The importance of genomic variation for biodiversity, ecosystems and people.

The 2019 United Nations Global assessment report on biodiversity and ecosystem services estimated that approximately 1 million species are at risk of extinction. This primarily human-driven loss of biodiversity has unprecedented negative consequences for ecosystems and people. Classic and emerging approaches in genetics and genomics have the potential to dramatically improve these outcomes. In particular, the study of interactions among genetic loci within and between species will play a critical role in understanding the adaptive potential of species and communities, and hence their direct and indirect effects on biodiversity, ecosystems and people. We explore these population and community genomic contexts in the hope of finding solutions for maintaining and improving ecosystem services and nature's contributions to people.

Counter-gradient variation in gene expression between fish populations facilitates colonization of low-dissolved oxygen environments.

The role of phenotypic plasticity during colonization remains unclear due to the shifting importance of plasticity across timescales. In the early stages of colonization, plasticity can facilitate persistence in a novel environment; but over evolutionary time, processes such as genetic assimilation may reduce variation in plastic traits such that species with a longer evolutionary history in an environment can show lower levels of plasticity than recent invaders. Therefore, comparing species in the early stages of colonization to long-established species provides a powerful approach for uncovering the role of phenotypic plasticity during different stages of colonization. We compared gene expression between low-dissolved oxygen (DO) and high-DO populations of two cyprinid fish: Enteromius apleurogramma, a species that has undergone a recent range expansion, and E. neumayeri, a long-established native species in the same region. We sampled tissue either immediately after capture from the field or after a 2-week acclimation under high-DO conditions, allowing us to test for both evolved and plastic differences in low-DO vs high-DO populations of each species. We found that most genes showing candidate-evolved differences in gene expression did not overlap with those showing plastic differences in gene expression. However, in the genes that did overlap, there was counter-gradient variation such that plastic and evolved gene expression responses were in opposite directions in both species. Additionally, E. apleurogramma had higher levels of plasticity and evolved divergence in gene expression between field populations. We suggest that the higher level of plasticity and counter-gradient variation may have allowed rapid genetic adaptation in E. apleurogramma and facilitated colonization. This study shows how counter-gradient variation may impact the colonization of divergent oxygen environments.

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.

Dimensionality and Modularity of Adaptive Variation: Divergence in Threespine Stickleback from Diverse Environments.

AbstractPopulations are subjected to diverse environmental conditions that affect fitness and induce evolutionary or plastic responses, resulting in phenotypic divergence. Some authors contend that such divergence is concentrated along a single major axis of trait covariance even if that axis does not lead populations directly toward a fitness optimum. Other authors argue that divergence can occur readily along many phenotype axes at the same time. We use populations of threespine stickleback (Gasterosteus aculeatus) from 14 lakes with contrasting ecological conditions to find some resolution along the continuum between these two extremes. Unlike many previous studies, we included several functional suites of traits (defensive, swimming, trophic) potentially subject to different sources of selection. We find that populations exhibit dimensionality of divergence that is high enough to preclude a history of constraint along a single axis-both for divergence in multivariate mean trait values and for the structure of trait covariances. Dimensionality varied among trait suites and were strongly influenced by the inclusion of specific traits, and integration of trait suites varied between populations. We leverage this variation into new insights about the process of divergence and suggest that similar analyses could increase understanding of other adaptive radiations.

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.

Freshwater fishes maintain multi-trait phenotypic stability across an environmental gradient in aqueous calcium.

Reductions in a limiting nutrient might be expected to necessitate compromises in the functional traits that depend on that nutrient; yet populations existing in locations with low levels of such nutrients often do not show the expected degradation of functional traits. Indeed, logperch (Percina caprodes), pumpkinseed sunfish (Lepomis gibbosus) and yellow perch (Perca flavescens) residing in low-calcium water in the Upper St. Lawrence River were all previously found to maintain levels of scale calcium comparable to those of conspecific populations in high-calcium water. Yet it remains possible that the maintenance of one functional trait (i.e., scale calcium) under nutrient-limited (i.e., low calcium) conditions could come at the expense of maintaining other functional traits that depend on the same nutrient. The present study therefore examines other calcium-dependent traits, specifically skeletal element sizes and bone densities in the same fish species in the same area. Using radiographs of 101 fish from the three species across four locations (two in high-calcium water and two in low-calcium water), this new work documents multi-trait "homeostasis" along the gradient of water calcium. That is, no effect of calcium regime (low-calcium vs. high-calcium) was detected on any of the measured variables. Further, effect sizes for the skeletal traits were very low - lower even than effect sizes previously documented for scale calcium. These results thus show that native fishes maintain phenotypic stability across a suite of functional traits linked to calcium regulation, perhaps pointing to an "organismal-level homeostasis" scenario rather than a "trait-level homeostasis" scenario.

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.

Compiling forty years of guppy research to investigate the factors contributing to (non)parallel evolution.

