The alignment between phenotypic plasticity,the major axis of genetic variation and the response to selection

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.     

Evolution in plant populations as a driver of ecological changes in arthropod communities

Heritable variation in traits can have wide-ranging impacts on species interactions, but the effects that ongoing evolution has on the temporal ecological dynamics of communities are not well understood. Here, we identify three conditions that, if experimentally satisfied, support the hypothesis that evolution by natural selection can drive ecological changes in communities. These conditions are: (i) a focal population exhibits genetic variation in a trait(s), (ii) there is measurable directional selection on the trait(s), and (iii) the trait(s) under selection affects variation in a community variable(s). When these conditions are met, we expect evolution by natural selection to cause ecological changes in the community. We tested these conditions in a field experiment examining the interactions between a native plant (Oenothera biennis) and its associated arthropod community (more than 90 spp.). Oenothera biennis exhibited genetic variation in several plant traits and there was directional selection on plant biomass, life-history strategy (annual versus biennial reproduction) and herbivore resistance. Genetically based variation in biomass and life-history strategy consistently affected the abundance of common arthropod species, total arthropod abundance and arthropod species richness. Using two modelling approaches, we show that evolution by natural selection in large O. biennis populations is predicted to cause changes in the abundance of individual arthropod species, increases in the total abundance of arthropods and a decline in the number of arthropod species. In small O. biennis populations, genetic drift is predicted to swamp out the effects of selection, making the evolution of plant populations unpredictable. In short, evolution by natural selection can play an important role in affecting the dynamics of communities, but these effects depend on several ecological factors. The framework presented here is general and can be applied to other systems to examine the community-level effects of ongoing evolution.     

Compensatory dynamics and the stability of phytoplankton biomass during four decades of eutrophication and oligotrophication

The link between compensatory dynamics and regime shifts is not well understood. We analyse a regime shift in phytoplankton in a large lake with respect to: (1) environmental forcing and (2) the type of dynamics (compensatory or synchronous) between phytoplankton groups. The regime shift in phytoplankton was related to gradual changes in nutrient levels, but unrelated to an almost concurrent shift in climatic conditions. The relationship between total phytoplankton biomass and phosphorus concentrations was sigmoid. Trajectories of phytoplankton biomass and community dynamics suggest that eutrophication effects can successfully be reversed when management efforts decrease nutrient loading to a level sufficiently low to overcome community resilience. The regime shift was associated with a loss of biomass compensation and compensatory dynamics among the phytoplankton groups. This suggests that the type of interactions is important for a better understanding of the existence and shape of nonlinear responses of phytoplankton biomass to environmental change.     

The contribution of post-copulatory mechanisms to incipient ecological speciation in sticklebacks

Ecology can play a major role in species diversification. As individuals are adapting to contrasting habitats, reproductive barriers may evolve at multiple levels. While pre-mating barriers have been extensively studied, the evolution of post-mating reproductive isolation during early stages of ecological speciation remains poorly understood. In diverging three-spined stickleback ecotypes from two lakes and two rivers, we observed differences in sperm traits between lake and river males. Interestingly, these differences did not translate into ecotype-specific gamete precedence for sympatric males in competitive in vitro fertilization experiments, potentially owing to antagonistic compensatory effects. However, we observed indirect evidence for impeded development of inter-ecotype zygotes, possibly suggesting an early stage of genetic incompatibility between ecotypes. Our results show that pre-zygotic post-copulatory mechanisms play a minor role during this first stage of ecotype divergence, but suggest that genetic incompatibilities may arise at early stages of ecological speciation.     

Testing limits to adaptation along altitudinal gradients in rainforest Drosophila

Given that evolution can generate rapid and dramatic shifts in the ecological tolerance of a species, what prevents populations adapting to expand into new habitat at the edge of their distributions? Recent population genetic models have focused on the relative costs and benefits of migration between populations. On the one hand, migration may limit adaptive divergence by preventing local populations from matching their local selective optima. On the other hand, migration may also contribute to the genetic variance necessary to allow populations to track these changing optima. Empirical evidence for these contrasting effects of gene flow in natural situations are lacking, largely because it remains difficult to acquire. Here, we develop a way to explore theoretical models by estimating genetic divergence in traits that confer stress resistance along similar ecological gradients in rainforest Drosophila. This approach allows testing for the coupling of clinal divergence with local density, and the effects of genetic variance and the rate of change of the optimum on the response to selection. In support of a swamping effect of migration on phenotypic divergence, our data show no evidence for a cline in stress-related traits where the altitudinal gradient is steep, but significant clinal divergence where it is shallow. However, where clinal divergence is detected, sites showing trait means closer to the presumed local optimum have more genetic variation than sites with trait means distant from their local optimum. This pattern suggests that gene flow also aids a sustained response to selection.     

