Spatial heterogeneity lowers rather than increases host–parasite specialization

Abiotic environmental heterogeneity can promote the evolution of diverse resource specialists, which in turn may increase the degree of host–parasite specialization. We coevolved Pseudomonas fluorescens and lytic phage ?2 in spatially structured populations, each consisting of two interconnected subpopulations evolving in the same or different nutrient media (homogeneous and heterogeneous environments, respectively). Counter to the normal expectation, host–parasite specialization was significantly lower in heterogeneous compared with homogeneous environments. This result could not be explained by dispersal homogenizing populations, as this would have resulted in the heterogeneous treatments having levels of specialization equal to or greater than that of the homogeneous environments. We argue that selection for costly generalists is greatest when the coevolving species are exposed to diverse environmental conditions and that this can provide an explanation for our results. A simple coevolutionary model of this process suggests that this can be a general mechanism by which environmental heterogeneity can reduce rather than increase host–parasite specialization.     

Is dietary or microhabitat specialization associated with environmental heterogeneity in horned lizards (Phrynosoma)?

Niche breadth is predicted to correlate with environmental heterogeneity, such that generalists will evolve in heterogeneous environments and specialists will evolve in environments that vary less over space and time. We tested the hypothesis that lizards in a heterogeneous environment were generalists compared to lizards in a homogeneous environment. We compared niche breadths of greater short‐horned lizards by quantifying resource selection in terms of two different niche axes, diet (prey items and trophic level), and microhabitat (ground cover and shade cover) between two populations occurring at different elevations. We assessed the heterogeneity of dietary and microhabitat resources within each population's environment by quantifying the availability of prey items, ground cover, and shade cover in each environment. Overall, our results demonstrate that despite differences in resource heterogeneity between elevations, resource selection did not consistently differ between populations. Moreover, environmental heterogeneity was not associated with generalization of resource use. The low‐elevation site had a broader range of available prey items, yet lizards at the high‐elevation site demonstrated more generalization in diet. In contrast, the high‐elevation site had a broader range of available microhabitats, but the lizard populations at both sites were similarly generalized for shade cover selection and were similarly specialized for ground cover selection. Our results demonstrate that environmental heterogeneity of a particular resource does not necessarily predict the degree to which organisms specialize on that resource.     

Effect of migration and environmental heterogeneity on the maintenance of quantitative genetic variation: a simulation study

The paradox of high genetic variation observed in traits under stabilizing selection is a long‐standing problem in evolutionary theory, as mutation rates appear too low to explain observed levels of standing genetic variation under classic models of mutation–selection balance. Spatially or temporally heterogeneous environments can maintain more standing genetic variation within populations than homogeneous environments, but it is unclear whether such conditions can resolve the above discrepancy between theory and observation. Here, we use individual‐based simulations to explore the effect of various types of environmental heterogeneity on the maintenance of genetic variation (V_A) for a quantitative trait under stabilizing selection. We find that V_A is maximized at intermediate migration rates in spatially heterogeneous environments and that the observed patterns are robust to changes in population size. Spatial environmental heterogeneity increased variation by as much as 10‐fold over mutation–selection balance alone, whereas pure temporal environmental heterogeneity increased variance by only 45% at max. Our results show that some combinations of spatial heterogeneity and migration can maintain considerably more variation than mutation–selection balance, potentially reconciling the discrepancy between theoretical predictions and empirical observations. However, given the narrow regions of parameter space required for this effect, this is unlikely to provide a general explanation for the maintenance of variation. Nonetheless, our results suggest that habitat fragmentation may affect the maintenance of V_A and thereby reduce the adaptive capacity of populations.     

Grain of environment explains variation in the strength of genotype × environment interaction

Theory predicts that genetic variation in phenotypic plasticity (genotype × environment interaction or G × E) should be eroded by selection acting across environments. However, it appears that G × E is often maintained under selection, although not universally. This variation in the presence and strength of G × E requires explanation. Here I ask whether the explanation may lie in the grain of the environment at which G × E is expressed. The grain (or grain size) of the environment refers to the scale of environmental heterogeneity relative to generation time – that is, relative to the window of operation of selection – with higher rates of heterogeneity occurring in finer‐grained environments. The hypothesis that the grain of the environment explains variation in the expression of G × E encapsulates variation in the power of selection to shape reaction norms: selection should be able to erode G × E in fine‐grained environments but lose its power as the grain becomes coarser. I survey studies of G × E in sexual traits and demonstrate that the strength of G × E varies with the grain of the environment across which it is expressed, with G × E being stronger in coarser‐grained environments. This result elucidates when G × E is most likely to be sustained in the reaction norms of fitness‐related traits and when its evolutionary consequences will be most pronounced.     

