Spatial Variation In Selection Research Articles

Climate change does not equally affect temporal patterns of natural selection on reproductive timing across populations in two songbird species.

Climate change has led to changes in the strength of directional selection on seasonal timing. Understanding the causes and consequences of these changes is crucial to predict the impact of climate change. But are observed patterns in one population generalizable to others, and can spatial variation in selection be explained by environmental variation among populations? We used long-term data (1955-2022) on blue and great tits co-occurring in four locations across the Netherlands to assess inter-population variation in temporal patterns of selection on laying date. To analyse selection, we combine reproduction and adult survival into a joined fitness measure. We found distinct spatial variation in temporal patterns of selection which overall acted towards earlier laying, and which was due to selection through reproduction rather than through survival. The underlying relationships between temperature, bird and caterpillar phenology were however the same across populations, and the spatial variation in selection patterns is thus caused by spatial variation in the temperatures and other habitat characteristics to which birds and caterpillars respond. This underlines that climate change is not necessarily equally affecting populations, but that we can understand this spatial variation, which enables us to predict climate change effects on selection for other populations.

Spatially and temporally varying selection influence species boundaries in two sympatric Mimulus.

Spatially and temporally varying selection can maintain genetic variation within and between populations, but it is less well known how these forces influence divergence between closely related species. We identify the interaction of temporal and spatial variation in selection and their role in either reinforcing or eroding divergence between two closely related Mimulus species. Using repeated reciprocal transplant experiments with advanced generation hybrids, we compare the strength of selection on quantitative traits involved in adaptation and reproductive isolation in Mimulus guttatus and Mimulus laciniatus between two years with dramatically different water availability. We found strong divergent habitat-mediated selection on traits in the direction of species differences during a drought in 2013, suggesting that spatially varying selection maintains species divergence. However, a relaxation in divergent selection on most traits in an unusually wet year (2019), including flowering time, which is involved in pre-zygotic isolation, suggests that temporal variation in selection may weaken species differences. Therefore, we find evidence that temporally and spatially varying selection may have opposing roles in mediating species boundaries. Given our changing climate, future growing seasons are expected to be more similar to the dry year, suggesting that in this system climate change may actually increase species divergence.

Population genetic differentiation and genomic signatures of adaptation to climate in an abundant lizard

Species distributed across climatic gradients will typically experience spatial variation in selection, but gene flow can prevent such selection from causing population genetic differentiation and local adaptation. Here, we studied genomic variation of 415 individuals across 34 populations of the common wall lizard (Podarcis muralis) in central Italy. This species is highly abundant throughout this region and populations belong to a single genetic lineage, yet there is extensive phenotypic variation across climatic regimes. We used redundancy analysis to, first, quantify the effect of climate and geography on population genomic variation in this region and, second, to test if climate consistently sorts specific alleles across the landscape. Climate explained 5% of the population genomic variation across the landscape, about half of which was collinear with geography. Linear models and redundancy analyses identified loci that were significantly differentiated across climatic regimes. These loci were distributed across the genome and physically associated with genes putatively involved in thermal tolerance, regulation of temperature-dependent metabolism and reproductive activity, and body colouration. Together, these findings suggest that climate can exercise sufficient selection in lizards to promote genetic differentiation across the landscape in spite of high gene flow.

Herbivore-Mediated Selection on Floral Display Covaries Nonlinearly With Plant-Antagonistic Interaction Intensity Among Primrose Populations.

Quantifying the relations between plant-antagonistic interactions and natural selection among populations is important for predicting how spatial variation in ecological interactions drive adaptive differentiation. Here, we investigate the relations between the opportunity for selection, herbivore-mediated selection, and the intensity of plant-herbivore interaction among 11 populations of the insect-pollinated plant Primula florindae over 2 years. We experimentally quantified herbivore-mediated directional selection on three floral traits (two display and one phenological) within populations and found evidence for herbivore-mediated selection for a later flowering start date and a greater number of flowers per plant. The opportunity for selection and strength of herbivore-mediated selection on number of flowers varied nonlinearly with the intensity of herbivory among populations. These parameters increased and then decreased with increasing intensity of plant-herbivore interactions, defined as an increase in the ratio of herbivore-damaged flowers per individual. Our results provide novel insights into how plant-antagonistic interactions can shape spatial variation in selection on floral traits and contribute toward understanding the mechanistic basis of geographic variation in angiosperm flowers.

