtus montanus), a North American rodent that regularly undergoes high‐amplitude fluctuations in population size. We tested for evidence of historic balancing selection, recombination, and gene duplication to identify mechanisms maintaining allelic diversity. Counter to our expectations, we found strong evidence of purifying selection acting on the DRB locus in montane voles. We speculate that the interplay between population fluctuations and gene duplication might be responsible for the weak evidence of historic balancing selection and strong evidence of purifying selection detected. To further explore this idea, we conducted a phylogenetically controlled comparative analysis across 16 rodent species with varying demographic histories and MHC duplication events (based on the maximum number of alleles detected per individual). On the basis of phylogenetic generalized linear model‐averaging, we found evidence that the estimated number of duplicated loci was positively related to allelic diversity and, surprisingly, to the strength of purifying selection at the DRB locus. Our analyses also revealed that species that had undergone population bottlenecks had lower allelic richness than stable species. This study highlights the need to consider demographic history and genetic structure alongside patterns of natural selection to understand resulting patterns of genetic variation at the MHC.