ECOLOGICAL HISTORY AND EVOLUTION IN A NOVEL ENVIRONMENT: HABITAT HETEROGENEITY AND INSECT ADAPTATION TO A NEW HOST PLANT

Environmental heterogeneity has often been implicated in the maintenance of genetic variation. However, previous research has not considered how environmental heterogeneity might affect the rate of adaptation to a novel environment. In this study, I used an insect-plant system to test the hypothesis that heterogeneous environments maintain more genetic variation in fitness components in a novel environment than do uniform environments. To manipulate recent ecological history, replicate populations of the dipteran leafminer Liriomyza trifolii were maintained for 20 generations in one of three treatments: a heterogeneous environment that contained five species of host plant, and two uniform environments that contained either a susceptible chrysanthemum or tomato. The hypothesis that greater genetic variance for survivorship and developmental time on a new host plant (a leafminer-resistant chrysanthemum) would be maintained in the heterogeneous treatment relative to the uniform environments was then tested with a sib-analysis and a natural selection experiment. Populations from the heterogeneous host plant treatment had no greater genetic variance in either larval survivorship or developmental time on the new host than did populations from either of the other treatments. Moreover, the rate of adaptation to the new host did not differ between the ecological history treatments, although the populations from the uniform chrysanthemum treatment had higher mean survivorship throughout the selection experiment. The estimates of the heritability of larval survivorship from the sib-analysis and selection experiment were quite similar. These results imply that ecologically realistic levels of environmental heterogeneity will not necessarily maintain more genetic variance than uniform environments when traits expressed in a particular novel environment are considered.     

Resource diversity promotes among‐individual diet variation,but not genomic diversity,in lake stickleback

Many generalist species consist of specialised individuals that use different resources. This within‐population niche variation can stabilise population and community dynamics. Consequently, ecologists wish to identify environmental settings that promote such variation. Theory predicts that environments with greater resource diversity favour ecological diversity among consumers (via disruptive selection or plasticity). Alternatively, niche variation might be a side‐effect of neutral genomic diversity in larger populations. We tested these alternatives in a metapopulation of threespine stickleback. Stickleback consume benthic and limnetic invertebrates, focusing on the former in small lakes, the latter in large lakes. Intermediate‐sized lakes support generalist stickleback populations using an even mixture of the two prey types, and exhibit greater among‐individual variation in diet and morphology. In contrast, genomic diversity increases with lake size. Thus, phenotypic diversity and neutral genetic polymorphism are decoupled: trophic diversity being greatest in intermediate‐sized lakes with high resource diversity, whereas neutral genetic diversity is greatest in the largest lakes.     

Evolution of resource specialisation in competitive metacommunities

Spatial environmental heterogeneity coupled with dispersal can promote ecological persistence of diverse metacommunities. Does this premise hold when metacommunities evolve? Using a two‐resource competition model, we studied the evolution of resource‐uptake specialisation as a function of resource type (substitutable to essential) and shape of the trade‐off between resource uptake affinities (generalist‐ to specialist‐favouring). In spatially homogeneous environments, evolutionarily stable coexistence of consumers is only possible for sufficiently substitutable resources and specialist‐favouring trade‐offs. Remarkably, these same conditions yield comparatively low diversity in heterogeneous environments, because they promote sympatric evolution of two opposite resource specialists that, together, monopolise the two resources everywhere. Consumer diversity is instead maximised for intermediate trade‐offs and clearly substitutable or clearly essential resources, where evolved metacommunities are characterised by contrasting selection regimes. Taken together, our results present new insights into resource‐competition‐mediated evolutionarily stable diversity in homogeneous and heterogeneous environments, which should be applicable to a wide range of systems.     

NO EFFECT OF ENVIRONMENTAL HETEROGENEITY ON THE MAINTENANCE OF GENETIC VARIATION IN WING SHAPE IN DROSOPHILA MELANOGASTER

Theory suggests that heterogeneous environments should maintain more genetic variation within populations than homogeneous environments, yet experimental evidence for this effect in quantitative traits has been inconsistent. To examine the effect of heterogeneity on quantitative genetic variation, we maintained replicate populations of Drosophila melanogaster under treatments with constant temperatures, temporally variable temperature, or spatially variable temperature with either panmictic or limited migration. Despite observing differences in fitness and divergence in several wing traits between the environments, we did not find any differences in the additive genetic variance for any wing traits among any of the treatments. Although we found an effect of gene flow constraining adaptive divergence between cages in the limited migration treatment, it did not tend to increase within‐population genetic variance relative to any of the other treatments. The lack of any clear and repeatable patterns of response to heterogeneous versus homogeneous environments across several empirical studies suggests that a single general mechanism for the maintenance of standing genetic variation is unlikely; rather, the relative importance of putative mechanisms likely varies considerably from one trait and ecological context to another.     

