Spatial variation in genomic signatures of local adaptation during the cane toad invasion of Australia.

Adaptive evolution can facilitate species' range expansions across environmentally heterogeneous landscapes. However, serial founder effects can limit the efficacy of selection, and the evolution of increased dispersal during range expansions may result in gene flow swamping local adaptation. Here, we study how genetic drift, gene flow and selection interact during the cane toad's (Rhinella marina) invasion across the heterogeneous landscape of Australia. Following its introduction in 1935, the cane toad colonised eastern Australia and established several stable range edges. The ongoing, more rapid range expansion in north-central Australia has occurred concomitant with an evolved increase in dispersal capacity. Using reduced representation genomic data of Australian cane toads from the expansion front and from two areas of their established range, we test the hypothesis that high gene flow constrains local adaptation at the expansion front relative to established areas. Genetic analyses indicate the three study areas are genetically distinct but show similar levels of allelic richness, heterozygosity and inbreeding. Markedly higher gene flow or recency of colonisation at the expansion front have likely hindered local adaptation at the time of sampling, as indicated by reduced slopes of genetic-environment associations (GEAs) estimated using a novel application of geographically weighted regression that accounts for allele surfing; GEA slopes are significantly steeper in established parts of the range. Our work bolsters evidence supporting adaptation of invasive species post-introduction and adds novel evidence for differing strengths of evolutionary forces among geographic areas with different invasion histories.

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.

Designing eco-evolutionary experiments for restoration projects: Opportunities and constraints revealed during stickleback introductions.

Eco-evolutionary experiments are typically conducted in semi-unnatural controlled settings, such as mesocosms; yet inferences about how evolution and ecology interact in the real world would surely benefit from experiments in natural uncontrolled settings. Opportunities for such experiments are rare but do arise in the context of restoration ecology-where different "types" of a given species can be introduced into different "replicate" locations. Designing such experiments requires wrestling with consequential questions. (Q1) Which specific "types" of a focal species should be introduced to the restoration location? (Q2) How many sources of each type should be used-and should they be mixed together? (Q3) Which specific source populations should be used? (Q4) Which type(s) or population(s) should be introduced into which restoration sites? We recently grappled with these questions when designing an eco-evolutionary experiment with threespine stickleback (Gasterosteus aculeatus) introduced into nine small lakes and ponds on the Kenai Peninsula in Alaska that required restoration. After considering the options at length, we decided to use benthic versus limnetic ecotypes (Q1) to create a mixed group of colonists from four source populations of each ecotype (Q2), where ecotypes were identified based on trophic morphology (Q3), and were then introduced into nine restoration lakes scaled by lake size (Q4). We hope that outlining the alternatives and resulting choices will make the rationales clear for future studies leveraging our experiment, while also proving useful for investigators considering similar experiments in the future.

Boom-bust population dynamics drive rapid genetic change.

Increasing environmental threats and more extreme environmental perturbations place species at risk of population declines, with associated loss of genetic diversity and evolutionary potential. While theory shows that rapid population declines can cause loss of genetic diversity, populations in some environments, like Australia's arid zone, are repeatedly subject to major population fluctuations yet persist and appear able to maintain genetic diversity. Here, we use repeated population sampling over 13 y and genotype-by-sequencing of 1903 individuals to investigate the genetic consequences of repeated population fluctuations in two small mammals in the Australian arid zone. The sandy inland mouse (Pseudomys hermannsburgensis) experiences marked boom-bust population dynamics in response to the highly variable desert environment. We show that heterozygosity levels declined, and population differentiation (FST) increased, during bust periods when populations became small and isolated, but that heterozygosity was rapidly restored during episodic population booms. In contrast, the lesser hairy-footed dunnart (Sminthopsis youngsoni), a desert marsupial that maintains relatively stable population sizes, showed no linear declines in heterozygosity. These results reveal two contrasting ways in which genetic diversity is maintained in highly variable environments. In one species, diversity is conserved through the maintenance of stable population sizes across time. In the other species, diversity is conserved through rapid genetic mixing during population booms that restores heterozygosity lost during population busts.

