Contemporary changes in phenotypic variation, and the potential consequences for eco-evolutionary dynamics.

Most studies assessing rates of phenotypic change focus on population mean trait values, whereas a largely overlooked additional component is changes in population trait variation. Theoretically, eco-evolutionary dynamics mediated by such changes in trait variation could be as important as those mediated by changes in trait means. To date, however, no study has comprehensively summarised how phenotypic variation is changing in contemporary populations. Here, we explore four questions using a large database: How do changes in trait variances compare to changes in trait means? Do different human disturbances have different effects on trait variance? Do different trait types have different effects on changes in trait variance? Do studies that established a genetic basis for trait change show different patterns from those that did not? We find that changes in variation are typically small; yet we also see some very large changes associated with particular disturbances or trait types. We close by interpreting and discussing the implications of our findings in the context of eco-evolutionary studies.

Drivers and Cascading Ecological Consequences of Gambusia affinis Trait Variation.

AbstractPhenotypic trait differences among populations can shape ecological outcomes for communities and ecosystems. However, few studies have mechanistically linked heritable and plastic components of trait variation to generalizable processes of ecology, such as trophic cascades. Here, we assess morphological and behavioral trait variation in nine populations of common garden-reared western mosquitofish (Gambusia affinis) from three distinct ancestral predator environments (three populations per environment), each reared in the presence and absence of predator cues. We then use a pond mesocosm experiment to examine the ecological consequences of mosquitofish trait variation and density variation. Our results show significant among-population trait variation, but this variation was generally unrelated to ancestral predator environment. When traits did vary congruently with respect to ancestral predator environment, this trait variation was driven by gene-by-environment interactions. Variation in several mosquitofish traits altered the cascading effects of mosquitofish on zooplankton and primary producers, but the effect of any given trait was typically weaker than that of density. We note that the relatively stronger ecological effects of density may mask the effects of traits in some systems. Our example here shows that trait variation can be highly noncongruent with respect to a perceived selective agent, phenotypic change is a product of complex interactions between genes and the environment, and numerous interacting phenotypes generate significant but potentially cryptic cascading ecological change.

Inconsistent evolution and growth-survival tradeoffs in Gambusia affinis.

Growth-survival tradeoffs may be a generalizable mechanism influencing trajectories of prey evolution. Here, we investigate evolutionary contributions to growth and survival in western mosquitofish (Gambusia affinis) from 10 populations from high- and low-predation ancestral environments. We assess (i) the degree to which evolutionary components of growth and survival are consistent or inconsistent across populations within ancestral predation environments, and (ii) whether growth and survival trade off at the population level. We measure growth and survival on groups of common-reared mosquitofish in pond mesocosms. We find that evolution of growth is consistent, with fish from low-predation ancestral environments showing higher growth, while the evolution of survival is inconsistent, with significant population-level divergence unrelated to ancestral predation environment. Such inconsistency prevents a growth-survival tradeoff across populations. Thus, the generalizability of contemporary evolution probably depends on local context of evolutionary tradeoffs, and a continued focus on singular selective agents (e.g. predators) without such local context will impede insights into generalizable evolutionary patterns.

The pace of modern life, revisited.

Wild populations must continuously respond to environmental changes or they risk extinction. Those responses can be measured as phenotypic rates of change, which can allow us to predict contemporary adaptive responses, some of which are evolutionary. About two decades ago, a database of phenotypic rates of change in wild populations was compiled. Since then, researchers have used (and expanded) this database to examine phenotypic responses to specific types of human disturbance. Here, we update the database by adding 5675 new estimates of phenotypic change. Using this newer version of the data base, now containing 7338 estimates of phenotypic change, we revisit the conclusions of four published articles. We then synthesize the expanded database to compare rates of change across different types of human disturbance. Analyses of this expanded database suggest that: (i) a small absolute difference in rates of change exists between human disturbed and natural populations, (ii) harvesting by humans results in higher rates of change than other types of disturbance, (iii) introduced populations have increased rates of change, and (iv) body size does not increase through time. Thus, findings from earlier analyses have largely held-up in analyses of our new database that encompass a much larger breadth of species, traits, and human disturbances. Lastly, we use new analyses to explore how various types of human disturbances affect rates of phenotypic change, and we call for this database to serve as a steppingstone for further analyses to understand patterns of contemporary phenotypic change.

The legacy of predator threat shapes prey foraging behaviour.

