Integrating otolith and genetic tools to reveal intraspecific biodiversity in a highly impacted salmon population.

Intraspecific biodiversity is vital for species persistence in an increasingly volatile world. By embracing methods that integrate information at different spatiotemporal scales, we can directly monitor and reconstruct changes in intraspecific biodiversity. Here we combined genetics and otolith biochronologies to describe the genotypic and phenotypic diversity of Chinook salmon (Oncorhynchus tshawytscha) in the Yuba River, California, comparing cohorts that experienced a range of hydroclimatic conditions. Yuba River salmon have been heavily impacted by habitat loss and degradation, and large influxes of unmarked hatchery fish each year have led to concern about introgression and uncertainty around the viability of its wild populations, particularly the rarer spring-run salmon. Otolith strontium isotopes showed that Yuba River origin fish represented, on average, 42% (range 7%-73%) of spawners across six return years (2009-2011, 2018-2020), with large interannual variability. The remainder of adult Chinook salmon in the river were primarily strays from the nearby Feather River hatchery, and since 2018 from the Mokelumne River hatchery. Among the Yuba-origin spawners, on average, 30% (range 14%-50%) exhibited the spring-run genotype. The Yuba-origin fish also displayed a variety of outmigration phenotypes that differed in the timing and size at which they left the Yuba river. Early-migrating fry dominated the returns (mean 59%, range 33%-89%), and their contribution rates were negatively correlated with freshwater flows. It is unlikely that fry survival rates are elevated during droughts, suggesting that this trend reflects disproportionately low survival of larger later migrating parr, smolts, and yearlings along the migratory corridor in drier years. Otolith daily increments indicated generally faster growth rates in non-natal habitats, emphasizing the importance of continuing upstream restoration efforts to improve in-river growing conditions. Together, these findings show that, despite a long history of habitat degradation and hatchery introgression, the Yuba River maintains intraspecific biodiversity that should be taken into account in future management, restoration, and reintroduction plans. The finding that genotypic spring-run are reproducing, surviving, and returning to the Yuba River every year suggests that re-establishment of an independent population is possible, although hatchery-wild interactions would need to be carefully considered. Integrating methods is critical to monitor changes in key genetic, physiological, and behavioral traits to assess population viability and resilience.

Evolutionary origins for ecological patterns in space.

Historically, many biologists assumed that evolution and ecology acted independently because evolution occurred over distances too great to influence most ecological patterns. Today, evidence indicates that evolution can operate over a range of spatial scales, including fine spatial scales. Thus, evolutionary divergence across space might frequently interact with the mechanisms that also determine spatial ecological patterns. Here, we synthesize insights from 500 eco-evolutionary studies and develop a predictive framework that seeks to understand whether and when evolution amplifies, dampens, or creates ecological patterns. We demonstrate that local adaptation can alter everything from spatial variation in population abundances to ecosystem properties. We uncover 14 mechanisms that can mediate the outcome of evolution on spatial ecological patterns. Sometimes, evolution amplifies environmental variation, especially when selection enhances resource uptake or patch selection. The local evolution of foundation or keystone species can create ecological patterns where none existed originally. However, most often, we find that evolution dampens existing environmental gradients, because local adaptation evens out fitness across environments and thus counteracts the variation in associated ecological patterns. Consequently, evolution generally smooths out the underlying heterogeneity in nature, making the world appear less ragged than it would be in the absence of evolution. We end by highlighting the future research needed to inform a fully integrated and predictive biology that accounts for eco-evolutionary interactions in both space and time.

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 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.

Using seasonal genomic changes to understand historical adaptation to new environments: Parallel selection on stickleback in highly-variable estuaries.

Parallel evolution is considered strong evidence for natural selection. However, few studies have investigated the process of parallel selection as it plays out in real time. The common approach is to study historical signatures of selection in populations already well adapted to different environments. Here, to document selection under natural conditions, we study six populations of threespine stickleback (Gasterosteus aculeatus) inhabiting bar-built estuaries that undergo seasonal cycles of environmental changes. Estuaries are periodically isolated from the ocean due to sandbar formation during dry summer months, with concurrent environmental shifts that resemble the long-term changes associated with postglacial colonization of freshwater habitats by marine populations. We used pooled whole-genome sequencing to track seasonal allele frequency changes in six of these populations and search for signatures of natural selection. We found consistent changes in allele frequency across estuaries, suggesting a potential role for parallel selection. Functional enrichment among candidate genes included transmembrane ion transport and calcium binding, which are important for osmoregulation and ion balance. The genomic changes that occur in threespine stickleback from bar-built estuaries could provide a glimpse into the early stages of adaptation that have occurred in many historical marine to freshwater transitions.

Shade affects magnitude and tactics of juvenile Chinook salmon antipredator behavior in the migration corridor.