Natural selection fluctuates at an extremely fine spatial scale inside a wild population of snapdragon plants.

Spatial variation in natural selection is expected to shape phenotypic variation of wild populations and drive their evolution. Although evidence of phenotypic divergence across populations experiencing different selection regimes is abundant, investigations of intrapopulation variation in selection pressures remain rare. Fine‐grained spatial environmental heterogeneity can be expected to influence selective forces within a wild population and thereby alter its fitness function by producing multiple fitness optima at a fine spatial scale. Here, we tested this hypothesis in a wild population of snapdragon plants living on an extremely small island in southern France (about 7500 m2). We estimated the spline‐based fitness function linking individuals’ fitness and five morphological traits in interaction with three spatially variable ecological drivers. We found that selection acting on several traits varied both in magnitude and direction in response to environmental variables at the scale of a meter. Our findings illustrate how different phenotypes can be selected at different locations within a population in response to environmental variation. Investigating spatial variation in selection within a population, in association with ecological conditions, represents an opportunity to identify putative ecological drivers of selection in the wild.

Heterogeneous selection on exploration behavior within and among West European populations of a passerine bird

Heterogeneous selection is often proposed as a key mechanism maintaining repeatable behavioral variation ("animal personality") in wild populations. Previous studies largely focused on temporal variation in selection within single populations. The relative importance of spatial versus temporal variation remains unexplored, despite these processes having distinct effects on local adaptation. Using data from >3,500 great tits (Parus major) and 35 nest box plots situated within five West-European populations monitored over 4 to 18 y, we show that selection on exploration behavior varies primarily spatially, across populations, and study plots within populations. Exploration was, simultaneously, selectively neutral in the average population and year. These findings imply that spatial variation in selection may represent a primary mechanism maintaining animal personalities, likely promoting the evolution of local adaptation, phenotype-dependent dispersal, and nonrandom settlement. Selection also varied within populations among years, which may counteract local adaptation. Our study underlines the importance of combining multiple spatiotemporal scales in the study of behavioral adaptation.

Ecological factors influence balancing selection on leaf chemical profiles of a wildflower.

Balancing selection is frequently invoked as a mechanism that maintains variation within and across populations. However, there are few examples of balancing selection operating on loci underpinning complex traits, which frequently display high levels of variation. We investigated mechanisms that may maintain variation in a focal polymorphism—leaf chemical profiles of a perennial wildflower (Boechera stricta, Brassicaceae)—explicitly interrogating multiple ecological and genetic processes including spatial variation in selection, antagonistic pleiotropy, and frequency-dependent selection. A suite of common garden and greenhouse experiments showed that the alleles underlying variation in chemical profile have contrasting fitness effects across environments, implicating two ecological drivers of selection on chemical profile: herbivory and drought. Phenotype-environment associations and molecular genetic analyses revealed additional evidence of past selection by these drivers. Together, these data are consistent with balancing selection on chemical profile, likely caused by pleiotropic effects of secondary chemical biosynthesis genes on herbivore defense and drought response.

Is variation in flower shape and length among native and non-native populations of Nicotiana glauca a product of pollinator-mediated selection?