Predators exert strong selection on prey foraging behaviour such that prey responses may reflect a combination of ancestral effects of predators (genetic and nongenetic transgenerational effects), past individual experience with predators (phenotypic plasticity), and current exposure to predators (behavioural response). However, the importance of these factors in shaping prey foraging behaviour is not well understood. To test the relative effects of ancestry, prior experience, and current exposure, we measured foraging rates and food size preference of different ancestry and exposure groups of Western mosquitofish in the presence and absence of immediate threat from predatory largemouth bass. Our results confirm that mosquitofish had lower foraging rate in the immediate presence of predator threat. Mosquitofish also foraged at a lower rate if they had ancestry with predators, regardless of immediate threat. In contrast, individual prior experience with predators only caused reduced foraging rates in the immediate presence of a predator. This suggests that phenotypic plasticity could carry a lower risk of maladaptive antipredator responses-i.e., reduced food intake-in the complete absence of a predator. Finally, in the presence of a predator, mosquitofish with both ancestry and experience with predators consumed larger, presumably more energetically valuable, food items. Overall, our results show that non-consumptive effects of predators on prey behaviour can persist within and across generations, such that the legacy of past predator exposure-or "the ghost of predation past"-may continue to shape prey behaviour even when predators are no longer around.

Recent warming reduces the reproductive advantage of large size and contributes to evolutionary downsizing in nature.

Body size is a key functional trait that is predicted to decline under warming. Warming is known to cause size declines via phenotypic plasticity, but evolutionary responses of body size to warming are poorly understood. To test for warming-induced evolutionary responses of body size and growth rates, we used populations of mosquitofish (Gambusia affinis) recently established (less than 100 years) from a common source across a strong thermal gradient (19-33°C) created by geothermal springs. Each spring is remarkably stable in temperature and is virtually closed to gene flow from other thermal environments. Field surveys show that with increasing site temperature, body size distributions become smaller and the reproductive advantage of larger body size decreases. After common rearing to reveal recently evolved trait differences, warmer-source populations expressed slowed juvenile growth rates and increased reproductive effort at small sizes. These results are consistent with an adaptive basis of the plastic temperature-size rule, and they suggest that temperature itself can drive the evolution of countergradient variation in growth rates. The rapid evolution of reduced juvenile growth rates and greater reproduction at a small size should contribute to substantial body downsizing in populations, with implications for population dynamics and for ecosystems in a warming world.

Prey adaptation along a competition-defense tradeoff cryptically shifts trophic cascades from density- to trait-mediated.

Trophic cascades have become a dominant paradigm in ecology, yet considerable debate remains about the relative strength of density- (consumptive) and trait-mediated (non-consumptive) effects in trophic cascades. This debate may, in part, be resolved by considering prey experience, which shapes prey traits (through genetic and plastic change) and influences prey survival (and therefore density). Here, we investigate the cascading role of prey experience through the addition of mosquitofish (Gambusia affinis) from predator-experienced or predator-naïve sources to mesocosms containing piscivorous largemouth bass (Micropterus salmoides), zooplankton, and phytoplankton. These two sources were positioned along a competition-defense tradeoff. Results show that predator-naïve mosquitofish suffered higher depredation rates, which drove a density-mediated cascade, whereas predator-experienced mosquitofish exhibited higher survival but fed less, which drove a trait-mediated cascade. Both cascades were similar in strength, leading to indistinguishable top-down effects on lower trophic levels. Therefore, the accumulation of prey experience with predators can cryptically shift cascade mechanisms from density- to trait-mediated.

Eco-evolutionary feedbacks link prey adaptation to predator performance.

Eco-evolutionary feedbacks may determine the outcome of predator-prey interactions in nature, but little work has been done to quantify the feedback effect of short-term prey adaptation on predator performance. We tested the effects of prey availability and recent (less than 100 years) prey adaptation on the feeding and growth rate of largemouth bass (Micropterus salmoides), foraging on western mosquitofish (Gambusia affinis). Field surveys showed higher densities and larger average body sizes of mosquitofish in recently introduced populations without bass. Over a six-week mesocosm experiment, bass were presented with either a high or low availability of mosquitofish prey from recently established populations either naive or experienced with bass. Naive mosquitofish were larger, less cryptic and more vulnerable to bass predation compared to their experienced counterparts. Bass consumed more naive prey, grew more quickly with naive prey, and grew more quickly per unit biomass of naive prey consumed. The effect of mosquitofish history with the bass on bass growth was similar in magnitude to the effect of mosquitofish availability. In showing that recently derived predation-related prey phenotypes strongly affect predator performance, this study supports the presence of reciprocal predator-prey trait feedbacks in nature.

Replicated Landscape Genomics Identifies Evidence of Local Adaptation to Urbanization in Wood Frogs.

