Host environment and local genetic adaptation determine phenotype in parasitic Rhinanthus angustifolius

Plants have a remarkable capacity to adapt to local environmental conditions, which can result in ecotypic differentiation. Patterns of differentiation can, however, also be influenced by the extensive phenotypic plasticity exhibited by many plant species. In this study, we evaluated the distinctness of two putative ecotypes of the parasitic herb Rhinanthus angustifolius. We compared population means of characters commonly used to distinguish between the putative ecotypes after growing individuals of R. angustifolius with a variety of host species in a common garden. Resulting data were also pooled over environments to study how phenotypic plasticity affects the distinctness of ecotypes and individual populations. Except for node number, most of the characters were plastic. The pattern of differentiation was consistent with the existence of two, or possibly three, habitat‐related groups of populations; however, we observed considerable overlap in flowering time and morphological characters after pooling data across host environments. The results show that the complex phenological and morphological variation in R. angustifolius is caused by a combination of genetically determined ecotypic differentiation and plastic responses to the host environment and other factors. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180 , 89–103.     

The relative importance of plasticity versus genetic differentiation in explaining between population differences; a meta‐analysis

Both plasticity and genetic differentiation can contribute to phenotypic differences between populations. Using data on non‐fitness traits from reciprocal transplant studies, we show that approximately 60% of traits exhibit co‐gradient variation whereby genetic differences and plasticity‐induced differences between populations are the same sign. In these cases, plasticity is about twice as important as genetic differentiation in explaining phenotypic divergence. In contrast to fitness traits, the amount of genotype by environment interaction is small. Of the 40% of traits that exhibit counter‐gradient variation the majority seem to be hyperplastic whereby non‐native individuals express phenotypes that exceed those of native individuals. In about 20% of cases plasticity causes non‐native phenotypes to diverge from the native phenotype to a greater extent than if plasticity was absent, consistent with maladaptive plasticity. The degree to which genetic differentiation versus plasticity can explain phenotypic divergence varies a lot between species, but our proxies for motility and migration explain little of this variation.     

Lack of local adaptation of invasive crofton weed (Ageratina adenophora) in different climatic areas of Yunnan Province,China

Aims Crofton weed, with a subtropical origin, has successfully invaded in diverse habitats that belong to different climate zones in Southwest China. We tested whether local adaptation plays an important role in the successful invasion of crofton weed in heterogeneous environments.Methods Five populations from different habitats with an altitude ranging from 678 to 2356 m were selected. Plant height, biomass, seed yield and seed germination capability of these populations were investigated in the field. Greenhouse and reciprocal transplant experiments with the five populations were conducted, and all the above characters were measured and compared among these populations.Important findings Plant height, biomass, seed yield and seed germination rate were each significantly different among the five populations in field. However, there was no difference among these populations in the greenhouse experiment. In the reciprocal transplant experiment, plants from the five populations responded similarly to different habitats in the field, indicating lack of local adaptation. Instead, phenotypic plasticity likely plays a key role in the invasion success of crofton weed in different habitats.     

Genetic and phenotypic population divergence on a microgeographic scale in brown trout

Salmonid populations of many rivers are rapidly declining. One possible explanation is that habitat fragmentation increases genetic drift and reduces the populations' potential to adapt to changing environmental conditions. We measured the genetic and eco-morphological diversity of brown trout (Salmo trutta) in a Swiss stream system, using multivariate statistics and Bayesian clustering. We found large genetic and phenotypic variation within only 40 km of stream length. Eighty-eight percent of all pairwise F(ST) comparisons and 50% of the population comparisons in body shape were significant. High success rates of population assignment tests confirmed the distinctiveness of populations in both genotype and phenotype. Spatial analysis revealed that divergence increased with waterway distance, the number of weirs, and stretches of poor habitat between sampling locations, but effects of isolation-by-distance and habitat fragmentation could not be fully disentangled. Stocking intensity varied between streams but did not appear to erode genetic diversity within populations. A lack of association between phenotypic and genetic divergence points to a role of local adaptation or phenotypically plastic responses to habitat heterogeneity. Indeed, body shape could be largely explained by topographic stream slope, and variation in overall phenotype matched the flow regimes of the respective habitats.     