Temporal genomics help in deciphering neutral and adaptive patterns in the contemporary evolution of kelp populations.

The impact of climate change on populations will be contingent upon their contemporary adaptive evolution. In this study, we investigated the contemporary evolution of 4 populations of the cold-water kelp Laminaria digitata by analyzing their spatial and temporal genomic variations using ddRAD-sequencing. These populations were sampled from the center to the southern margin of its north-eastern Atlantic distribution at 2 time points, spanning at least 2 generations. Through genome scans for local adaptation at a single time point, we identified candidate loci that showed clinal variation correlated with changes in sea surface temperature (SST) along latitudinal gradients. This finding suggests that SST may drive the adaptive response of these kelp populations, although factors such as species' demographic history should also be considered. Additionally, we performed a simulation approach to distinguish the effect of selection from genetic drift in allele frequency changes over time. This enabled the detection of loci in the southernmost population that exhibited temporal differentiation beyond what would be expected from genetic drift alone: these are candidate loci which could have evolved under selection over time. In contrast, we did not detect any outlier locus based on temporal differentiation in the population from the North Sea, which also displayed low and decreasing levels of genetic diversity. The diverse evolutionary scenarios observed among populations can be attributed to variations in the prevalence of selection relative to genetic drift across different environments. Therefore, our study highlights the potential of temporal genomics to offer valuable insights into the contemporary evolution of marine foundation species facing climate change.

Go west: Population genomics reveals unexpected population fluctuations and little gene flow in Western hemisphere populations of the predatory lady beetle, Hippodamia convergens.

Hippodamia convergens-the convergent lady beetle, has been used extensively in augmentative biological control of aphids, thrips, and whiteflies across its native range in North America, and was introduced into South America in the 1950s. Overwintering H. convergens populations from its native western range in the United States are commercially collected and released across its current range in the eastern USA, with little knowledge of the effectiveness of its augmentative biological control. Here we use a novel ddRADseq-based SNP/haplotype discovery approach to estimate its range-wide population diversity, differentiation, and recent evolutionary history. Our results indicate (1) significant population differentiation among eastern USA, western USA, and South American populations of H. convergens, with (2) little to no detectable recent admixture between them, despite repeated population augmentation, and (3) continued recent population size expansion across its range. These results contradict previous findings using microsatellite markers. In light of these new findings, the implications for the effectiveness of augmentative biological control using H. convergens are discussed. Additionally, because quantifying the non-target effects of augmentative biological control is a difficult problem in migratory beetles, our results could serve as a cornerstone in improving and predicting the efficacy of future releases of H. convergens across its range.

Independently evolved pollution resistance in four killifish populations is largely explained by few variants of large effect.

The genetic architecture of phenotypic traits can affect the mode and tempo of trait evolution. Human-altered environments can impose strong natural selection, where successful evolutionary adaptation requires swift and large phenotypic shifts. In these scenarios, theory predicts that adaptation is due to a few adaptive variants of large effect, but empirical studies that have revealed the genetic architecture of rapidly evolved phenotypes are rare, especially for populations inhabiting polluted environments. Fundulus killifish have repeatedly evolved adaptive resistance to extreme pollution in urban estuaries. Prior studies, including genome scans for signatures of natural selection, have revealed some of the genes and pathways important for evolved pollution resistance, and provide context for the genotype-phenotype association studies reported here. We created multiple quantitative trait locus (QTL) mapping families using progenitors from four different resistant populations, and using RAD-seq genetically mapped variation in sensitivity (developmental perturbations) following embryonic exposure to a model toxicant PCB-126. We found that one to two large-effect QTL loci accounted for resistance to PCB-mediated developmental toxicity. QTLs harbored candidate genes that govern the regulation of aryl hydrocarbon receptor (AHR) signaling. One QTL locus was shared across all populations and another was shared across three populations. One QTL locus showed strong signatures of recent natural selection in the corresponding wild population but another QTL locus did not. Some candidate genes for PCB resistance inferred from genome scans in wild populations were identified as QTL, but some key candidate genes were not. We conclude that rapidly evolved resistance to the developmental defects normally caused by PCB-126 is governed by few genes of large effect. However, other aspects of resistance beyond developmental phenotypes may be governed by additional loci, such that comprehensive resistance to PCB-126, and to the mixtures of chemicals that distinguish urban estuaries more broadly, may be more genetically complex.