The interactive effects of competition and predation risk on dispersal in an insect

Dispersal dynamics have significant consequences for ecological and evolutionary processes. Previous work has demonstrated that dispersal can be context-dependent. However, factors affecting dispersal are typically considered in isolation, despite the probability that individuals make dispersal decisions in response to multiple, possibly interacting factors. We examined whether two ecological factors, predation risk and intraspecific competition, have interactive effects on dispersal dynamics. We performed a factorial experiment in mesocosms using backswimmers (Notonecta undulata), flight-capable, semi-aquatic insects. Emigration rates increased with density, and increased with predation risk at intermediate densities; however, predation had minimal effects on emigration at high and low densities. Our results indicate that factorial experiments may be required to understand dispersal dynamics under realistic ecological conditions.     

Shift in a Large River Fish Assemblage: Body-Size and Trophic Structure Dynamics

As the intensity and speed of environmental change increase at both local and global scales it is imperative that we gain a better understanding of the ecological implications of community shifts. While there has been substantial progress toward understanding the drivers and subsequent responses of community change (e.g. lake trophic state), the ecological impacts of food web changes are far less understood. We analyzed Wabash River fish assemblage data collected from 1974-2008, to evaluate temporal variation in body-size structure and functional group composition. Two parameters derived from annual community size-spectra were our major response variables: (1) the regression slope is an index of ecological efficiency and predator-prey biomass ratios, and (2) spectral elevation (regression midpoint height) is a proxy for food web capacity. We detected a large assemblage shift, over at least a seven year period, defined by dramatic changes in abundance (measured as catch-per-unit-effort) of the dominant functional feeding groups among two time periods; from an assemblage dominated by planktivore-omnivores to benthic invertivores. There was a concurrent increase in ecological efficiency (slopes increased over time) following the shift associated with an increase in large-bodied low trophic level fish. Food web capacity remained relatively stable with no clear temporal trends. Thus, increased ecological efficiency occurred simultaneous to a compensatory response that shifted biomass among functional feeding groups.     

Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota

To explain differences in gut microbial communities we must determine how processes regulating microbial community assembly (colonization, persistence) differ among hosts and affect microbiota composition. We surveyed the gut microbiota of threespine stickleback (Gasterosteus aculeatus) from 10 geographically clustered populations and sequenced environmental samples to track potential colonizing microbes and quantify the effects of host environment and genotype. Gut microbiota composition and diversity varied among populations. These among-population differences were associated with multiple covarying ecological variables: habitat type (lake, stream, estuary), lake geomorphology and food- (but not water-) associated microbiota. Fish genotype also covaried with gut microbiota composition; more genetically divergent populations exhibited more divergent gut microbiota. Our results suggest that population level differences in stickleback gut microbiota may depend more on internal sorting processes (host genotype) than on colonization processes (transient environmental effects).     

Genetic architecture of a feeding adaptation: garter snake (Thamnophis) resistance to tetrodotoxin bearing prey

Detailing the genetic basis of adaptive variation in natural populations is a first step towards understanding the process of adaptive evolution, yet few ecologically relevant traits have been characterized at the genetic level in wild populations. Traits that mediate coevolutionary interactions between species are ideal for studying adaptation because of the intensity of selection and the well-characterized ecological context. We have previously described the ecological context, evolutionary history and partial genetic basis of tetrodotoxin (TTX) resistance in garter snakes (Thamnophis). Derived mutations in a voltage-gated sodium channel gene (Na_v1.4) in three garter snake species are associated with resistance to TTX, the lethal neurotoxin found in their newt prey (Taricha). Here we evaluate the contribution of Na_v1.4 alleles to TTX resistance in two of those species from central coastal California. We measured the phenotypes (TTX resistance) and genotypes (Na_v1.4 and microsatellites) in a local sample of Thamnophis atratus and Thamnophis sirtalis. Allelic variation in Na_v1.4 explains 23 per cent of the variation in TTX resistance in T. atratus while variation in a haphazard sample of the genome (neutral microsatellite markers) shows no association with the phenotype. Similarly, allelic variation in Na_v1.4 correlates almost perfectly with TTX resistance in T. sirtalis, but neutral variation does not. These strong correlations suggest that Na_v1.4 is a major effect locus. The simple genetic architecture of TTX resistance in garter snakes may significantly impact the dynamics of phenotypic coevolution. Fixation of a few alleles of major effect in some garter snake populations may have led to the evolution of extreme phenotypes and an ‘escape’ from the arms race with newts.     