Due to drastic changes in pollinators between native and invaded habitats, we might expect that pollinator-mediated selection on floral traits of alien plants differ from that in their native ranges. Here, through geometric morphometric tools and phenotypic selection analyses, we examined whether adaptation in flower shape and length occurred in Nicotiana glauca as a response to pollinator selection in contrasting pollination environments. We assessed populations of this plant species in the native range (South America), where plants depend on hummingbird pollination, and in two invaded areas, one where sunbirds act as pollinators (South Africa), and another where nectar feeding birds are absent and reproduction is entirely by autonomous self-pollination (Mallorca, Spain). Corolla length and shape varied significantly among pollination environments. Non-native sites were less variable and their range of variation fell within the native range of variation. Flower length in native populations and in a South African population matched the bill length of their respective pollinators. In contrast with the straight floral tubes in the native range, both non-native areas had significantly curved tubes. Curvature may improve the fit with the curved bills of sunbirds in South Africa (versus straight beaks of hummingbirds) and may enhance self-pollination in Mallorca, but this similarity between invaded areas may equally be due to drift and a shared colonization route. We found spatial variation in selection acting on corolla length but not on corolla shape. Overall, selection patterns were not consistent with floral trait variation. Although some results are consistent with both drift and selection, our study suggests that population divergence in flower shape and length is more likely the result of long-term diversifying pollinator-driven selection, which is difficult to detect by studying a single selection event.

Niche Construction Affects the Variability and Strength of Natural Selection.

Consideration of the properties of the sources of selection potentially helps biologists account for variation in selection. Here we explore how the variability of natural selection is affected by organisms that regulate the experienced environment through their activities (whether by constructing components of their local environments, such as nests, burrows, or pupal cases, or by choosing suitable resources). Specifically, we test the predictions that organism-constructed sources of selection that buffer environmental variation will result in (i) reduced variation in selection gradients, including reduced variation between (a) years (temporal variation) and (b) locations (spatial variation), and (ii) weaker directional selection relative to nonconstructed sources. Using compiled data sets of 1,045 temporally replicated selection gradients, 257 spatially replicated selection gradients, and a pooled data set of 1,230 selection gradients, we find compelling evidence for reduced temporal variation and weaker selection in response to constructed compared to nonconstructed sources of selection and some evidence for reduced spatial variation in selection. These findings, which remained robust to alternative data sets, taxa, analytical methods, definitions of constructed/nonconstructed, and other tests of reliability, suggest that organism-manufactured or chosen components of environments may have qualitatively different properties from other environmental features.

Is there spatial variation in phenotypic selection on floral traits in a generalist plant–pollinator system?

The selective role of pollinators on the floral phenotype has been identified as the main force behind angiosperm diversification. However, in generalized plant–pollinator interactions this association may not be that evident, since pollinator assemblages vary in composition among populations, possibly influencing the direction and intensity of floral trait selection. In this study we determine whether there was spatial variation in pollinator assemblages and the selective forces they exert in ten populations of Alstroemeria ligtu var. simsii. We characterized the whole pollinator assemblage in ten populations, quantified four floral attraction traits and determined potential selection targets in each of the study populations. Our results revealed that populations differed in the composition of their pollinator assemblages, and the pollinators with the highest visitation rates also differed among populations. Using phenotypic selection analysis we detected significant differentials and selection gradients only in two of the ten populations, for corolla tube length and ratio of the nectar guide. The spatial variation in selection showed that linear selection acting upon these traits differed significantly among the studied populations. Our study indicates that selection can be detected in generalized plant–pollinator systems and brings new evidence of phenotypic selection variation in space for this endemic plant species. Future studies are needed to determine whether the selective patterns described here are consistent over time and whether they produce evolutionary change in the populations under study.

Natural selection favors local specialization in a widespread habitat generalist.

The ecological success of widespread species is attributed to an ability to generalize across diverse habitats, a so-called "jack of all trades" scenario. However, this assumption ignores the potential for local specialization, an alternative scenario whereby spatial variation in natural selection generates habitat-specific fitness surfaces. Despite a growing recognition of spatial variation in selection in nature, and the inevitable exploitation of distinct habitat types across an extensive geographic range, attention to this hypothesis has been lacking for widespread taxa. We test this hypothesis using data from four populations of a widespread species drawing from two distinct habitat types (tree- and boulder-dominated, respectively). Specifically, we compare major physiological traits of male and female lizards by habitat type and then estimate the shape of natural selection gradients on those traits for each sex in each habitat (i.e., their fitness surfaces). We detected significant differences in morphology and performance across habitats that mirror interspecific patterns. Importantly, patterns of linear and nonlinear selection on these traits were habitat-specific for both sexes, supporting a clear but underappreciated capacity for local specialization. Our findings challenge assumptions of habitat generalism in widespread taxa, and instead provide some evidence for adaptive diversification in driving their ecological success.