Native species that persist in urban environments may benefit from local adaptation to novel selection factors. We used double-digest restriction-side associated DNA (RAD) sequencing to evaluate shifts in genome-wide genetic diversity and investigate the presence of parallel evolution associated with urban-specific selection factors in wood frogs (Lithobates sylvaticus). Our replicated paired study design involved 12 individuals from each of 4 rural and urban populations to improve our confidence that detected signals of selection are indeed associated with urbanization. Genetic diversity measures were less for urban populations; however, the effect size was small, suggesting little biological consequence. Using an FST outlier approach, we identified 37 of 8344 genotyped single nucleotide polymorphisms with consistent evidence of directional selection across replicates. A genome-wide association study analysis detected modest support for an association between environment type and 12 of the 37 FST outlier loci. Discriminant analysis of principal components using the 37 FST outlier loci produced correct reassignment for 87.5% of rural samples and 93.8% of urban samples. Eighteen of the 37 FST outlier loci mapped to the American bullfrog (Rana [Lithobates] catesbeiana) genome, although none were in coding regions. This evidence of parallel evolution to urban environments provides a powerful example of the ability of urban landscapes to direct evolutionary processes.

Local adaptation reduces the metabolic cost of environmental warming.

Metabolism shapes the ecosystem role of organisms by dictating their energy demand and nutrient recycling potential. Metabolic theory (MTE) predicts consumer metabolic and recycling rates will rise with warming, especially if body size declines, but it ignores potential for adaptation. We measured metabolic and nutrient excretion rates of individuals from populations of a globally invasive fish that colonized sites spanning a wide temperature range (19-37°C) on two continents within the last 100 yr. Fish body size declined across our temperature gradient and MTE predicted large rises in population energy demand and nutrient recycling. However, we found that the allometry and temperature dependency of metabolism varied in a countergradient pattern with local temperature in a way that offset predictions of MTE. Scaling of nutrient excretion was more variable and did not track temperature. Our results suggest that adaptation can reduce the metabolic cost of warming, increasing the prospects for population persistence under extreme warming scenarios.

Population divergence in fish elemental phenotypes associated with trophic phenotypes and lake trophic state.

Studies of ecological stoichiometry typically emphasize the role of interspecific variation in body elemental content and the effects of species or family identity. Recent work suggests substantial variation in body stoichiometry can also exist within species. The importance of this variation will depend on insights into its origins and consequences at various ecological scales, including the distribution of elemental phenotypes across landscapes and their role in nutrient recycling. We investigated whether trophic divergence can produce predictable patterns of elemental phenotypes among populations of an invasive fish, the white perch (Morone americana), and whether elemental phenotypes predict nutrient excretion. White perch populations exhibited a gradient of trophic phenotypes associated with landscape-scale variation in lake trophic state. Perch body chemistry varied considerably among lakes (from 0.09 for % C to 0.31-fold for % P) casting doubt on the assumption of homogenous elemental phenotypes. This variation was correlated with divergence in fish body shape and other trophic traits. Elemental phenotypes covaried (r (2) up to 0.84) with lake trophic state. This covariation likely arose in contemporary time since many of these perch populations were introduced in the last century and the trophic state in many of the lakes has changed in the past few decades. Nutrient excretion varied extensively among populations, but was not readily related to fish body chemistry or lake trophic state. This suggests that predictable patterns of fish body composition can arise quickly through trophic specialization to lake conditions, but such elemental phenotypes may not translate to altered nutrient recycling by fish.

Sex ratio variation shapes the ecological effects of a globally introduced freshwater fish.

Sex ratio and sexual dimorphism have long been of interest in population and evolutionary ecology, but consequences for communities and ecosystems remain untested. Sex ratio could influence ecological conditions whenever sexual dimorphism is associated with ecological dimorphism in species with strong ecological interactions. We tested for ecological implications of sex ratio variation in the sexually dimorphic western mosquitofish, Gambusia affinis. This species causes strong pelagic trophic cascades and exhibits substantial variation in adult sex ratios. We found that female-biased populations induced stronger pelagic trophic cascades compared with male-biased populations, causing larger changes to key community and ecosystem responses, including zooplankton abundance, phytoplankton abundance, productivity, pH and temperature. The magnitude of such effects indicates that sex ratio is important for mediating the ecological role of mosquitofish. Because both sex ratio variation and sexual dimorphism are common features of natural populations, our findings should encourage broader consideration of the ecological significance of sex ratio variation in nature, including the relative contributions of various sexually dimorphic traits to these effects.

Plumage microorganism communities of tidal marsh sparrows.