The effect of population structure on the adaptive radiation of microbial populations evolving in spatially structured environments

Spatial structure is thought to be an important factor influencing the emergence and maintenance of genetic diversity. Previous studies have demonstrated that environmental heterogeneity, provided by spatial structure, leads to adaptive radiation of populations. In the present study, we investigate not only the impact of environmental heterogeneity on adaptive radiation, but also of population fragmentation and niche construction. Replicate populations founded by a single genotype of Escherichia coli were allowed to evolve for 900 generations by serial transfer in either a homogeneous environment, or a spatially structured environment that was either kept intact or destroyed with each daily transfer. Only populations evolving in the structured environment with intact population structure diversified: clones are significantly divergent in sugar catabolism, and show frequency-dependent fitness interactions indicative of stable coexistence. These findings demonstrate an important role for population fragmentation, a consequence of population structure in spatially structured environments, on the diversification of populations.     

Quantitative genetic variance in experimental fly populations evolving with or without environmental heterogeneity

Heterogeneous environments are typically expected to maintain more genetic variation in fitness within populations than homogeneous environments. However, the accuracy of this claim depends on the form of heterogeneity as well as the genetic basis of fitness traits and how similar the assay environment is to the environment of past selection. Here, we measure quantitative genetic (QG) variance for three traits important for fitness using replicated experimental populations of Drosophila melanogaster evolving under four selective regimes: constant salt‐enriched medium (Salt), constant cadmium‐enriched medium (Cad), and two heterogeneous regimes that vary either temporally (Temp) or spatially (Spatial). As theory predicts, we found that Spatial populations tend to harbor more genetic variation than Temp populations or those maintained in a constant environment that is the same as the assay environment. Contrary to expectation, Salt populations tend to have more genetic variation than Cad populations in both assay environments. We discuss the patterns for QG variances across regimes in relation to previously reported data on genome‐wide sequence diversity. For some traits, the QG patterns are similar to the diversity patterns of ecological selected SNPs, whereas the QG patterns for some other traits resembled that of neutral SNPs.     

Diversification in temporally heterogeneous environments: effect of the grain in experimental bacterial populations

Although theory established the necessary conditions for diversification in temporally heterogeneous environments, empirical evidence remains controversial. One possible explanation is the difficulty of designing experiments including the relevant range of temporal grains and the appropriate environmental trade-offs. Here, we experimentally explore the impact of the grain on the diversification of the bacterium Pseudomonas fluorescens SBW25 in a temporally fluctuating environment by including 20 different pairs of environments and four temporal grains. In general, higher levels of diversity were observed at intermediate temporal grains. This resulted in part from the enhanced capacity of disruptive selection to generate negative genotypic correlations in performance at intermediate grains. However, the evolution of reciprocal specialization was an uncommon outcome. Although the temporal heterogeneity is in theory less powerful than the spatial heterogeneity to generate and maintain the diversity, our results show that diversification under temporal heterogeneity is possible provided appropriate environmental grains.     

Environmental heterogeneity,species diversity and co‐existence at different spatial scales

The positive relationship between spatial environmental heterogeneity and species diversity is a widely accepted concept, generally associated with niche limitation. However, niche limitation cannot account for negative heterogeneity–diversity relationships (HDR) revealed in several case studies. Here we explore how HDR varies at different spatial scales and provide novel theories for small‐scale species co‐existence that explain both positive and negative HDR. At large spatial scales of heterogeneity (e.g. landscape level), different communities co‐exist, promoting large regional species pool size and resulting in positive HDR. At smaller scales within communities, species co‐existence can be enhanced by increasing the number of different patches, as predicted by the niche limitation theory, or alternatively, restrained by heterogeneity. We conducted meta‐regressions for experimental and observational HDR studies, and found that negative HDRs are significantly more common at smaller spatial scales. We propose three theories to account for niche limitation at small spatial scales. (1) Microfragmentation theory: with increasing spatial heterogeneity, large homogeneous patches lose area and become isolated, which in turn restrains the establishment of new plant individuals and populations, thus reducing species richness. (2) Heterogeneity confounded by mean: when heterogeneity occurs at spatial scales smaller than the size of individual plants, which forage through the patches, species diversity can be either positively or negatively affected by a change in the mean of an environmental factor. (3) Heterogeneity as a separate niche axis: the ability of species to tolerate heterogeneity at spatial scales smaller than plant size varies, affecting HDR. We conclude that processes other than niche limitation can affect the relationship between heterogeneity and diversity.     