Environmental conditions strongly affect antipredator behaviors; however, it is less known how migrating prey adjust antipredator behavior in migration corridors, in part, because active migrants are difficult to observe and study. Migrants are vulnerable and encounter many predators in the corridor, and their propensity to travel towards their destination ties antipredator behavior with movement. We evaluated how environmental risk cues in the migration corridor including in-water habitat structure (present, absent) and overhead shade (sun, shade), and salmon origin (hatchery, wild) affected how juvenile Chinook salmon (Oncorhynchus tshawytscha) reacted to a live predator. We measured how salmon react to predation risk as the difference in time to swim downstream through a 9.1-m long field enclosure with or without a live predatory largemouth bass (Micropterus salmoides). Shade significantly modified the reaction to the predator, and it did so in two ways. First, the magnitude of antipredator behavior was larger in shade compared to direct sun, which suggests salmon perceived shade to be a riskier environment than sun. Second, the escape tactic also varied; salmon slowed down to be cautious in shade and sped up in sun. Structure did not significantly affect behavior and hatchery and wild salmon behaved similarly. Our study suggests that environmental risk cues can shape the magnitude and tactics of how migrants react to predation risk and illustrates how these responses relate to movement with potential to scale up and affect migration patterns.

Trophic control changes with season and nutrient loading in lakes.

Experiments have revealed much about top-down and bottom-up control in ecosystems, but manipulative experiments are limited in spatial and temporal scale. To obtain a more nuanced understanding of trophic control over large scales, we explored long-term time-series data from 13 globally distributed lakes and used empirical dynamic modelling to quantify interaction strengths between zooplankton and phytoplankton over time within and across lakes. Across all lakes, top-down effects were associated with nutrients, switching from negative in mesotrophic lakes to positive in oligotrophic lakes. This result suggests that zooplankton nutrient recycling exceeds grazing pressure in nutrient-limited systems. Within individual lakes, results were consistent with a 'seasonal reset' hypothesis in which top-down and bottom-up interactions varied seasonally and were both strongest at the beginning of the growing season. Thus, trophic control is not static, but varies with abiotic conditions - dynamics that only become evident when observing changes over large spatial and temporal scales.

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.

Climate-driven habitat change causes evolution in Threespine Stickleback.

Climate change can shape evolution directly by altering abiotic conditions or indirectly by modifying habitats, yet few studies have investigated the effects of climate-driven habitat change on contemporary evolution. We resampled populations of Threespine Stickleback (Gasterosteus aculeatus) along a latitudinal gradient in California bar-built estuaries to examine their evolution in response to changing climate and habitat. We took advantage of the strong association between stickleback lateral plate phenotypes and Ectodysplasin A (Eda) genotypes to infer changes in allele frequencies over time. Our results show that over time the frequency of low-plated alleles has generally increased and heterozygosity has decreased. Latitudinal patterns in stickleback plate phenotypes suggest that evolution at Eda is a response to climate-driven habitat transformation rather than a direct consequence of climate. As climate change has reduced precipitation and increased temperature and drought, bar-built estuaries have transitioned from lotic (flowing-water) to lentic (still-water) habitats, where the low-plated allele is favoured. The low-plated allele has achieved fixation at the driest, hottest southernmost sites, a trend that is progressing northward with climate change. Climate-driven habitat change is therefore causing a reduction in genetic variation that may hinder future adaptation for populations facing multiple threats.

An escape theory model for directionally moving prey and an experimental test in juvenile Chinook salmon.

Prey evaluate risk and make decisions based on the balance between the costs of predation and those of engaging in antipredator behaviour. Economic escape theory has been valuable in understanding the responses of stationary prey under predation risk; however, current models are not applicable for directionally moving prey. Here we present an extension of existing escape theory that predicts how much predation risk is perceived by directionally moving prey. Perceived risk is measured by the extent antipredator behaviour causes a change in travel speed (the distance to a destination divided by the total time to reach that destination). Cryptic or cautious antipredator behaviour slows travel speed, while prey may also speed up to reduce predator-prey overlap. Next, we applied the sensitization hypothesis to our model, which predicts that prey with more predator experience should engage in more antipredator behaviour, which leads to a larger change in travel speed under predation risk. We then compared the qualitative predictions of our model to the results of a behavioural assay with juvenile Chinook salmon Oncorhynchus tshawytscha that varied in their past predator experience. We timed salmon swimming downstream through a mesh enclosure in the river with and without predator cues present to measure their reaction to a predator. Hatchery salmon had the least predator experience, followed by wild salmon captured upstream (wild-upstream) and wild-salmon captured downstream (wild-downstream). Both wild salmon groups slowed down in response to predator cues, whereas hatchery salmon did not change travel speed. The magnitude of reaction to predator cues by salmon group followed the gradient of previous predator experience, supporting the sensitization hypothesis. Moving animals are conspicuous and vulnerable to predators. Here we provide a novel conceptual framework for understanding how directionally moving prey perceive risk and make antipredator decisions. Our study extends the scope of economic escape theory and improves general understanding of non-lethal effects of predators on moving prey.