Microorganism communities can shape host phenotype evolution but are often comprised of thousands of taxa with varied impact on hosts. Identification of taxa influencing host evolution relies on first describing microorganism communities and acquisition routes. Keratinolytic (keratin-degrading) microorganisms are hypothesized to be abundant in saltmarsh sediments and to contribute to plumage evolution in saltmarsh-adapted sparrows. Metabarcoding was used to describe plumage bacterial (16S rRNA) and fungal (ITS) communities in three sparrow species endemic to North America's Atlantic coast saltmarshes. Results describe limited within-species variability and moderate host species-level patterns in microorganism diversity and community composition. A small percentage of overall microorganism diversity was comprised of potentially keratinolytic microorganisms, warranting further functional studies. Distinctions between plumage and saltmarsh sediment bacteria, but not fungal, communities were detected, suggesting multiple bacterial acquisition routes and/or vertebrate host specialization. This research lays groundwork for future testing of causal links between microorganisms and avian host evolution.

Human predators outpace other agents of trait change in the wild.

The observable traits of wild populations are continually shaped and reshaped by the environment and numerous agents of natural selection, including predators. In stark contrast with most predators, humans now typically exploit high proportions of prey populations and target large, reproductive-aged adults. Consequently, organisms subject to consistent and strong 'harvest selection' by fishers, hunters, and plant harvesters may be expected to show particularly rapid and dramatic changes in phenotype. However, a comparison of the rate at which phenotypic changes in exploited taxa occurs relative to other systems has never been undertaken. Here, we show that average phenotypic changes in 40 human-harvested systems are much more rapid than changes reported in studies examining not only natural (n = 20 systems) but also other human-driven (n = 25 systems) perturbations in the wild, outpacing them by >300% and 50%, respectively. Accordingly, harvested organisms show some of the most abrupt trait changes ever observed in wild populations, providing a new appreciation for how fast phenotypes are capable of changing. These changes, which include average declines of almost 20% in size-related traits and shifts in life history traits of nearly 25%, are most rapid in commercially exploited systems and, thus, have profound conservation and economic implications. Specifically, the widespread potential for transitively rapid and large effects on size- or life history-mediated ecological dynamics might imperil populations, industries, and ecosystems.

Environmental DNA detects Spawning Habitat of an ephemeral migrant fish (Anadromous Rainbow Smelt: Osmerus mordax).

BACKGROUND: Anadromous rainbow smelt (Osmerus mordax) have experienced a large range reduction in recent decades and the status of remnant spawning populations is poorly known in Maine, where these fish have significant ecological, cultural, and commercial relevance. Defining the remnant range of anadromous smelt is more difficult than for many declining fish species because adults are only ephemerally present while spawning in small coastal streams at night during spring runoff periods when traditional assessments can be unreliable or even hazardous. We hypothesized that eDNA might facilitate improved survey efforts to define smelt spawning habitat, but that detection could also face challenges from adult eDNA quickly flushing out of these small stream systems. We combined daytime eDNA sampling with nighttime fyke netting to ascertain a potential window of eDNA detection before conducting eDNA surveys in four streams of varying abundance. Hierarchical occupancy modeling was in turn employed to estimate eDNA encounter probabilities relative to numbers of sampling events (date), samples within events, and qPCR replicates within samples. RESULTS: Results from the combined eDNA and fyke net study indicated eDNA was detectable over an extended period, culminating approximately 8-13 days following peak spawning, suggesting developing smelt larvae might be the primary source of eDNA. Subsequently, smelt eDNA was readily detected in eDNA surveys of four streams, particularly following remediation of PCR inhibitors. Hierarchical occupancy modeling confirmed our surveys had high empirical detection for most sites, and that future surveys employing at least three sampling events, three samples per event, and six qPCR replicates can afford greater than 90% combined detection capability in low abundance systems. CONCLUSIONS: These results demonstrate that relatively modest eDNA sampling effort has high capacity to detect this ephemerally present species of concern at low to moderate abundances. As such, smelt eDNA detection could improve range mapping by providing longer survey windows, safer sampling conditions, and lower field effort in low density systems, than afforded by existing visual and netting approaches.

Meta-analysis: Congruence of genomic and phenotypic differentiation across diverse natural study systems.