Environmental forcing alters fisheries selection.

Fishing-induced evolution (FIE) threatens the ecology, resilience, and economic value of fish populations. Traits under selection, and mechanisms of selection, can be influenced by abiotic and biotic perturbations, yet this has been overlooked. Here, we present the fishery selection continuum, where selection ranges from rigid fisheries selection to flexible fisheries selection. We provide examples on how FIE may function along this continuum, and identify selective processes that should be considered less or more flexible. We also introduce fishery reaction norms, which serve to conceptualise how selection from fishing may function in a dynamic context. Ultimately, we suggest an integrative approach to studying FIE that considers the environmental conditions in which it functions.

Population genomic structure of a widespread, urban-dwelling mammal: The eastern grey squirrel (Sciurus carolinensis).

Urbanization is a persistent and widespread driver of global environmental change, potentially shaping evolutionary processes due to genetic drift and reduced gene flow in cities induced by habitat fragmentation and small population sizes. We tested this prediction for the eastern grey squirrel (Sciurus carolinensis), a common and conspicuous forest-dwelling rodent, by obtaining 44K SNPs using reduced representation sequencing (ddRAD) for 403 individuals sampled across the species' native range in eastern North America. We observed moderate levels of genetic diversity, low levels of inbreeding, and only a modest signal of isolation-by-distance. Clustering and migration analyses show that estimated levels of migration and genetic connectivity were higher than expected across cities and forested areas, specifically within the eastern portion of the species' range dominated by urbanization, and genetic connectivity was less than expected within the western range where the landscape is fragmented by agriculture. Landscape genetic methods revealed greater gene flow among individual squirrels in forested regions, which likely provide abundant food and shelter for squirrels. Although gene flow appears to be higher in areas with more tree cover, only slight discontinuities in gene flow suggest eastern grey squirrels have maintained connected populations across urban areas in all but the most heavily fragmented agricultural landscapes. Our results suggest urbanization shapes biological evolution in wildlife species depending strongly on the composition and habitability of the landscape matrix surrounding urban areas.

Environmental change unlinks a gene from its trait.

In Atlantic salmon (Salmo salar), sea age is a major life history trait governed by a sex-specific trade-off between reproductive success and survival. In this issue of Molecular Ecology, Besnier et al. (Molecular Ecology, 2023) found evidence to suggest that the disassociation between sea age and major effect loci, including the previously identified candidate genes vgll3 and six6, may be related to the recently observed trend towards slower growth and later maturation. These results are of importance because they challenge the prevailing view that evolution moves in a slow shuffle, and they provide a pertinent example of how an optimal phenotype can change due to growth-driven plasticity and lead to contemporary molecular and phenotypic evolution.

Do chromosome rearrangements fix by genetic drift or natural selection? Insights from Brenthis butterflies.

Large-scale chromosome rearrangements, such as fissions and fusions, are a common feature of eukaryote evolution. They can have considerable influence on the evolution of populations, yet it remains unclear exactly how rearrangements become established and eventually fix. Rearrangements could fix by genetic drift if they are weakly deleterious or neutral, or they may instead be favoured by positive natural selection. Here, we compare genome assemblies of three closely related Brenthis butterfly species and characterize a complex history of fission and fusion rearrangements. An inferred demographic history of these species suggests that rearrangements became fixed in populations with large long-term effective size (Ne ), consistent with rearrangements being selectively neutral or only very weakly underdominant. Using a recently developed analytic framework for characterizing hard selective sweeps, we find that chromosome fusions are not enriched for evidence of past sweeps compared to other regions of the genome. Nonetheless, we do infer a strong and recent selective sweep around one chromosome fusion in the B. daphne genome. Our results suggest that rearrangements in these species likely have weak absolute fitness effects and fix by genetic drift. However, one putative selective sweep raises the possibility that natural selection may sometimes play a role in the fixation of chromosome fusions.