Examples of parallel evolution have been crucial for our understanding of adaptation via natural selection. However, strong parallelism is not always observed even in seemingly similar environments where natural selection is expected to favour similar phenotypes. Leveraging this variation in parallelism within well-researched study systems can provide insight into the factors that contribute to variation in adaptive responses. Here we analyse the results of 36 studies reporting 446 average trait values in Trinidadian guppies, Poecilia reticulata, from different predation regimes. We examine how the extent of predator-driven phenotypic parallelism is influenced by six factors: sex, trait type, rearing environment, ecological complexity, evolutionary history, and time since colonization. Analyses show that parallel evolution in guppies is highly variable and weak on average, with only 24.7% of the variation among populations being explained by predation regime. Levels of parallelism appeared to be especially weak for colour traits, and parallelism decreased with increasing complexity of evolutionary history (i.e., when estimates of parallelism from populations within a single drainage were compared to estimates of parallelism from populations pooled between two major drainages). Suggestive - but not significant - trends that warrant further research include interactions between the sexes and different trait categories. Quantifying and accounting for these and other sources of variation among evolutionary 'replicates' can be leveraged to better understand the extent to which seemingly similar environments drive parallel and nonparallel aspects of phenotypic divergence.

Resistance and resilience of genetic and phenotypic diversity to "black swan" flood events: A retrospective analysis with historical samples of guppies.

Rare extreme "black swan" disturbances can impact ecosystems in many ways, such as destroying habitats, depleting resources, and causing high mortality. In rivers, for instance, exceptional floods that occur infrequently (e.g., so-called "50-year floods") can strongly impact the abundance of fishes and other aquatic organisms. Beyond such ecological effects, these floods could also impact intraspecific diversity by elevating genetic drift or dispersal and by imposing strong selection, which could then influence the population's ability to recover from disturbance. And yet, natural systems might be resistant (show little change) or resilient (show rapid recovery) even to rare extreme events - perhaps as a result of selection due to past events. We considered these possibilities in two rivers where native guppies experienced two extreme floods - one in 2005 and another in 2016. For each river, we selected four sites and used archived "historical" samples to compare levels of genetic and phenotypic diversity before vs. after floods. Genetic diversity was represented by 33 neutral microsatellite markers, and phenotypic diversity was represented by body length and male melanic (black) colour. We found that genetic diversity and population structure was mostly "resistant" to even these extreme floods; whereas the larger impacts on phenotypic diversity were short-lived, suggesting additional "resilience". We discuss the determinants of these two outcomes for guppies facing floods, and then consider the general implications for the resistance and resilience of intraspecific variation to black swan disturbances.

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.

Human influences on the strength of phenotypic selection.

Human activities are driving rapid phenotypic change in many species, with harvesting considered to be a particularly potent evolutionary force. We hypothesized that faster evolutionary change in human-disturbed populations could be caused by a strengthening of phenotypic selection, for example, if human disturbances trigger maladaptation and/or increase the opportunity for selection. We tested this hypothesis by synthesizing 1,366 phenotypic selection coefficients from 37 species exposed to various anthropogenic disturbances, including harvest. We used a paired design that only included studies measuring selection on the same traits in both human-disturbed and control (not obviously human-disturbed "natural") populations. Surprisingly, this meta-analysis did not reveal stronger selection in human-disturbed environments; in fact, we even found some evidence that human disturbances might slightly reduce selection strength. The only clear exceptions were two fisheries showing very strong harvest selection. On closer inspection, we discovered that many disturbances weakened selection by increasing absolute fitness and by decreasing the opportunity for selection-thus explaining what initially seemed a counterintuitive result. We discuss how human disturbances can sometimes weaken rather than strengthen selection, and why measuring the total effect of disturbances on selection is exceedingly difficult. Despite these challenges, documenting human influences on selection can reveal disturbances with particularly strong effects (e.g., fishing), and thus better inform the management of populations exposed to these disturbances.

Repeatability of Adaptive Radiation Depends on Spatial Scale: Regional Versus Global Replicates of Stickleback in Lake Versus Stream Habitats.

The repeatability of adaptive radiation is expected to be scale-dependent, with determinism decreasing as greater spatial separation among "replicates" leads to their increased genetic and ecological independence. Threespine stickleback (Gasterosteus aculeatus) provide an opportunity to test whether this expectation holds for the early stages of adaptive radiation-their diversification in freshwater ecosystems has been replicated many times. To better understand the repeatability of that adaptive radiation, we examined the influence of geographic scale on levels of parallel evolution by quantifying phenotypic and genetic divergence between lake and stream stickleback pairs sampled at regional (Vancouver Island) and global (North America and Europe) scales. We measured phenotypes known to show lake-stream divergence and used reduced representation genome-wide sequencing to estimate genetic divergence. We assessed the scale dependence of parallel evolution by comparing effect sizes from multivariate models and also the direction and magnitude of lake-stream divergence vectors. At the phenotypic level, parallelism was greater at the regional than the global scale. At the genetic level, putative selected loci showed greater lake-stream parallelism at the regional than the global scale. Generally, the level of parallel evolution was low at both scales, except for some key univariate traits. Divergence vectors were often orthogonal, highlighting possible ecological and genetic constraints on parallel evolution at both scales. Overall, our results confirm that the repeatability of adaptive radiation decreases at increasing spatial scales. We suggest that greater environmental heterogeneity at larger scales imposes different selection regimes, thus generating lower repeatability of adaptive radiation at larger spatial scales.