Linking genotype to phenotype is a primary goal for understanding the genomic underpinnings of evolution. However, little work has explored whether patterns of linked genomic and phenotypic differentiation are congruent across natural study systems and traits. Here, we investigate such patterns with a meta-analysis of studies examining population-level differentiation at subsets of loci and traits putatively responding to divergent selection. We show that across the 31 studies (88 natural population-level comparisons) we examined, there was a moderate (R 2 = 0.39) relationship between genomic differentiation (F ST ) and phenotypic differentiation (P ST ) for loci and traits putatively under selection. This quantitative relationship between P ST and F ST for loci under selection in diverse taxa provides broad context and cross-system predictions for genomic and phenotypic adaptation by natural selection in natural populations. This context may eventually allow for more precise ideas of what constitutes "strong" differentiation, predictions about the effect size of loci, comparisons of taxa evolving in nonparallel ways, and more. On the other hand, links between P ST and F ST within studies were very weak, suggesting that much work remains in linking genomic differentiation to phenotypic differentiation at specific phenotypes. We suggest that linking genotypes to specific phenotypes can be improved by correlating genomic and phenotypic differentiation across a spectrum of diverging populations within a taxon and including wide coverage of both genomes and phenomes.

Phenotypic plasticity and population viability: the importance of environmental predictability.

Phenotypic plasticity plays a key role in modulating how environmental variation influences population dynamics, but we have only rudimentary understanding of how plasticity interacts with the magnitude and predictability of environmental variation to affect population dynamics and persistence. We developed a stochastic individual-based model, in which phenotypes could respond to a temporally fluctuating environmental cue and fitness depended on the match between the phenotype and a randomly fluctuating trait optimum, to assess the absolute fitness and population dynamic consequences of plasticity under different levels of environmental stochasticity and cue reliability. When cue and optimum were tightly correlated, plasticity buffered absolute fitness from environmental variability, and population size remained high and relatively invariant. In contrast, when this correlation weakened and environmental variability was high, strong plasticity reduced population size, and populations with excessively strong plasticity had substantially greater extinction probability. Given that environments might become more variable and unpredictable in the future owing to anthropogenic influences, reaction norms that evolved under historic selective regimes could imperil populations in novel or changing environmental contexts. We suggest that demographic models (e.g. population viability analyses) would benefit from a more explicit consideration of how phenotypic plasticity influences population responses to environmental change.

Adaptive changes in life history and survival following a new guppy introduction.

Numerous studies of wild populations have shown that phenotypic traits can change adaptively on short timescales, but very few studies have considered coincident changes in major fitness components. We here examine adaptive changes in life-history traits and survival rates for wild guppies introduced into new environments. Female life-history traits in the derived (Damier River) populations diverged from the ancestral (Yarra River) population, as a result of adaptation to predation regime (high vs. low) and other aspects of the local river. Moreover, some components of the derived Damier populations, particularly juveniles, now show higher survival in the Damier than do contemporary representatives from the ancestral Yarra population. These results suggest that adaptive change can improve survival rates after fewer than 10 years (fewer than 30 guppy generations) in a new environment.

Landscape genetics reveals unique and shared effects of urbanization for two sympatric pool-breeding amphibians.

Metapopulation-structured species can be negatively affected when landscape fragmentation impairs connectivity. We investigated the effects of urbanization on genetic diversity and gene flow for two sympatric amphibian species, spotted salamanders (Ambystoma maculatum) and wood frogs (Lithobates sylvaticus), across a large (>35,000 km2) landscape in Maine, USA, containing numerous natural and anthropogenic gradients. Isolation-by-distance (IBD) patterns differed between the species. Spotted salamanders showed a linear and relatively high variance relationship between genetic and geographic distances (r = .057, p < .001), whereas wood frogs exhibited a strongly nonlinear and lower variance relationship (r = 0.429, p < .001). Scale dependence analysis of IBD found gene flow has its most predictable influence (strongest IBD correlations) at distances up to 9 km for spotted salamanders and up to 6 km for wood frogs. Estimated effective migration surfaces revealed contrasting patterns of high and low genetic diversity and gene flow between the two species. Population isolation, quantified as the mean IBD residuals for each population, was associated with local urbanization and less genetic diversity in both species. The influence of geographic proximity and urbanization on population connectivity was further supported by distance-based redundancy analysis and multiple matrix regression with randomization. Resistance surface modeling found interpopulation connectivity to be influenced by developed land cover, light roads, interstates, and topography for both species, plus secondary roads and rivers for wood frogs. Our results highlight the influence of anthropogenic landscape features within the context of natural features and broad spatial genetic patterns, in turn supporting the premise that while urbanization significantly restricts interpopulation connectivity for wood frogs and spotted salamanders, specific landscape elements have unique effects on these two sympatric species.

Eco-Evolutionary Dynamics of Sexual Dimorphism.

Sexual dimorphism is widespread, but we have a limited understanding of its significance for communities and ecosystems. Several new experiments demonstrate that sexual dimorphism can have far-reaching ecological effects. These results suggest that sexual dimorphism and sexual selection are potent, but largely overlooked components of eco-evolutionary dynamics.