Natural selection relentlessly reshapes the genetic and phenotypic composition of populations, yet often adaptations cannot emerge due to excessive migration and gene flow. Nevertheless, in heterogeneous habitats strong selection could temporarily establish significant trait divergence among environmental patches. Here, we show that in Fundulus heteroclitus, a single generation of selection drives significant phenotypic divergence (5-15%) in organismal metabolic rate, cardiac metabolic rate and hypoxia tolerance. This divergence occurs among individuals of the same panmictic population residing in environmentally distinct microhabitats. Phenotypic divergence remains observable following long-term common-gardening and is supported by previous work documenting fine-scale, genetic divergence among microhabitat residents. We show that the magnitude of within-generation trait divergence is on the order of what is commonly observed among more isolated populations that have diverged over multiple generations. Although panmictic reproduction among microhabitat residents erodes trait divergence every generation, strong selection could potentially reestablish it in the next. In heterogeneous habitats, transient, fine-scale divergence could have a considerable impact on eco-evolutionary dynamics. Ignoring its contribution to overall trait variance could limit our ability to define meaningful, evolved divergence.Summary Natural selection can lead to changes in organisms’ traits over time. Typically, these changes occur slowly over multiple generations and over large spatial scales. By studying a wild population of Atlantic killifish, we show that a single generation of natural selection can generate substantial trait variation over short distances. We observe significant differences in several physiological traits among individuals inhabiting distinct ‘microhabitats’ in a patchy salt marsh environment. These differences are unlikely due to physiological acclimation and are best explained by strong, natural selection removing those individuals not suited to a particular microhabitat. Previous studies support natural selection as the most likely explanation, having shown subtle genetic differences among microhabitat residents. Remarkably, the magnitude of trait divergence is on the order of what is typically observed among populations that have diverged over multiple generations and larger spatial scales. Our results highlight the significant contribution of natural selection to trait variation in patchy environments, even over exceptionally short time and small spatial scales.### Competing Interest StatementThe authors have declared no competing interest.

High throughput low-density SNP arrays provide a cost-effective solution for population genetic studies and monitoring of genetic diversity as well as population structure commonly implemented in real time stock assessment of commercially important fish species. However, the application of high throughput SNP arrays for monitoring of invasive species has so far not been implemented. We developed a species-specific SNP array for the invasive comb jelly Mnemiopsis leidyi based on whole genome re-sequencing data. Initially, a total of 1,395 high quality SNPs were identified using stringent filtering criteria. From those, 192 assays were designed and validated, resulting in the final panel of 116 SNPs. Markers were diagnostic between the northern and southern M. leidyi lineages and highly polymorphic to distinguish populations. Despite using a reduced representation of the genome, our SNP panel yielded comparable results to using a whole genome re-sequencing approach (832,323 SNPs), recovering similar values of genetic differentiation between samples and detecting the same clustering groups when performing Structure analyses. The resource presented here provides a cost-effective, high throughput solution for population genetic studies, allowing to routinely genotype large number of individuals. Monitoring of genetic diversity and effective population size estimations in this highly invasive species will allow for the early detection of new introductions from distant source regions or hybridization events. Thereby, this SNP chip represents an important management tool in order to understand invasion dynamics and opens the door for implementing such methods for a wider range of non-indigenous invasive species.