Eco-evolutionary feedbacks drive species interactions

In the biosphere, many species live in close proximity and can thus interact in many different ways. Such interactions are dynamic and fall along a continuum between antagonism and cooperation. Because interspecies interactions are the key to understanding biological communities, it is important to know how species interactions arise and evolve. Here, we show that the feedback between ecological and evolutionary processes has a fundamental role in the emergence and dynamics of species interaction. Using a two-species artificial community, we demonstrate that ecological processes and rapid evolution interact to influence the dynamics of the symbiosis between a eukaryote (Saccharomyces cerevisiae) and a bacterium (Rhizobium etli). The simplicity of our experimental design enables an explicit statement of causality. The niche-constructing activities of the fungus were the key ecological process: it allowed the establishment of a commensal relationship that switched to ammensalism and provided the selective conditions necessary for the adaptive evolution of the bacteria. In this latter state, the bacterial population radiates into more than five genotypes that vary with respect to nutrient transport, metabolic strategies and global regulation. Evolutionary diversification of the bacterial populations has strong effects on the community; the nature of interaction subsequently switches from ammensalism to antagonism where bacteria promote yeast extinction. Our results demonstrate the importance of the evolution-to-ecology pathway in the persistence of interactions and the stability of communities. Thus, eco-evolutionary dynamics have the potential to transform the structure and functioning of ecosystems. Our results suggest that these dynamics should be considered to improve our understanding of beneficial and detrimental host–microbe interactions.     

Adaptive genetic variation mediates bottom-up and top-down control in an aquatic ecosystem

Research in eco-evolutionary dynamics and community genetics has demonstrated that variation within a species can have strong impacts on associated communities and ecosystem processes. Yet, these studies have centred around individual focal species and at single trophic levels, ignoring the role of phenotypic variation in multiple taxa within an ecosystem. Given the ubiquitous nature of local adaptation, and thus intraspecific variation, we sought to understand how combinations of intraspecific variation in multiple species within an ecosystem impacts its ecology. Using two species that co-occur and demonstrate adaptation to their natal environments, black cottonwood (Populus trichocarpa) and three-spined stickleback (Gasterosteus aculeatus), we investigated the effects of intraspecific phenotypic variation on both top-down and bottom-up forces using a large-scale aquatic mesocosm experiment. Black cottonwood genotypes exhibit genetic variation in their productivity and consequently their leaf litter subsidies to the aquatic system, which mediates the strength of top-down effects from stickleback on prey abundances. Abundances of four common invertebrate prey species and available phosphorous, the most critically limiting nutrient in freshwater systems, are dictated by the interaction between genetic variation in cottonwood productivity and stickleback morphology. These interactive effects fit with ecological theory on the relationship between productivity and top-down control and are comparable in strength to the effects of predator addition. Our results illustrate that intraspecific variation, which can evolve rapidly, is an under-appreciated driver of community structure and ecosystem function, demonstrating that a multi-trophic perspective is essential to understanding the role of evolution in structuring ecological patterns.     

Standing genetic variation in host preference for mutualist microbial symbionts

Many models of mutualisms show that mutualisms are unstable if hosts lack mechanisms enabling preferential associations with mutualistic symbiotic partners over exploitative partners. Despite the theoretical importance of mutualism-stabilizing mechanisms, we have little empirical evidence to infer their evolutionary dynamics in response to exploitation by non-beneficial partners. Using a model mutualism—the interaction between legumes and nitrogen-fixing soil symbionts—we tested for quantitative genetic variation in plant responses to mutualistic and exploitative symbiotic rhizobia in controlled greenhouse conditions. We found significant broad-sense heritability in a legume host''s preferential association with mutualistic over exploitative symbionts and selection to reduce frequency of associations with exploitative partners. We failed to detect evidence that selection will favour the loss of mutualism-stabilizing mechanisms in the absence of exploitation, as we found no evidence for a fitness cost to the host trait or indirect selection on genetically correlated traits. Our results show that genetic variation in the ability to preferentially reduce associations with an exploitative partner exists within mutualisms and is under selection, indicating that micro-evolutionary responses in mutualism-stabilizing traits in the face of rapidly evolving mutualistic and exploitative symbiotic bacteria can occur in natural host populations.     

Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes

Increasing evidence has emerged for non-random spatial distributions of microbes, but knowledge of the processes that cause variation in microbial assemblage among ecosystems is lacking. For instance, some studies showed that deterministic processes such as habitat specialization are important, while other studies hold that bacterial communities are assembled by stochastic forces. Here we examine the relative influence of deterministic and stochastic processes for bacterial communities from subsurface environments, stream biofilm, lake water, lake sediment and soil using pyrosequencing of the 16S ribosomal RNA gene. We show that there is a general pattern in phylogenetic signal in species ecological niches across recent evolutionary time for all studied habitats, enabling us to infer the influences of community assembly processes from patterns of phylogenetic turnover in community composition. The phylogenetic dissimilarities among-habitat types were significantly higher than within them, and the communities were clustered according to their original habitat types. For communities within-habitat types, the highest phylogenetic turnover rate through space was observed in subsurface environments, followed by stream biofilm on mountainsides, whereas the sediment assemblages across regional scales showed the lowest turnover rate. Quantifying phylogenetic turnover as the deviation from a null expectation suggested that measured environmental variables imposed strong selection on bacterial communities for nearly all sample groups. For three sample groups, spatial distance reflected unmeasured environmental variables that impose selection, as opposed to spatial isolation. Such characterization of spatial and environmental variables proved essential for proper interpretation of partial Mantel results based on observed beta diversity metrics. In summary, our results clearly indicate a dominant role of deterministic processes on bacterial assemblages and highlight that bacteria show strong habitat associations that have likely emerged through evolutionary adaptation.     

Predators modify the evolutionary response of prey to temperature change

As climate regimes shift in many ecosystems worldwide, evolution may be a critical process allowing persistence in rapidly changing environments. Organisms regularly interact with other species, yet whether climate-mediated evolution can occur in the context of species interactions is not well understood. We tested whether a species interaction could modify evolutionary responses to temperature. We demonstrate that predation pressure by Dipteran larvae (Chaoborus americanus) modified the evolutionary response of a freshwater crustacean (Daphnia pulex) to its thermal environment over approximately seven generations in laboratory conditions. Daphnia kept at 21°C evolved higher population growth rates than those kept at 18°C, but only in those populations that were also reared with predators. Furthermore, predator-mediated selection resulted in the evolution of elevated Daphnia thermal plasticity. This laboratory natural selection experiment demonstrates that biotic interactions can modify evolutionary adaptation to temperature. Understanding the interplay between multiple selective forces can improve predictions of ecological and evolutionary responses of organisms to rapid environmental change.     

Distinct successional patterns and processes of free-living and particle-attached bacterial communities throughout a phytoplankton bloom

1. Understanding the successional patterns of microbial communities during a phytoplankton bloom is crucial for predicting the compositional and functional stability of lake ecosystems in response to the disturbance of a bloom. Previous studies on bacterial communities associated with blooms have rarely studied the dynamics of these communities. The successional patterns of bacterial communities within different micro-habitats (i.e. water column versus particles) and mechanisms that shape these communities that differ in composition and structure remain unclear.
2. We selected a eutrophic urban lake to investigate the succession of bacterial communities during a bloom. We divided the bacterial communities into free-living (FL) and particle-attached (PA) groups based on their different lifestyles. The amplicon-based 16S rRNA gene high-throughput sequencing technology was used to obtain bacterial community composition and phylogenetic structure.
3. Our study showed distinct successional patterns between FL and PA bacterial communities, and the two bacterial lifestyles showed different responses and resilience to the bloom, in terms of diversity and relative abundance of bacterial taxa. Alpha-diversity of the PA bacterial community decreased during the bloom, whereas that of the FL bacterial community increased. More taxa in the FL bacterial community showed resilience after the disturbance than in the PA bacterial community.
4. The influence of phytoplankton blooms on the assembly of the bacterial community can be viewed as niche selection that led to the decrease in the relative importance of stochastic processes in shaping both FL and PA bacterial communities. This study shows the ecological significance of the bacterial community response to bloom events in lakes. It also shows that assembly processes differ for bacterial communities that have different lifestyles in lake ecosystems disturbed by phytoplankton blooms.

     

Environmental fluctuations restrict eco-evolutionary dynamics in predator–prey system

Environmental fluctuations, species interactions and rapid evolution are all predicted to affect community structure and their temporal dynamics. Although the effects of the abiotic environment and prey evolution on ecological community dynamics have been studied separately, these factors can also have interactive effects. Here we used bacteria–ciliate microcosm experiments to test for eco-evolutionary dynamics in fluctuating environments. Specifically, we followed population dynamics and a prey defence trait over time when populations were exposed to regular changes of bottom-up or top-down stressors, or combinations of these. We found that the rate of evolution of a defence trait was significantly lower in fluctuating compared with stable environments, and that the defence trait evolved to lower levels when two environmental stressors changed recurrently. The latter suggests that top-down and bottom-up changes can have additive effects constraining evolutionary response within populations. The differences in evolutionary trajectories are explained by fluctuations in population sizes of the prey and the predator, which continuously alter the supply of mutations in the prey and strength of selection through predation. Thus, it may be necessary to adopt an eco-evolutionary perspective on studies concerning the evolution of traits mediating species interactions.     