Rapid evolution of novel biotic interactions in the UK Brown Argus butterfly uses genomic variation from across its geographical range.

Understanding the rate and extent to which populations can adapt to novel environments at their ecological margins is fundamental to predicting the persistence of biological communities during ongoing and rapid global change. Recent range expansion in response to climate change in the UK butterfly Aricia agestis is associated with the evolution of novel interactions with a larval food plant, and the loss of its ability to use an ancestral host species. Using ddRAD analysis of 61,210 variable SNPs from 261 females from throughout the UK range of this species, we identify genomic regions at multiple chromosomes that are associated with evolutionary responses, and their association with demographic history and ecological variation. Gene flow appears widespread throughout the range, despite the apparently fragmented nature of the habitats used by this species. Patterns of haplotype variation between selected and neutral genomic regions suggest that evolution associated with climate adaptation is polygenic, resulting from the independent spread of alleles throughout the established range of this species, rather than the colonization of pre-adapted genotypes from coastal populations. These data suggest that rapid responses to climate change do not depend on the availability of pre-adapted genotypes. Instead, the evolution of novel forms of biotic interaction in A. agestis has occurred during range expansion, through the assembly of novel genotypes from alleles from multiple localities.

Eco-evolution from deep time to contemporary dynamics: The role of timescales and rate modulators.

Eco-evolutionary dynamics, or eco-evolution for short, are often thought to involve rapid demography (ecology) and equally rapid heritable phenotypic changes (evolution) leading to novel, emergent system behaviours. We argue that this focus on contemporary dynamics is too narrow: Eco-evolution should be extended, first, beyond pure demography to include all environmental dimensions and, second, to include slow eco-evolution which unfolds over thousands or millions of years. This extension allows us to conceptualise biological systems as occupying a two-dimensional time space along axes that capture the speed of ecology and evolution. Using Hutchinson's analogy: Time is the 'theatre' in which ecology and evolution are two interacting 'players'. Eco-evolutionary systems are therefore dynamic: We identify modulators of ecological and evolutionary rates, like temperature or sensitivity to mutation, which can change the speed of ecology and evolution, and hence impact eco-evolution. Environmental change may synchronise the speed of ecology and evolution via these rate modulators, increasing the occurrence of eco-evolution and emergent system behaviours. This represents substantial challenges for prediction, especially in the context of global change. Our perspective attempts to integrate ecology and evolution across disciplines, from gene-regulatory networks to geomorphology and across timescales, from today to deep time.

Resurrecting urban sunflowers: Phenotypic and molecular changes between antecedent and modern populations separated by 36 years.

Resurrection experiments provide a unique opportunity to evaluate phenotypic and molecular evolution in response to environmental challenges. To understand the evolution of urban populations of Helianthus annuus, we compared plants from 36-year-old antecedent seed collections to modern seed collections from the same area using molecular and quantitative genetic approaches. We found 200 differentially expressed transcripts between antecedent and modern groups, and transcript expression was generally higher in modern samples as compared to antecedent samples. Admixture analysis indicated gene flow from domesticated to modern populations over time. After a greenhouse refresher generation, one antecedent-modern population pair was grown under two water availability (well-watered and drought) and temperature (ambient and elevated by 2.8°C) conditions reflecting historical and contemporary climates. Overall, 78% (7 out of 9) of traits differed between the antecedent and modern populations, with modern individuals displaying some trait changes that are coherent with climate changes expectations and some trait changes in the direction of crop varieties. Phenotypic selection analysis showed that modern trait values were often favoured by selection, especially in environmental treatments resembling modern conditions. Trait heritability in the antecedent population was five times as high as in the modern population, on average. In addition, phenotypic plasticity for some traits, such as flowering phenology, was present in the antecedent population but absent in the modern population. The combination of phenotypic and molecular information suggests that evolution has been influenced by crop-wild introgression, adaptive processes and drift. We discuss these results in the context of continued evolution in response to anthropogenic factors.