Little plant, big city: a test of adaptation to urban environments in common ragweed (Ambrosia artemisiifolia).

A full understanding of how cities shape adaptation requires characterizing genetically-based phenotypic and fitness differences between urban and rural populations under field conditions. We used a reciprocal transplant experiment with the native plant common ragweed, (Ambrosia artemisiifolia), and found that urban and rural populations have diverged in flowering time, a trait that strongly affects fitness. Although urban populations flowered earlier than rural populations, plants growing in urban field sites flowered later than plants in rural field sites. This counter-gradient variation is consistent adaptive divergence between urban and rural populations. Also consistent with local adaptation, both urban and rural genotypes experienced stronger net selection in the foreign than in the local habitat, but this pattern was not significant for male fitness. Despite the evidence for local adaptation, rural populations had higher lifetime fitness at all sites, suggesting that selection has been stronger or more uniform in rural than urban populations. We also found that inter-population differences in both flowering time and fitness tended to be greater among urban than rural populations, which is consistent with greater drift or spatial variation in selection within urban environments. In summary, our results are consistent with adaptive divergence of urban and rural populations, but also suggest there may be greater environmental heterogeneity in urban environments which also affects evolution in urban landscapes.

Adaptation in temporally variable environments: stickleback armor in periodically breaching bar-built estuaries.

The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar-built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re-form within a few weeks or months, thereby re-isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within-population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure and then analysed how stickleback armor traits, the associated genes Eda and Pitx1 and elemental composition (%P) varies within and among populations. Despite strong gene flow, we detected evidence for divergence in stickleback defensive traits and Eda genotypes associated with predation regime. However, this among-population variation was lower than that observed among other stickleback populations exposed to divergent predator regimes. In addition, within-population variation was very high as compared to populations from environmentally stable locations. Elemental composition was strongly associated with armor traits, Eda genotype and the presence of predators, thus suggesting that spatiotemporal variation in armor traits generates corresponding variation in elemental phenotypes. We conclude that gene flow, and especially temporal environmental variation, can maintain high levels of within-population variation while reducing, but not eliminating, among-population variation driven by spatial environmental variation.

Contribution of gene flow to the evolution of recombination suppression in sex chromosomes

Polymorphism of alleles that benefit one sex but harm the other (sexually antagonistic alleles) generates selective pressures for reduced recombination between themselves and sex-determination loci. Such polymorphism can be maintained within a population when selection coefficients are sufficiently balanced between males and females. However, if regulatory mutations restrict gene expression only to one sex, these alleles become neutral in the other sex and easily fixed within a population, removing the selective pressures for recombination suppression in sex chromosomes. When there is spatial variation in selection regimes, however, alleles that are deleterious in one sex and neutral in the other can be maintained in other neighboring populations and gene flow may continuously supply deleterious alleles. We hypothesized that this maintenance of genetic variation may promote the establishment of recombination suppression in sex chromosomes even in cases where selection is limited to one sex. Using individual-based simulations, we show that spatial variation in male-limited selection and gene flow can promote the establishment of Y-autosome fusions, a special case of recombination suppression in sex chromosomes. This can be explained by the fact that fused Y-chromosomes that capture alleles that are beneficial for local males have a higher mean fitness compared to unfused Y chromosomes in the presence of deleterious gene flow. We also simulated the case of sex-concordant selection and found that gene flow of alleles that are deleterious in both sexes did not substantially increase the establishment rates of Y-autosome fusions across the parameter space examined. This can be accounted for by the fact that foreign alleles that are deleterious in both sexes can be efficiently removed from the population compared to alleles that are neutral in females. These results indicate that how gene flow affects the establishment rates of Y-autosome fusions depends largely on selection regimes. Spatial variation in sex-specific selection and gene flow should be appreciated as a factor affecting sex chromosome evolution.