Eco‐evolutionary partitioning metrics: assessing the importance of ecological and evolutionary contributions to population and community change

Interest in eco‐evolutionary dynamics is rapidly increasing thanks to ground‐breaking research indicating that evolution can occur rapidly and can alter the outcome of ecological processes. A key challenge in this sub‐discipline is establishing how important the contribution of evolutionary and ecological processes and their interactions are to observed shifts in population and community characteristics. Although a variety of metrics to separate and quantify the effects of evolutionary and ecological contributions to observed trait changes have been used, they often allocate fractions of observed changes to ecology and evolution in different ways. We used a mathematical and numerical comparison of two commonly used frameworks – the Price equation and reaction norms – to reveal that the Price equation cannot partition genetic from non‐genetic trait change within lineages, whereas the reaction norm approach cannot partition among‐ from within‐lineage trait change. We developed a new metric that combines the strengths of both Price‐based and reaction norm metrics, extended all metrics to analyse community change and also incorporated extinction and colonisation of species in these metrics. Depending on whether our new metric is applied to populations or communities, it can correctly separate intraspecific, interspecific, evolutionary, non‐evolutionary and interacting eco‐evolutionary contributions to trait change.     

Nearly a decade‐long repeatable seasonal diversity patterns of bacterioplankton communities in the eutrophic Lake Donghu (Wuhan,China)

Uncovering which environmental factors govern community diversity patterns and how ecological processes drive community turnover are key questions related to understand the community assembly. However, the ecological mechanisms regulating long‐term variations of bacterioplankton communities in lake ecosystems remain poorly understood. Here we present nearly a decade‐long study of bacterioplankton communities from the eutrophic Lake Donghu (Wuhan, China) using 16S rRNA gene amplicon sequencing with MiSeq platform. We found strong repeatable seasonal diversity patterns in terms of both common (detected in more than 50% samples) and dominant (relative abundance >1%) bacterial taxa turnover. Moreover, community composition tracked the seasonal temperature gradient, indicating that temperature is a key environmental factor controlling observed diversity patterns. Total phosphorus also contributed significantly to the seasonal shifts in bacterioplankton composition. However, any spatial pattern of bacterioplankton communities across the main lake areas within season was overwhelmed by their temporal variabilities. Phylogenetic analysis further indicated that 75%–82% of community turnover was governed by homogeneous selection due to consistent environmental conditions within seasons, suggesting that the microbial communities in Lake Donghu are mainly controlled by niche‐based processes. Therefore, dominant niches available within seasons might be occupied by similar combinations of bacterial taxa with modest dispersal rates throughout different lake areas.     

N:P stoichiometric changes via species turnover in arid versus saline desert environments

1. Aridity and salinity have a key role in driving physiological and ecological processes in desert ecosystems. However, how community‐scale foliar nutrients respond to aridity and salinity, and how these responses might vary with community composition along aridity and salinity gradients is unclear. We hypothesize that the response will be a shift in community stoichiometric values resulting from nutrient variability of shared species and unique species (site‐specific species), but little research has addressed the relative contribution of either component.
2. We analyzed the community‐scale stoichiometric response of a desert community of perennial plants along an aridity and salinity transect by focusing on foliar nitrogen (N) and phosphorous (P) concentrations and N:P ratios. After evaluating the shared and unique species variability, we determined their relative contribution to the community stoichiometric response to aridity and salinity, reflected by changes in nonweighted and weighted community‐average values.
3. Community‐scale stoichiometry decreased significantly under aridity and salinity, with significantly consistent changes in nonweighted and weighted community‐average stoichiometry for most shared and unique species measurements. The relative contribution of unique species shifts to the changes in community stoichiometry was greater (15%–77%) than the relative contribution of shared species shifts (7%–45%), excluding the change in weighted P concentration under aridity. Thus, the shifts of unique species amplified the community stoichiometric response to environmental changes.
4. Synthesis. These results highlighted the need for a more in‐depth consideration of shared and unique species variability to understand and predict the effects of environmental change on the stoichiometry of plant communities. Although variation in community stoichiometry can be expected under extreme aridity and salinity conditions, changes of unique species could be a more important driver of the stoichiometric response of plant communities.