Keep your cool: Overwintering physiology in response to urbanization in the acorn ant, Temnothorax curvispinosus.

Winter presents a challenge for survival, yet temperate ectotherms have remarkable physiological adaptations to cope with low-temperature conditions. Under recent climate change, rather than strictly relaxing pressure on overwintering survival, warmer winters can instead disrupt these low-temperature trait-environment associations, with negative consequences for populations. While there is increasing evidence of physiological adaptation to contemporary warming during the growing season, the effects of winter warming on physiological traits are less clear. To address this knowledge gap, we performed a common garden experiment using relatively warm-adapted versus cold-adapted populations of the acorn ant, Temnothorax curvispinosus, sampled across an urban heat island gradient, to explore the effects of winter conditions on plasticity and evolution of physiological traits. We found no evidence of evolutionary divergence in chill coma recovery nor in metabolic rate at either of two test temperatures (4 and 10 °C). Although we found the expected plastic response of increased metabolic rate under the 10 °C acute test temperature as compared with the 4 °C test temperature, this plastic response, (i.e., the acute thermal sensitivity of metabolic rate), was not different across populations. Surprisingly, we found that winter-acclimated urban ant populations exhibited higher heat tolerance compared with rural ant populations, and that the magnitude of divergence was comparable to that observed among growing-season acclimated ants. Finally, we found no evidence of differences between populations with respect to changes in colony size from the beginning to the end of the overwintering experiment. Together, these findings indicate that despite the evolution of higher heat tolerance that is often accompanied by losses in low-temperature tolerance, urban acorn ants have retained several components of low-temperature physiological performance when assessed under ecologically relevant overwintering conditions. Our study suggests the importance of measuring physiological traits under seasonally-relevant conditions to understand the causes and consequences of evolutionary responses to contemporary warming.

Evolution of butterfly seasonal plasticity driven by climate change varies across life stages.

Photoperiod is a common cue for seasonal plasticity and phenology, but climate change can create cue-environment mismatches for organisms that rely on it. Evolution could potentially correct these mismatches, but phenology often depends on multiple plastic decisions made during different life stages and seasons that may evolve separately. For example, Pararge aegeria (Speckled wood butterfly) has photoperiod-cued seasonal life history plasticity in two different life stages: larval development time and pupal diapause. We tested for climate change-associated evolution of this plasticity by replicating common garden experiments conducted on two Swedish populations 30 years ago. We found evidence for evolutionary change in the contemporary larval reaction norm-although these changes differed between populations-but no evidence for evolution of the pupal reaction norm. This variation in evolution across life stages demonstrates the need to consider how climate change affects the whole life cycle to understand its impacts on phenology.

Rapidly evolved traits enable new conservation tools: perspectives from the cane toad invasion of Australia.

Natural populations can show rapid adaptive responses to intense (human-mediated) environmental change. The potential for exploiting rapidly evolved traits for conservation management has been often discussed but rarely implemented. Capitalizing on a well-studied biological invasion, we here explore the idea that rapid phenotypic change in the invaders, their pathogens, and the native biota provide opportunities for managers to control invader abundance and buffer adverse impacts on native wildlife. Intensive studies of the invasion of tropical Australia by cane toads (Rhinella marina) have identified newly evolved vulnerabilities that we could exploit for toad control; and newly evolved resilience of native wildlife that we could exploit for impact reduction. For example, distinctive phenotypes of toads at the expanding range edge enhance dispersal rate but reduce reproductive output, intraspecific competitive ability, and immunocompetence; and the evolution of larval cannibalism creates opportunities not only for species-specific trapping of toad tadpoles, but also could be exploited (when allied to emerging CRISPR-Cas9 techniques) to intensify intraspecific conflict in invasive toads. That is, we could use the invasive species to control their own populations. This case study illustrates the potential of detailed basic research to identify novel approaches for conservation.