ABSTRACTPhysiology defines individual responses to global climate change and species distributions across environments. Physiological responses are driven by temperature on three time scales: acute, acclimatory and evolutionary. Acutely, passive temperature effects often dictate an expected 2-fold increase in metabolic processes for every 10°C change in temperature (Q10). Yet, these acute responses often are mitigated through acclimation within an individual or evolutionary adaptation within populations over time. Natural selection can influence both responses and often reduces interindividual variation towards an optimum. However, this interindividual physiological variation is not well characterized. Here, we quantified responses to a 16°C temperature difference in six physiological traits across nine thermally distinct Fundulus heteroclitus populations. These traits included whole-animal metabolism (WAM), critical thermal maximum (CTmax) and substrate-specific cardiac metabolism measured in approximately 350 individuals. These traits exhibited high variation among both individuals and populations. Thermal sensitivity (Q10) was determined, specifically as the acclimated Q10, in which individuals were both acclimated and assayed at each temperature. The interindividual variation in Q10 was unexpectedly large: ranging from 0.6 to 5.4 for WAM. Thus, with a 16°C difference, metabolic rates were unchanged in some individuals, while in others they were 15-fold higher. Furthermore, a significant portion of variation was related to habitat temperature. Warmer populations had a significantly lower Q10 for WAM and CTmax after acclimation. These data suggest that individual variation in thermal sensitivity reflects different physiological strategies to respond to temperature variation, providing many different adaptive responses to changing environments.

Invasion rates have increased in the past 100 y irrespective of international conventions. What characterizes a successful invasion event? And how does genetic diversity translate into invasion success? Employing a whole-genome perspective using one of the most successful marine invasive species world-wide as a model, we resolve temporal invasion dynamics during independent invasion events in Eurasia. We reveal complex regionally independent invasion histories including cases of recurrent translocations, time-limited translocations, and stepping-stone range expansions with severe bottlenecks within the same species. Irrespective of these different invasion dynamics, which lead to contrasting patterns of genetic diversity, all nonindigenous populations are similarly successful. This illustrates that genetic diversity, per se, is not necessarily the driving force behind invasion success. Other factors such as propagule pressure and repeated introductions are an important contribution to facilitate successful invasions. This calls into question the dominant paradigm of the genetic paradox of invasions, i.e., the successful establishment of nonindigenous populations with low levels of genetic diversity.

Selection on standing genetic variation may be effective enough to allow for adaptation to distinct niche environments within a single generation. Minor allele frequency changes at multiple, redundant loci of small effect can produce remarkable phenotypic shifts. Yet, demonstrating rapid adaptation via polygenic selection in the wild remains challenging. Here we harness natural replicate populations that experience similar selection pressures and harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus that inhabits marine estuaries characterized by high environmental heterogeneity. We identify 10,861 single nucleotide polymorphisms in F. heteroclitus that belong to a single, panmictic population yet reside in environmentally distinct niches (one coastal basin and three replicate tidal ponds). By sampling at two time points within a single generation, we quantify both allele frequency change within as well as spatial divergence among niche subpopulations. We observe few individually significant allele frequency changes yet find that the "number" of moderate changes exceeds the neutral expectation by 10-100%. We find allele frequency changes to be significantly concordant in both direction and magnitude among all niche subpopulations, suggestive of parallel selection. In addition, within-generation allele frequency changes generate subtle but significant divergence among niches, indicative of local adaptation. Although we cannot distinguish between selection and genotype-dependent migration as drivers of within-generation allele frequency changes, the trait/s determining fitness and/or migration likelihood appear to be polygenic. In heterogeneous environments, polygenic selection and polygenic, genotype-dependent migration offer conceivable mechanisms for within-generation, local adaptation to distinct niches.