The Relative Contributions of the X Chromosome and Autosomes to Local Adaptation.

Models of sex chromosome and autosome evolution yield key predictions about the genomic basis of adaptive divergence, and such models have been important in guiding empirical research in comparative genomics and studies of speciation. In addition to the adaptive differentiation that occurs between species over time, selection also favors genetic divergence across geographic space, with subpopulations of single species evolving conspicuous differences in traits involved in adaptation to local environmental conditions. The potential contribution of sex chromosomes (the X or Z) to local adaptation remains unclear, as we currently lack theory that directly links spatial variation in selection to local adaptation of X-linked and autosomal genes. Here, we develop population genetic models that explicitly consider the effects of genetic dominance, effective population size, and sex-specific migration and selection on the relative contributions of X-linked and autosomal genes to local adaptation. We show that X-linked genes should nearly always disproportionately contribute to local adaptation in the presence of gene flow. We also show that considerations of dominance and effective population size-which play pivotal roles in the theory of faster-X adaptation between species-have surprisingly little influence on the relative contribution of the X chromosome to local adaptation. Instead, sex-biased migration is the primary mediator of the strength of spatial large-X effects. Our results yield novel predictions about the role of sex chromosomes in local adaptation. We outline empirical approaches in evolutionary quantitative genetics and genomics that could build upon this new theory.

From the ground up: biotic and abiotic features that set the course from genes to ecosystems.

Spatial variation in cone serotiny in Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) across Yellowstone National Park influences initial pine recruitment after stand‐replacing fire with tremendous population, community, and ecosystem consequences. A previous study showed that much of the spatial variation in serotiny results from the balance of selection arising from high frequencies of fire favoring serotiny countered by opposing selection exerted by American red squirrels (Tamiasciurus hudsonicus) as seed predators. This earlier study, however, assumed stable local red squirrel densities over multiple generations of pines. Here, we examine environmental properties that might contribute to long‐term stability in the densities of red squirrels among sites. We found that the amount of clay in the soil, an indicator of plant and fungal growth—the latter an important food resource for red squirrels—and the coefficient of variation (CV) in diameter at breast height (DBH) of forest trees together account for a substantial amount of variation in red squirrel density. Soil development occurs over very long time scales, and thus, intersite variation in the amount of clay is unlikely to shift across pine generations. However, CV of DBH and squirrel density increase with stand age, which acts to amplify selection against serotiny with increasing interfire interval. Regardless, much of the variation in the CV of DBH is accounted for by soil bulk density, mean annual temperature, and surface curvature, which are unlikely to vary in their relative differences among sites over time. Consequently, these soil and abiotic attributes could contribute to consistent spatial patterns of red squirrel densities from one pine generation to the next, resulting in consistent local and spatial variation in selection exerted by red squirrels against serotiny.

Environment-dependent variation in selection on life history across small spatial scales.

Variation in life-history traits is ubiquitous, even though genetic variation is thought to be depleted by selection. One potential mechanism for the maintenance of trait variation is spatially variable selection. We explored spatial variation in selection in the field for a colonial marine invertebrate that shows phenotypic differences across a depth gradient of only 3 m. Our analysis included life-history traits relating to module size, colony growth, and phenology. Directional selection on colony growth varied in strength across depths, while module size was under directional selection at one depth but not the other. Differences in selection may explain some of the observed phenotypic differentiation among depths for one trait but not another: instead, selection should actually erode the differences observed for this trait. Our results suggest selection is not acting alone to maintain trait variation within and across environments in this system.

Inter and intra-population phenotypic and genotypic structuring in the European whitefish Coregonus lavaretus, a rare freshwater fish in Scotland.