Comparing Adaptive Radiations Across Space, Time, and Taxa.

Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.

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.

Independent lineages in a common environment: the roles of determinism and contingency in shaping the migration timing of even- versus odd-year pink salmon over broad spatial and temporal scales.

Studies of parallel evolution are seldom able to disentangle the influence of cryptic environmental variation from that of evolutionary history; whereas the unique life history of pink salmon (Oncorhynchus gorbuscha) presents an opportunity to do so. All pink salmon mature at age two and die after breeding. Hence, pink salmon bred in even years are completely reproductively isolated from those bred in odd years, even if the two lineages bred in same location. We used time series (mean = 7 years, maximum = 74 years) of paired even- and odd-year populations from 36 rivers spanning over 2000 km to explore parallelism in migration timing, a trait with a strong genetic basis. Migration timing was highly parallel, being determined almost entirely by local environmental differences among rivers. Interestingly, interannual changes in migration timing different somewhat between lineages. Overall, our findings indicate very strong determinism, with only a minor contribution of contingency.

Understanding Maladaptation by Uniting Ecological and Evolutionary Perspectives.

Evolutionary biologists have long trained their sights on adaptation, focusing on the power of natural selection to produce relative fitness advantages while often ignoring changes in absolute fitness. Ecologists generally have taken a different tack, focusing on changes in abundance and ranges that reflect absolute fitness while often ignoring relative fitness. Uniting these perspectives, we articulate various causes of relative and absolute maladaptation and review numerous examples of their occurrence. This review indicates that maladaptation is reasonably common from both perspectives, yet often in contrasting ways. That is, maladaptation can appear strong from a relative fitness perspective, yet populations can be growing in abundance. Conversely, resident individuals can appear locally adapted (relative to nonresident individuals) yet be declining in abundance. Understanding and interpreting these disconnects between relative and absolute maladaptation, as well as the cases of agreement, is increasingly critical in the face of accelerating human-mediated environmental change. We therefore present a framework for studying maladaptation, focusing in particular on the relationship between absolute and relative fitness, thereby drawing together evolutionary and ecological perspectives. The unification of these ecological and evolutionary perspectives has the potential to bring together previously disjunct research areas while addressing key conceptual issues and specific practical problems.

Temporally varying disruptive selection in the medium ground finch (Geospiza fortis).

Disruptive natural selection within populations exploiting different resources is considered to be a major driver of adaptive radiation and the production of biodiversity. Fitness functions, which describe the relationships between trait variation and fitness, can help to illuminate how this disruptive selection leads to population differentiation. However, a single fitness function represents only a particular selection regime over a single specified time period (often a single season or a year), and therefore might not capture longer-term dynamics. Here, we build a series of annual fitness functions that quantify the relationships between phenotype and apparent survival. These functions are based on a 9-year mark-recapture dataset of over 600 medium ground finches (Geospiza fortis) within a population bimodal for beak size. We then relate changes in the shape of these functions to climate variables. We find that disruptive selection between small and large beak morphotypes, as reported previously for 2 years, is present throughout the study period, but that the intensity of this selection varies in association with the harshness of environment. In particular, we find that disruptive selection was strongest when precipitation was high during the dry season of the previous year. Our results shed light on climatic factors associated with disruptive selection in Darwin's finches, and highlight the role of temporally varying fitness functions in modulating the extent of population differentiation.

Sexual dimorphism modifies habitat-associated divergence: Evidence from beach and creek breeding sockeye salmon.

Studies of parallel or convergent evolution (the repeated, independent evolution of similar traits in similar habitats) rarely explicitly quantify the extent of parallelism (i.e. variation in the direction and/or magnitude of divergence) between the sexes; instead, they often investigate both sexes together or exclude one sex. However, differences in male and female patterns of divergence could contribute to overall variation in the extent of parallelism among ecotype pairs, especially in sexually dimorphic traits. Failing to properly attribute such variation could lead to underestimates of the importance of environmental variation in shaping phenotypes. We investigate the extent of parallelism in the body shape of male and female beach and creek spawning sockeye salmon (Oncorhynchus nerka) from two lake systems in western Alaska that were colonized independently after the last ice age. Although both sexes showed some degree of parallelism, patterns of beach-creek body shape divergence vary between the sexes and between lake systems. Phenotypic change vector analyses revealed highly parallel aspects of divergence between males from different lake systems (males from beaches had deeper bodies than males from creeks) but weaker parallelism in females and high parallelism between the sexes in one lake system but not the other. Body shape also had population-specific components, which were mostly, but not entirely, explained by environmental variation in the form of creek depth. Our results highlight the importance of explicitly considering the extent of parallelism between the sexes and environmental variation among sites within habitat types.

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.