To better understand temperature's role in the interaction between local evolutionary adaptation and physiological plasticity, we investigated acclimation effects on metabolic performance and thermal tolerance among natural Fundulus heteroclitus (small estuarine fish) populations from different thermal environments. Fundulus heteroclitus populations experience large daily and seasonal temperature variations, as well as local mean temperature differences across their large geographical cline. In this study, we use three populations: one locally heated (32°C) by thermal effluence (TE) from the Oyster Creek Nuclear Generating Station, NJ, and two nearby reference populations that do not experience local heating (28°C). After acclimation to 12 or 28°C, we quantified whole-animal metabolic (WAM) rate, critical thermal maximum (CT max ) and substrate-specific cardiac metabolic rate (CaM, substrates: glucose, fatty acids, lactate plus ketones plus ethanol, and endogenous (i.e. no added substrates)) in approximately 160 individuals from these three populations. Populations showed few significant differences due to large interindividual variation within populations. In general, for WAM and CT max , the interindividual variation in acclimation response (log 2 ratio 28/12°C) was a function of performance at 12°C and order of acclimation (12–28°C versus 28–12°C). CT max and WAM were greater at 28°C than 12°C, although WAM had a small change (2.32-fold) compared with the expectation for a 16°C increase in temperature (expect 3- to 4.4-fold). By contrast, for CaM, the rates when acclimatized and assayed at 12 or 28°C were nearly identical. The small differences in CaM between 12 and 28°C temperature were partially explained by cardiac remodeling where individuals acclimatized to 12°C had larger hearts than individuals acclimatized to 28°C. Correlation among physiological traits was dependent on acclimation temperature. For example, WAM was negatively correlated with CT max at 12°C but positively correlated at 28°C. Additionally, glucose substrate supported higher CaM than fatty acid, and fatty acid supported higher CaM than lactate, ketones and alcohol (LKA) or endogenous. However, these responses were highly variable with some individuals using much more FA than glucose. These findings suggest interindividual variation in physiological responses to temperature acclimation and indicate that additional research investigating interindividual may be relevant for global climate change responses in many species.

Evolution by natural selection may be effective enough to allow for recurrent, rapid adaptation to distinct niche environments within a well-mixed population. For this to occur, selection must act on standing genetic variation such that mortality i.e. genetic load, is minimized while polymorphism is maintained. Selection on multiple, redundant loci of small effect provides a potentially inexpensive solution. Yet, demonstrating adaptation via redundant, polygenic selection in the wild remains extremely challenging because low per-locus effect sizes and high genetic redundancy severely reduce statistical power. One approach to facilitate identification of loci underlying polygenic selection is to harness natural replicate populations experiencing similar selection pressures that harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus. F. heteroclitus inhabits salt marsh estuaries that are characterized by high environmental heterogeneity e.g. tidal ponds, creeks, coastal basins. Here, we sample four of these heterogeneous niches (one coastal basin and three replicate tidal ponds) at two time points from among a single, panmictic F. heteroclitus population. We identify 10,861 single nucleotide polymorphisms using a genotyping-by-sequencing approach and quantify temporal allele frequency change within, as well as spatial divergence among subpopulations residing in these niches. We find a significantly elevated number of concordant allele frequency changes among all subpopulations, suggesting ecosystem-wide adaptation to a common selection pressure. Remarkably, we also find an unexpected number of temporal allele frequency changes that generate fine-scale divergence among subpopulations, suggestive of local adaptation to distinct niche environments. Both patterns are characterized by a lack of large-effect loci yet an elevated total number of significant loci. Adaptation via redundant, polygenic selection offers a likely explanation for these patterns as well as a potential mechanism for polymorphism maintenance in the F. heteroclitus system.Author Summary Evolution by adaptation to local environmental conditions may occur more rapidly than previously thought. Recent studies show that natural selection is extremely effective when acting on, not one, but multiple genetic variants that are already present in a population. Here, we show that polygenic selection can lead to adaptation within a single generation by studying a wild, well-mixed population of mud minnows inhabiting environmentally distinct locations or niches (i.e. tidal ponds and coastal basins). We monitor allele proportions at over 10,000 genetic variants over time within a single generation and find a significant number to be changing substantially in every niche, suggestive of natural selection. We further demonstrate this genetic change to be non-random, generating mild, yet significant divergence between residents inhabiting distinct niches, indicative of local adaptation. We corroborate a previous study which discovered similar genetic divergence among niches during a different year, suggesting that local adaptation via natural selection occurs every generation. We show polygenic selection on standing genetic variation to be an effective and evolutionarily inexpensive mechanism, allowing organisms to rapidly adapt to their environments even at extremely short time scales. Our study provides valuable insights into the rate of evolution and the ability of organisms to respond to environmental change.