This study revealed between-lake genetic structuring between Coregonus lavaretus collected from the only two native populations of this species in Scotland, U.K. (Lochs Eck and Lomond) evidenced by the existence of private alleles (12 in Lomond and four in Eck) and significant genetic differentiation (FST = 0·056) across 10 microsatellite markers. Juvenile C. lavaretus originating from eggs collected from the two lakes and reared in a common-garden experiment showed clear phenotypic differences in trophic morphology (i.e. head and body shape) between these populations indicating that these characteristics were, at least partly, inherited. Microsatellite analysis of adults collected from different geographic regions within Loch Lomond revealed detectable and statistically significant but relatively weak genetic structuring (FST = 0·001-0·024) and evidence of private alleles related to the basin structure of the lake. Within-lake genetic divergence patterns suggest three possibilities for this observed pattern: (1) differential selection pressures causing divergence into separate gene pools, (2) a collapse of two formerly divergent gene pools and (3) a stable state maintained by balancing selection forces resulting from spatial variation in selection and lake heterogeneity. Small estimates of effective population sizes for the populations in both lakes suggest that the capacity of both populations to adapt to future environmental change may be limited.

The role of migration in the evolution of phenotypic switching.

Stochastic switching is an example of phenotypic bet hedging, where an individual can switch between different phenotypic states in a fluctuating environment. Although the evolution of stochastic switching has been studied when the environment varies temporally, there has been little theoretical work on the evolution of phenotypic switching under both spatially and temporally fluctuating selection pressures. Here, we explore the interaction of temporal and spatial change in determining the evolutionary dynamics of phenotypic switching. We find that spatial variation in selection is important; when selection pressures are similar across space, migration can decrease the rate of switching, but when selection pressures differ spatially, increasing migration between demes can facilitate the evolution of higher rates of switching. These results may help explain the diverse array of non-genetic contributions to phenotypic variability and phenotypic inheritance observed in both wild and experimental populations.

Spatial variation in selective mortality on larval traits in the coral reef fish Chromis viridis

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 509:303-308 (2014) - DOI: https://doi.org/10.3354/meps10859 NOTE Spatial variation in selective mortality on larval traits in the coral reef fish Chromis viridis Heidi E. Block*, Mark A. Steele California State University Northridge, 18111 Nordhoff St., Northridge, California 91330-8303, USA *Corresponding author: heidieblock@gmail.com ABSTRACT: Larval traits in reef fishes influence their probability of surviving after settling, but few studies have explored the extent to which selective mortality varies from site to site. We examined the effects of larval traits on the survival of Chromis viridis at 2 sites in Moorea, French Polynesia. We compared average traits of recently settled fish with those of 1 mo old survivors from the same cohort. At both study sites, there was selection for larger size at settlement. A commonly used statistical approach that does not account for correlations among larval traits (ANOVA) indicated that selection on planktonic larval duration (PLD) and larval growth rate was inconsistent between the 2 sites, with selection for PLD at one site and larval growth rate at the other. Larval growth rate and PLD, however, were strongly correlated, such that faster-growing larvae settled at younger ages at both sites. Selection gradient analysis, which accounts for correlations among larval traits, revealed that selection for longer PLD and faster larval growth rates occurred at both study sites but was stronger at one site than the other. We detected no significant differences in habitat characteristics or predator assemblages between the 2 sites. Our findings highlight the need to statistically control for correlations among larval traits when measuring selection, as well as the need to explore spatial variation in selection on larval traits. KEY WORDS: Larval growth · Planktonic larval duration · Size at settlement · Moorea · Otolith · Correlated larval traits Full text in pdf format PreviousCite this article as: Block HE, Steele MA (2014) Spatial variation in selective mortality on larval traits in the coral reef fish Chromis viridis. Mar Ecol Prog Ser 509:303-308. https://doi.org/10.3354/meps10859 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 509. Online publication date: August 27, 2014 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2014 Inter-Research.