表型可塑性和局域适应在紫茎泽兰入侵不同海拔生境中的作用

紫茎泽兰是我国危害最严重的外来入侵物种之一,为探讨表型可塑性和局域适应在其入侵中的作用,在高、低海拔的两个样地内,测定了来自云南南部640～2450 m海拔范围的6个种源的紫茎泽兰种群的株高、冠宽、分枝数和高温半致死温度(HSLT).结果表明,在高海拔样地,各种群紫茎泽兰株高、冠宽、分枝数和HSLT(2130 m的哀牢山种群除外)均显著低于在低海拔样地,紫茎泽兰各种群的株高、冠宽和分枝数的可塑性指数(0.881～0.975)均较大,而HSLT的可塑性(0.052～0.200)较小.无论在高还是低海拔样地,紫茎泽兰的株高、冠宽和分枝数在种群间的差异均不显著,而HSLT在种群间的差异达极显著水平,表现出明显的遗传分化,但其在种群间的差异仍小于其在样地间的差异.在高海拔样地,紫茎泽兰各种群的分枝数与种源海拔呈显著正相关;在低海拔样地,紫茎泽兰的HSLT与种源海拔呈显著负相关,表现出明显的局域适应特征.表型可塑性和局域适应均与紫茎泽兰的入侵有关,但前者的作用可能更大.     

Flowering time QTL in natural populations of Arabidopsis thaliana and implications for their adaptive value

The genetic basis of phenotypic traits is of great interest to evolutionary biologists, but their contribution to adaptation in nature is often unknown. To determine the genetic architecture of flowering time in ecologically relevant conditions, we used a recombinant inbred line population created from two locally adapted populations of Arabidopsis thaliana from Sweden and Italy. Using these RILs, we identified flowering time QTL in growth chambers that mimicked the natural temperature and photoperiod variation across the growing season in each native environment. We also compared the genomic locations of flowering time QTL to those of fitness (total fruit number) QTL from a previous three‐year field study. Ten total flowering time QTL were found, and in all cases, the Italy genotype caused early flowering regardless of the conditions. Two QTL were consistent across chamber environments, and these had the largest effects on flowering time. Five of the fitness QTL colocalized with flowering time QTL found in the Italy conditions, and in each case, the local genotype was favoured. In contrast, just two flowering time QTL found in the Sweden conditions colocalized with fitness QTL and in only one case was the local genotype favoured. This implies that flowering time may be more important for adaptation in Italy than Sweden. Two candidate genes (FLC and VIN3) underlying the major flowering time QTL found in the current study are implicated in local adaptation.     

Local adaptation at the range peripheries of Sitka spruce

High‐dispersal rates in heterogeneous environments and historical rapid range expansion can hamper local adaptation; however, we often see clinal variation in high‐dispersal tree species. To understand the mechanisms of the species’ distribution, we investigated local adaptation and adaptive plasticity in a range‐wide context in Sitka spruce, a wind‐pollinated tree species that has recently expanded its range after glaciations. Phenotypic traits were observed using growth chamber experiments that mimicked temperature and photoperiodic regimes from the limits of the species realized niche. Bud phenology exhibited parallel reaction norms among populations; however, putatively adaptive plasticity and strong divergent selection were seen in bud burst and bud set timing respectively. Natural selection appears to have favoured genotypes that maximize growth rate during available frost‐free periods in each environment. We conclude that Sitka spruce has developed local adaptation and adaptive plasticity throughout its range in response to current climatic conditions despite generally high pollen flow and recent range expansion.     

Local adaptation in populations of a Brachionus group plicatilis cryptic species inhabiting three deep crater lakes in Central Mexico

1. Salinity is a strong selective force for many aquatic organisms, affecting both ecological and evolutionary processes. Most of our knowledge on the effects of salinity on rotifers in the Brachionus plicatilis species complex is based mainly on populations from waterbodies that experience broad environmental changes both seasonally and annually. We tested the hypothesis that, despite the supposedly high potential for gene flow among rotifers inhabiting neighbouring environments, constant salinity has promoted local adaptation, genetic population divergence and even cryptic speciation in B. plicatilis complex populations from three deep maar lakes of distinct salinities [1.1, 6.5 and 9.0 g L^?1 total dissolved solids (TDS)] in Central Mexico. 2. To look for local adaptation, we performed common garden experiments to test the effect of different salinities on population density and intrinsic growth rate (r). Then, we evaluated the genetic divergence by sequencing the cytochrome c oxidase subunit I (COI) gene and performed reproductive trials to assess the potential gene flow among the three populations and with other closely related B. plicatilis complex species. 3. We confirmed that the rotifer populations have phenotypic plasticity in tolerance of salinity, but only rotifers from the least saline lake are adapted to low salinity. Among the populations, sequence divergence at COI was very low (just a single haplotype was found), suggesting a persistent founder effect from a relatively recent single colonisation event and a subsequent dispersal from one lake to the others, and a very restricted immigration rate. In the phylogenetic analysis, rotifers from this area of Mexico clustered in the same clade with the middle‐sized species Brachionus ibericus and B. sp. ‘Almenara’. Mexican rotifers showed successful recognition, copulation and formation of hybrids among them, but interpopulation breeding with the Spanish B. ibericus and B. sp. ‘Almenara’ was unsuccessful. 4. We conclude that the B. plicatilis complex populations from these three lakes belong to a new biological species not yet described (presently named B. sp. ‘Mexico’). To our knowledge, this is the first report of local adaptation of a natural B. plicatilis complex population living in freshwater conditions (1.1 g L^?1 TDS).     