Climate shapes population variation in dogwhelk predation on foundational mussels.

Trait variation among populations is important for shaping ecological dynamics. In marine intertidal systems, seawater temperature, low tide emersion temperature, and pH can drive variation in traits and affect species interactions. In western North America, Nucella dogwhelks are intertidal drilling predators of the habitat-forming mussel Mytilus californianus. Nucella exhibit local adaptation, but it is not known to what extent environmental factors and genetic structure contribute to variation in prey selectivity among populations. We surveyed drilled mussels at sites across Oregon and California, USA, and used multiple regression and Mantel tests to test the effects of abiotic factors and Nucella neutral genetic relatedness on the size of mussels drilled across sites. Our results show that Nucella at sites characterized by higher and less variable temperature and pH drilled larger mussels. Warmer temperatures appear to induce faster handling time, and more stable pH conditions may prolong opportunities for active foraging by reducing exposure to repeated stressful conditions. In contrast, there was no significant effect of genetic relatedness on prey size selectivity. Our results emphasize the role of climate in shaping marine predator selectivity on a foundation species. As coastal climates change, predator traits will respond to localized environmental conditions, changing ecological interactions.

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.

Global urban signatures of phenotypic change in animal and plant populations.

Humans challenge the phenotypic, genetic, and cultural makeup of species by affecting the fitness landscapes on which they evolve. Recent studies show that cities might play a major role in contemporary evolution by accelerating phenotypic changes in wildlife, including animals, plants, fungi, and other organisms. Many studies of ecoevolutionary change have focused on anthropogenic drivers, but none of these studies has specifically examined the role that urbanization plays in ecoevolution or explicitly examined its mechanisms. This paper presents evidence on the mechanisms linking urban development patterns to rapid evolutionary changes for species that play important functional roles in communities and ecosystems. Through a metaanalysis of experimental and observational studies reporting more than 1,600 phenotypic changes in species across multiple regions, we ask whether we can discriminate an urban signature of phenotypic change beyond the established natural baselines and other anthropogenic signals. We then assess the relative impact of five types of urban disturbances including habitat modifications, biotic interactions, habitat heterogeneity, novel disturbances, and social interactions. Our study shows a clear urban signal; rates of phenotypic change are greater in urbanizing systems compared with natural and nonurban anthropogenic systems. By explicitly linking urban development to traits that affect ecosystem function, we can map potential ecoevolutionary implications of emerging patterns of urban agglomerations and uncover insights for maintaining key ecosystem functions upon which the sustainability of human well-being depends.

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.

Key transitions in morphological development improve age estimates in white sturgeon Acipenser transmontanus.

We reared white sturgeon Acipenser transmontanus under laboratory conditions and found that a random-forest model containing scute counts and total length predicted age significantly better than total length alone. Scute counts are rapid, inexpensive and non-lethal meristics to gather in the field. This technique could improve age estimates of imperilled sturgeon populations.

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.

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

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

Cross-habitat effects shape the ecosystem consequences of co-invasion by a pelagic and a benthic consumer.

Invasive species can have major impacts on ecosystems, yet little work has addressed the combined effects of multiple invaders that exploit different habitats. Two common invaders in aquatic systems are pelagic fishes and crayfishes. Pelagic-oriented fish effects are typically strong on the pelagic food web, whereas crayfish effects are strong on the benthic food web. Thus, co-invasion may generate strong ecological responses in both habitats. We tested the effects of co-invasion on experimental pond ecosystems using two widespread invasive species, one pelagic (western mosquitofish) and one benthic (red swamp crayfish). As expected, mosquitofish had strong effects on the pelagic food web, reducing the abundance of Daphnia and causing a strong trophic cascade (increase in phytoplankton). Crayfish had strong effects on the benthic food web, reducing the abundance of benthic filamentous algae. Yet, we also found evidence for important cross-habitat effects. Mosquitofish treatments reduced the biomass of benthic filamentous algae, and crayfish treatments increased Daphnia and phytoplankton abundance. Combined effects of mosquitofish and crayfish were primarily positively or negatively additive, and completely offsetting for some responses, including gross primary production (GPP). Though co-invasion did not affect GPP, it strongly shifted primary production from the benthos into the water column. Effects on snail abundance revealed an interaction; snail abundance decreased only in the presence of both invaders. These results suggest that cross-habitat effects of co-invaders may lead to a variety of ecological outcomes; some of which may be unpredictable based on an understanding of each invader alone.

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.