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.

Genetic divergence and one-way gene flow influence contemporary evolution and ecology of a partially migratory fish.

Recent work has revealed the importance of contemporary evolution in shaping ecological outcomes. In particular, rapid evolutionary divergence between populations has been shown to impact the ecology of populations, communities, and ecosystems. While studies have focused largely on the role of adaptive divergence in generating ecologically important variation among populations, much less is known about the role of gene flow in shaping ecological outcomes. After divergence, populations may continue to interact through gene flow, which may influence evolutionary and ecological processes. Here, we investigate the role of gene flow in shaping the contemporary evolution and ecology of recently diverged populations of anadromous steelhead and resident rainbow trout (Oncorhynchus mykiss). Results show that resident rainbow trout introduced above waterfalls have diverged evolutionarily from downstream anadromous steelhead, which were the source of introductions. However, the movement of fish from above to below the waterfalls has facilitated gene flow, which has reshaped genetic and phenotypic variation in the anadromous source population. In particular, gene flow has led to an increased frequency of residency, which in turn has altered population density, size structure, and sex ratio. This result establishes gene flow as a contemporary evolutionary process that can have important ecological outcomes. From a management perspective, anadromous steelhead are generally regarded as a higher conservation priority than resident rainbow trout, even when found within the same watershed. Our results show that anadromous and resident O. mykiss populations may be connected via gene flow, with important ecological consequences. Such eco-evolutionary processes should be considered when managing recently diverged populations connected by gene flow.

Intraspecific variation in a predator changes intertidal community through effects on a foundation species.

Intraspecific variation is an important form of biodiversity that can alter community and ecosystem properties. Recent work demonstrates the community effects of intraspecific variation in predators via altering prey communities and in foundation species via shaping habitat attributes. However, tests of the community effects of intraspecific trait variation in predators acting on foundation species are lacking despite the fact that consumption of foundation species can have strong community effects by shaping habitat structure. Here, we tested the hypothesis that intraspecific foraging differences among populations of mussel-drilling dogwhelk predators (Nucella) differentially alter intertidal communities through effects on foundational mussels. We conducted a 9-month field experiment where we exposed intertidal mussel bed communities to predation from three Nucella populations that exhibit differences in size-selectivity and consumption time for mussel prey. At the end of the experiment, we measured mussel bed structure, species diversity, and community composition. While exposure to Nucella originating from different populations did not significantly alter overall community diversity, we found that differences in Nucella mussel selectivity significantly altered foundational mussel bed structure, which in turn altered the biomass of shore crabs and periwinkle snails. Our study extends the emerging paradigm of the ecological importance of intraspecific variation to include the effects of intraspecific variation on predators of foundation species.

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.

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.

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.

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.

Predation landscapes influence migratory prey ecology and evolution.

Migratory prey experience spatially variable predation across their life cycle. They face unique challenges in navigating this predation landscape, which affects their perception of risk, antipredator responses, and resulting mortality. Variable and unfamiliar predator cues during migration can limit accurate perception of risk and migrants often rely on social information and learning to compensate. The energetic demands of migration constrain antipredator responses, often through context-dependent patterns. While migration can increase mortality, migrants employ diverse strategies to balance risks and rewards, including life history and antipredator responses. Humans interact frequently with migratory prey across space and alter both mortality risk and antipredator responses, which can scale up to affect migratory populations and should be considered in conservation and management.

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.

Conserving intraspecific variation for nature's contributions to people.

The rapid loss of intraspecific variation is a hidden biodiversity crisis. Intraspecific variation, which includes the genomic and phenotypic diversity found within and among populations, is threatened by local extinctions, abundance declines, and anthropogenic selection. However, biodiversity assessments often fail to highlight this loss of diversity within species. We review the literature on how intraspecific variation supports critical ecological functions and nature's contributions to people (NCP). Results show that the main categories of NCP (material, non-material, and regulating) are supported by intraspecific variation. We highlight new strategies that are needed to further explore these connections and to make explicit the value of intraspecific variation for NCP. These strategies will require collaboration with local and Indigenous groups who possess critical knowledge on the relationships between intraspecific variation and ecosystem function. New genomic methods provide a promising set of tools to uncover hidden variation. Urgent action is needed to document, conserve, and restore the intraspecific variation that supports nature and people. Thus, we propose that the maintenance and restoration of intraspecific variation should be raised to a major global conservation objective.

Socio-eco-evolutionary dynamics in cities.