Size differentiation in Finnish house sparrows follows Bergmann's rule with evidence of local adaptation

Bergmann's rule predicts that individuals are larger in more poleward populations and that this size gradient has an adaptive basis. Hence, phenotypic divergence in size traits between populations (P_ST) is expected to exceed the level of divergence by drift alone (F_ST). We measured 16 skeletal traits, body mass and wing length in 409 male and 296 female house sparrows Passer domesticus sampled in 12 populations throughout Finland, where the species has its northernmost European distributional margin. Morphometric differentiation across populations (P_ST) was compared with differentiation in 13 microsatellites (F_ST). We find that twelve traits phenotypically diverged more than F_ST in both sexes, and an additional two traits diverged in males. The phenotypic divergence exceeded F_ST in several traits to such a degree that findings were robust also to strong between‐population environmental effects. Divergence was particularly strong in dimensions of the bill, making it a strong candidate for the study of adaptive molecular genetic divergence. Divergent traits increased in size in more northern populations. We conclude that house sparrows show evidence of an adaptive latitudinal size gradient consistent with Bergmann's rule on the modest spatial scale of ca. 600 km.     

Adaptive phenotypic plasticity and local adaptation for temperature tolerance in freshwater zooplankton

Many organisms have geographical distributions extending from the tropics to near polar regions or can experience up to 30°C temperature variation within the lifespan of an individual. Two forms of evolutionary adaptation to such wide ranges in ambient temperatures are frequently discussed: local adaptation and phenotypic plasticity. The freshwater planktonic crustacean Daphnia magna, whose range extends from South Africa to near arctic sites, shows strong phenotypic and genotypic variation in response to temperature. In this study, we use D. magna clones from 22 populations (one clone per population) ranging from latitude 0° (Kenya) to 66° North (White Sea) to explore the contributions of phenotypic plasticity and local adaptation to high temperature tolerance. Temperature tolerance was studied as knockout time (time until immobilization, T_imm) at 37°C in clones acclimatized to either 20°C or 28°C. Acclimatization to 28°C strongly increased T_imm, testifying to adaptive phenotypic plasticity. At the same time, T_imm significantly correlated with average high temperature at the clones’ sites of origin, suggesting local adaptation. As earlier studies have found that haemoglobin expression contributes to temperature tolerance, we also quantified haemoglobin concentration in experimental animals and found that both acclimatization temperature (AccT) and temperature at the site of origin are positively correlated with haemoglobin concentration. Furthermore, Daphnia from warmer climates upregulate haemoglobin much more strongly in response to AccT, suggesting local adaptation for plasticity in haemoglobin expression. Our results show that both local adaptation and phenotypic plasticity contribute to temperature tolerance, and elucidate a possible role of haemoglobin in mediating these effects that differs along a cold–warm gradient.     

Plastic inducible morphologies are not always adaptive: The importance of time delays in a stochastic environment

Summary We present a mathematical model for predicting the expected fitness of phenotypically plastic organisms experiencing a variable environment. We assume that individuals experience two discrete environments probabilistically in time (as a Markov process) and that there are two different phenotypic states, each yielding the highest fitness in one of the two environments. We compare the expected fitness of a phenotypically fixed individual to that of an individual whose phenotype is induced to produce the better phenotype in each environment with a time lag between experiencing a new environment and realization of the new phenotype. Such time lags are common in organisms where phenotypically plastic, inducible traits have been documented. We find that although plasticity is generally adaptive when time lags are short (relative to the time scale of environmental variability), plasticity can be disadvantageous for longer lag times. Asymmetries in environmental change probabilities and/or the relative fitnesses of each phenotype strongly influence whether plasticity is favoured. In contrast to other models, our model does not require costs for plasticity to be disadvantageous; costs affect the results quantitatively, not qualitatively.     