Overlap and partitioning of the ecological and isotopic niches

Recently, it was proposed that stable isotope patterns can be used to quantify the width of the ecological niche of animals. However, the potential effects of habitat use on isotopic patterns of consumers have not been fully explored and consequently isotopic patterns may yield deceptive estimates of niche width. Here, we simulated four different scenarios of a consumer foraging across an isotopically heterogeneous landscape to test the combined effects of habitat and diet selection on the widths of the isotopic niche. We then modeled the actions of a naïve researcher who randomly sampled consumers from the simulated populations, and used these results to assess the overlap and partitioning of the isotopic and the ecological niches when habitat‐derived differences among isotope signatures are not considered. Our results suggest that populations of dietary specialists exhibited broader isotopic niches than populations composed of dietary generalists, and habitat generalists exhibited narrower isotopic niche widths compared with populations of individuals that foraged in specific habitats. The conversion of isotopic niches to ecological niches without knowledge of foraging behavior and habitat‐derived isotopic differences transformed an informative δ‐space into ‘a blurry p‐space’. Therefore, knowledge of habitat‐derived differences in stable isotope values and understanding of habitat use and individual foraging behavior are critical for the correct quantification of the ecological niche.     

Emergence of long‐term balanced polymorphism under cyclic selection of spatially variable magnitude

A fundamental question in evolutionary biology is what promotes genetic variation at nonneutral loci, a major precursor to adaptation in changing environments. In particular, balanced polymorphism under realistic evolutionary models of temporally varying environments in finite natural populations remains to be demonstrated. Here, we propose a novel mechanism of balancing selection under temporally varying fitnesses. Using forward‐in‐time computer simulations and mathematical analysis, we show that cyclic selection that spatially varies in magnitude, such as along an environmental gradient, can lead to elevated levels of nonneutral genetic polymorphism in finite populations. Balanced polymorphism is more likely with an increase in gene flow, magnitude and period of fitness oscillations, and spatial heterogeneity. This polymorphism‐promoting effect is robust to small systematic fitness differences between competing alleles or to random environmental perturbation. Furthermore, we demonstrate analytically that protected polymorphism arises as spatially heterogeneous cyclic fitness oscillations generate a type of storage effect that leads to negative frequency dependent selection. Our findings imply that spatially variable cyclic environments can promote elevated levels of nonneutral genetic variation in natural populations.     

On the experimental evolution of specialization and diversity in heterogeneous environments

Environmental variance can be decomposed into two components: the contrast among patches in the optimal phenotype and the variance in productivity among patches. Both components can influence the outcome of selection in heterogeneous environments. In general genetic diversity within a population should increase as the contrast among patches increases. As the variance in productivity increases, on the other hand, individual niche breadth should decrease since the response to selection becomes dominated by adaptation to the most productive patch. We tested this interpretation of diversity in heterogeneous environments by selecting the bacterium Pseudomonas fluorescens over several hundred generations in pair-wise mixtures of four carbon substrates. We then assessed the response to selection in the mixtures in terms of performance on each component substrate. The results provide general support for this interpretation of the environmental variance and suggest further that competition among genotypes promotes diversification in heterogeneous environments.     

Differential predation on sexes affects colour polymorphism of the isopod Idotea baltica (Pallas)

Variable selection, including spatio-temporal variation, frequency-dependent selection and differential selection due to habitat choice, may maintain polymorphism in heterogeneous environments. We studied predation as a selective agent on colour polymorphism of the aquatic isopod I baltica. Variable predation on this species can arise from at least three sources. First, apostatic selection was studied by testing the formation of preferences on colour morphs in the perch, a common predator of I baltica. Such acquired preferences should induce apostatic selection. While our results indicate some acquired preferences, there was significant heterogeneity in the behaviour of predator individuals. Second, temporal variation in selection can arise due to habitat shift from the green algae juvenile habitat to the bladderwrack adult habitat, and the consequent change in the crypsis of the morphs. Different crypsis between sexes probably promoted high predation mortality among females in the juvenile habitat. The high rate of male mortality during the breeding period, on the other hand, was presumably due to their high mate-searching activity. Third, the sex-dependent habitat choice of I baltica leads to sexual differences in the susceptibility of morphs to predation. Predators preferred the white-spotted morph over the uniform one in males but not in females, supporting the 'dimorphic niche' hypothesis as an explanation of sexual differences in morph frequencies. Finally, no evidence was found that the colouration patterns were under sexual selection. We therefore conclude diat variable predation is the most promising explanation for the maintenance of polymorphism in I. baltica.     