Cities are uniquely complex systems regulated by interactions and feedbacks between nature and human society. Characteristics of human society-including culture, economics, technology and politics-underlie social patterns and activity, creating a heterogeneous environment that can influence and be influenced by both ecological and evolutionary processes. Increasing research on urban ecology and evolutionary biology has coincided with growing interest in eco-evolutionary dynamics, which encompasses the interactions and reciprocal feedbacks between evolution and ecology. Research on both urban evolutionary biology and eco-evolutionary dynamics frequently focuses on contemporary evolution of species that have potentially substantial ecological-and even social-significance. Still, little work fully integrates urban evolutionary biology and eco-evolutionary dynamics, and rarely do researchers in either of these fields fully consider the role of human social patterns and processes. Because cities are fundamentally regulated by human activities, are inherently interconnected and are frequently undergoing social and economic transformation, they represent an opportunity for ecologists and evolutionary biologists to study urban "socio-eco-evolutionary dynamics." Through this new framework, we encourage researchers of urban ecology and evolution to fully integrate human social drivers and feedbacks to increase understanding and conservation of ecosystems, their functions and their contributions to people within and outside cities.

A century of intermittent eco-evolutionary feedbacks resulted in novel trait combinations in invasive Great Lakes alewives (Alosa pseudoharengus).

Species introductions provide opportunities to quantify rates and patterns of evolutionary change in response to novel environments. Alewives (Alosa pseudoharengus) are native to the East Coast of North America where they ascend coastal rivers to spawn in lakes and then return to the ocean. Some populations have become landlocked within the last 350 years and diverged phenotypically from their ancestral marine population. More recently, alewives were introduced to the Laurentian Great Lakes (~150 years ago), but these populations have not been compared to East Coast anadromous and landlocked populations. We quantified 95 years of evolution in foraging traits and overall body shape of Great Lakes alewives and compared patterns of phenotypic evolution of Great Lakes alewives to East Coast anadromous and landlocked populations. Our results suggest that gill raker spacing in Great Lakes alewives has evolved in a dynamic pattern that is consistent with responses to strong but intermittent eco-evolutionary feedbacks with zooplankton size. Following their initial colonization of Lakes Ontario and Michigan, dense alewife populations likely depleted large-bodied zooplankton, which drove a decrease in alewife gill raker spacing. However, the introduction of large, non-native zooplankton to the Great Lakes in later decades resulted in an increase in gill raker spacing, and present-day Great Lakes alewives have gill raker spacing patterns that are similar to the ancestral East Coast anadromous population. Conversely, contemporary Great Lakes alewife populations possess a gape width consistent with East Coast landlocked populations. Body shape showed remarkable parallel evolution with East Coast landlocked populations, likely due to a shared response to the loss of long-distance movement or migrations. Our results suggest the colonization of a new environment and cessation of migration can result in rapid parallel evolution in some traits, but contingency also plays a role, and a dynamic ecosystem can also yield novel trait combinations.

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.

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.

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.

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.

Restoration-mediated secondary contact leads to introgression of alewife ecotypes separated by a colonial-era dam.

Secondary contact may have important implications for ecological and evolutionary processes; however, few studies have tracked the outcomes of secondary contact from its onset in natural ecosystems. We evaluated an anadromous alewife (Alosa pseudoharengus ) reintroduction project in Rogers Lake (Connecticut, USA), which contains a landlocked alewife population that was isolated as a result of colonial-era damming. After access to the ocean was restored, adult anadromous alewife were stocked into the lake. We assessed anadromous juvenile production, the magnitude and direction of introgression, and the potential for competition between ecotypes. We obtained fin clips from all adult alewife stocked into the lake during the restoration and a sample of juveniles produced in the lake two years after the stocking began. We assessed the ancestry of juveniles using categorical assignment and pedigree reconstruction with newly developed microhaplotype genetic markers. Anadromous alewives successfully spawned in the lake and hybridized with the landlocked population. Parentage assignments revealed that male and female anadromous fish contributed equally to juvenile F1 hybrids. The presence of landlocked backcrosses shows that some hybrids were produced within the first two years of secondary contact, matured in the lake, and reproduced. Therefore, introgression appears directional, from anadromous into landlocked, in the lake environment. Differences in estimated abundance of juveniles of different ecotypes in different habitats were also detected, which may reduce competition between ecotypes as the restoration continues. Our results illustrate the utility of restoration projects to study the outcomes of secondary contact in real ecosystems.

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.

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.

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.