EVOLUTION OF GENERALISTS AND SPECIALISTS IN SPATIALLY HETEROGENEOUS ENVIRONMENTS

Quantitative genetic models are used to investigate the evolution of generalists and specialists in a coarse-grained environment with two habitat types when there are costs attached to being a generalist. The outcomes for soft and hard selection models are qualitatively different. Under soft selection (e.g., for juvenile or male-reproductive traits) the population evolves towards the single peak in the adaptive landscape. At equilibrium, the population mean phenotype is a compromise between the reaction that would be optimal in both habitats and the reaction with the lowest cost. Furthermore, the equilibrium is closer to the optimal phenotype in the most frequent habitat, or the habitat in which selection on the focal trait is stronger. A specialist genotype always has a lower fitness than a generalist, even when the costs are high. In contrast, under hard selection (e.g., for adult or female-reproductive traits) the adaptive landscape can have one, two, or three peaks; a peak represents a population specialized to one habitat, equally adapted to both habitats, or an intermediate. One peak is always found when the reaction with the lowest cost is not much different from the optimal reaction, and this situation is similar to the soft selection case. However, multiple peaks are present when the costs become higher, and the course of evolution is then determined by initial conditions, and the region of attraction of each peak. This implies that the evolution of specialization and phenotypic plasticity may not only depend on selection regimes within habitats, but also on contingent, historical events (migration, mutation). Furthermore, the evolutionary dynamics in changing environments can be widely different for populations under hard and soft selection. Approaches to measure costs in natural and experimental populations are discussed.     

Fine-scale thermal adaptation in a green turtle nesting population

The effect of climate warming on the reproductive success of ectothermic animals is currently a subject of major conservation concern. However, for many threatened species, we still know surprisingly little about the extent of naturally occurring adaptive variation in heat-tolerance. Here, we show that the thermal tolerances of green turtle (Chelonia mydas) embryos in a single, island-breeding population have diverged in response to the contrasting incubation temperatures of nesting beaches just a few kilometres apart. In natural nests and in a common-garden rearing experiment, the offspring of females nesting on a naturally hot (black sand) beach survived better and grew larger at hot incubation temperatures compared with the offspring of females nesting on a cooler (pale sand) beach nearby. These differences were owing to shallower thermal reaction norms in the hot beach population, rather than shifts in thermal optima, and could not be explained by egg-mediated maternal effects. Our results suggest that marine turtle nesting behaviour can drive adaptive differentiation at remarkably fine spatial scales, and have important implications for how we define conservation units for protection. In particular, previous studies may have underestimated the extent of adaptive structuring in marine turtle populations that may significantly affect their capacity to respond to environmental change.     

Parasite local adaptation in a geographic mosaic

A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.     

The selective advantage of reaction norms for environmental tolerance

A tolerance curve defines the dependence of a genotype's fitness on the state of an environmental gradient. It can be characterized by a mode (the genotype's optimal environment) and a width (the breadth of adaptation). It seems possible that one or both of these characters can be modified in an adaptive manner, at least partially, during development. Thus, we extend the theory of environmental tolerance to include reaction norms for the mode and the width of the tolerance curve. We demonstrate that the selective value of such reaction norms increases with increasing spatial heterogeneity and between-generation temporal variation in the environment and with decreasing within-generation temporal variation. Assuming that the maintenance of a high breadth of adaptation is costly, reaction, norms are shown to induce correlated selection for a reduction in this character. Nevertheless, regardless of the magnitude of the reaction norm, there is a nearly one to one relationship between the optimal breadth of adaptation and the within-generation temporal variation perceived by the organism. This suggests that empirical estimates of the breadth of adaptation may provide a useful index of this type of environmental variation from the organism's point of view.     

Maternal effects provide phenotypic adaptation to local environmental conditions

In outcrossing plants, seed dispersal distance is often less than pollen movement. If the scale of environmental heterogeneity within a population is greater than typical seed dispersal distances but less than pollen movement, an individual's environment will be similar to that of its mother but not necessarily its father. Under these conditions, environmental maternal effects may evolve as a source of adaptive plasticity between generations, enhancing offspring fitness in the environment that they are likely to experience. This idea is illustrated using Campanula americana, an herb that grows in understory and light-gap habitats. Estimates of seed dispersal suggest that offspring typically experience the same light environment as their mother. In a field experiment testing the effect of open vs understory maternal light environments, maternal light directly influenced offspring germination rate and season, and indirectly affected germination season by altering maternal flowering time. Results to date indicate that these maternal effects are adaptive; further experimental tests are ongoing. Evaluating maternal environmental effects in an ecological context demonstrates that they may provide phenotypic adaptation to local environmental conditions.     