Examining the social landscapes of alternative reproductive strategies

Social environments are inherently dynamic, often changing depending on the frequency and outcomes of conspecific interactions – they can be simultaneously the targets and agents of selection. Understanding how organisms settle in heterogeneous social environments and the effects this has on reproductive success is vital to our understanding of the selective forces at work in wild populations. From an intensive behavioural and ecological study of territoriality in the polymorphic white‐throated sparrow (Zonotrichia albicollis), we demonstrate that males of the two morphs inhabit social niches that correspond to their respective alternative reproductive strategies. By integrating molecular ecology and Geographic Information Systems, we generated continuous, socio‐spatial models of local conspecific density and cuckoldry risk. Our results suggest that the morphs segregate their territories based on socio‐spatial variables, creating a heterogeneous social landscape that matches each behavioural phenotype with a favourable social environment. Specifically, the monogamous tan males tended to settle in low‐density areas that were also low for cuckoldry risk, while the opposite was true for the promiscuous white males. This pattern of socio‐spatial heterogeneity, combined with the social niche partitioning we observed, might act as a social niche polymorphism, and play an important role in maintenance of the alternative reproductive strategies of the white‐throated sparrow. Socio‐spatial factors, similar to those observed in the white‐throated sparrow, may play important roles in the evolution of mating systems in other species, even those with more continuous or cryptic variation.     

FLUCTUATING SELECTION AND THE MAINTENANCE OF INDIVIDUAL AND SEX‐SPECIFIC DIET SPECIALIZATION IN FREE‐LIVING OYSTERCATCHERS

Fluctuating and disruptive selection are important mechanisms for maintaining intrapopulation trait variation. Nonetheless, few field studies quantify selection pressures over long periods and identify what causes them to fluctuate. Diet specialists in oystercatchers differ in short‐term payoffs (intake), but their long‐term payoffs are hypothesized to be condition dependent. We test whether phenotypic selection on diet specialization fluctuates between years due to the frequency of specialists, competitor density, prey abundance, and environmental conditions. Short‐term payoffs proved to be poor predictors of long‐term fitness payoffs of specialization. Sex‐differences in diet specialization were maintained by opposing directional fecundity and viability selection between the sexes. Contrasting other studies, selection on individual diet specialization was neither negative frequency‐ or density‐dependent nor dependent on prey abundance. Notwithstanding, viability selection fluctuated strongly (stabilizing?disruptive) over the 26‐year study period: slightly favoring generalists in most years, but strongly disfavoring generalists in rare harsh winters, suggesting generalists cannot cope with extreme conditions. Although selection fluctuated, mean selection on specialists was weak, which can explain how individual specialization can persist over long periods. Because rare events can dramatically affect long‐term selective landscapes, more care should be taken to match the timescale of evolutionary studies to the temporal variability of critical environmental conditions.     

Microbial generalist or specialist: Intraspecific variation and dormancy potential matter

Microbial generalists and specialists coexist in the soil environment while having distinctive impacts on microbial community dynamics. In microbial ecology, the underlying mechanisms as to why a species is a generalist or a specialist remain ambiguous. Herein, we collected soils across a national scale and identified bacterial generalists and specialists according to niche breadth at the species level (OTU level), and the single-nucleotide differences in each species were measured to investigate intraspecific variation (at zero-radius OTU level). Compared with that of the specialists, the intraspecific variation of the generalists was much higher, which ensured their wider niche breadth and lower variability. The higher asynchrony and different niche preferences of conspecific individuals and the higher dormancy potential within the generalists further contributed to their stability in varying environments. Besides, generalists were less controlled by environmental filtering, which was indicated by the stronger signature of stochastic processes in their assembly, and had higher diversification and transition rates that allowed them to adapt to environmental changes to a greater extent than specialists. Overall, this study provides a new comprehensive understanding of the rules of assembly and the evolutionary roles of bacterial generalists and specialists. It also highlights the importance of intraspecific variation and the dormancy potential in the stability of species.