Phenotype–environment mismatches reduce connectivity in the sea

The connectivity of marine populations is often surprisingly lower than predicted by the dispersal capabilities of propagules alone. Estimates of connectivity, moreover, do not always scale with distance and are sometimes counterintuitive. Population connectivity requires more than just the simple exchange of settlers among populations: it also requires the successful establishment and reproduction of exogenous colonizers. Marine organisms often disperse over large spatial scales, encountering very different environments and suffering extremely high levels of post-colonization mortality. Given the growing evidence that such selection pressures often vary over spatial scales that are much smaller than those of dispersal, we argue that selection will bias survival against exogenous colonizers. We call this selection against exogenous colonizers a phenotype–environment mismatch and argue that phenotype–environment mismatches represent an important barrier to connectivity in the sea. Crucially, these mismatches may operate independently of distance and thereby have the potential to explain the counterintuitive patterns of connectivity often seen in marine environments. We discuss how such mismatches might alter our understanding and management of marine populations.
Ecology Letters (2010) 13: 128–140     

Spatial scale of local adaptation and population genetic structure in a miniature succulent, Argyroderma pearsonii

Explicit understanding of the spatial scale of evolutionary processes is required in order to set targets for their effective conservation. Here, we explore the spatial context of neutral and adaptive divergence in the species-rich Knersvlakte region of South Africa. Specifically, we aimed to assess the importance of erosional drainage basins as spatial units of evolutionary process. We used amplified fragment length polymorphism (AFLP) and reciprocal transplants to investigate genetic differentiation in Argyroderma pearsonii, sampled from sparse and dense quartz habitats within each of three drainage basins. This design allowed assessment of differentiation at two distinct spatial scales; between habitats within basins, and between basins. We found near-perfect concordance between genetic clusters and basin occupancy, suggesting restricted interbasin gene flow. In addition, transplants reveal adaptive divergence between basins on the dense quartz habitat. We have shown that neutral and adaptive differentiation occurs between basins, but not between habitats within basins, suggesting that conservation plans aimed at conserving multiple interconnected drainage basins will capture an important axis of evolutionary process on the Knersvlakte.     

Genomic signatures of local adaptation in the Drosophila immune response

As environments and pathogen landscapes shift, host defenses must evolve to remain effective. Due to this selection pressure, among-species comparisons of genetic sequence data often find immune genes to be among the fastest evolving genes across the genome. The full extent and nature of these immune adaptations, however, remain largely unexplored. In a recent study, we analyzed patterns of selection within distinct components of the Drosophila melanogaster immune pathway. While we found evidence of positive selection within some immune processes, immune genes were not universally characterized by signatures of strong selection. On the contrary, we even found that some immune functions show greater than expected constraint. Overall these results highlight 2 major factors that appear to play an outsize role in determining a gene's evolutionary rate: the type of pathogen the gene targets and the gene's position within the immune network. These results join a growing body of literature that highlight the complexity of immune adaptation. Rather than there being uniformly strong selection across all immune genes, a combination of pathogen-specificity and host genetic constraints appear to play key roles in determining each immune gene's individual evolutionary trajectory.     

The genetic differentiation at quantitative trait loci under local adaptation

Most adaptive traits are controlled by large number of genes that may all together be the targets of selection. Adaptation may thus involve multiple but not necessarily substantial allele frequency changes. This has important consequences for the detection of selected loci and implies that a quantitative genetics framework may be more appropriate than the classical 'selective sweep' paradigm. Preferred methods to detect loci involved in local adaptation are based on the detection of 'outlier' values of the allelic differentiation F(ST) . A quantitative genetics framework is adopted here to review theoretical expectations for how allelic differentiation at quantitative trait loci (F(STQ) ) relates to (i), neutral genetic differentiation (F(ST) ) and (ii), phenotypic differentiation (Q(ST) ). We identify cases where results of outlier-based methods are likely to be poor and where differentiation at selected loci conveys little information regarding local adaptation. A first case is when neutral differentiation is high, so that local adaptation does not necessitate increased differentiation. A second case is when local adaptation is reached via an increased covariance of allelic effects rather than via allele frequency changes, which is more likely under high gene flow when the number of loci is high and selection is recent. The comparison of theoretical predictions with observed data from the literature suggests that polygenic local adaptation involving only faint allele frequency changes are very likely in some species such as forest trees and for climate-related traits. Recent methodological improvements that may alleviate the weakness of F(ST) -based detection methods are presented.