Independently evolved pollution resistance in four killifish populations is largely explained by few variants of large effect.

The genetic architecture of phenotypic traits can affect the mode and tempo of trait evolution. Human-altered environments can impose strong natural selection, where successful evolutionary adaptation requires swift and large phenotypic shifts. In these scenarios, theory predicts the influence of few adaptive variants of large effect, but empirical studies that have revealed the genetic architecture of rapidly evolved phenotypes are rare, especially for populations inhabiting polluted environments. Fundulus killifish have repeatedly evolved adaptive resistance to extreme pollution in urban estuaries. Prior studies, including genome scans for signatures of natural selection, have revealed some of the genes and pathways important for evolved pollution resistance, and provide context for the genotype-phenotype association studies reported here. We created multiple quantitative trait locus (QTL) mapping families using progenitors from four different resistant populations, and genetically mapped variation in sensitivity (developmental perturbations) following embryonic exposure to a model toxicant PCB-126. We found that a few large-effect QTL loci accounted for resistance to PCB-mediated developmental toxicity. QTLs harbored candidate genes that govern the regulation of aryl hydrocarbon receptor (AHR) signaling, where some (but not all) of these QTL loci were shared across all populations, and some (but not all) of these loci showed signatures of recent natural selection in the corresponding wild population. Some strong candidate genes for PCB resistance inferred from genome scans in wild populations were identified as QTL, but some key candidate genes were not. We conclude that rapidly evolved resistance to the developmental defects normally caused by PCB-126 is governed by few genes of large effect. However, other aspects of resistance beyond developmental phenotypes may be governed by additional loci, such that comprehensive resistance to PCB-126, and to the mixtures of chemicals that distinguish urban estuaries more broadly, may be more genetically complex.

The practice and promise of temporal genomics for measuring evolutionary responses to global change.

Understanding the evolutionary consequences of anthropogenic change is imperative for estimating long-term species resilience. While contemporary genomic data can provide us with important insights into recent demographic histories, investigating past change using present genomic data alone has limitations. In comparison, temporal genomics studies, defined herein as those that incorporate time series genomic data, utilize museum collections and repeated field sampling to directly examine evolutionary change. As temporal genomics is applied to more systems, species and questions, best practices can be helpful guides to make the most efficient use of limited resources. Here, we conduct a systematic literature review to synthesize the effects of temporal genomics methodology on our ability to detect evolutionary changes. We focus on studies investigating recent change within the past 200 years, highlighting evolutionary processes that have occurred during the past two centuries of accelerated anthropogenic pressure. We first identify the most frequently studied taxa, systems, questions and drivers, before highlighting overlooked areas where further temporal genomic studies may be particularly enlightening. Then, we provide guidelines for future study and sample designs while identifying key considerations that may influence statistical and analytical power. Our aim is to provide recommendations to a broad array of researchers interested in using temporal genomics in their work.

Testing the predictability of morphological evolution in contrasting thermal environments.

Gaining the ability to predict population responses to climate change is a pressing concern. Using a "natural experiment," we show that testing for divergent evolution in wild populations from contrasting thermal environments provides a powerful approach, and likely an enhanced predictive power for responses to climate change. Specifically, we used a unique study system in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity, adjacent to populations in ambient-temperature water. We focused on morphological traits across six pairs from warm and cold habitats. We found that fish from warm habitats tended to have a deeper mid-body, a subterminally orientated jaw, steeper craniofacial profile, and deeper caudal region relative to fish from cold habitats. Our common garden experiment showed that most of these differences were heritable. Population age did not appear to influence the magnitude or type of thermal divergence, but similar types of divergence between thermal habitats were more prevalent across allopatric than sympatric population pairs. These findings suggest that morphological divergence in response to thermal habitat, despite being relatively complex and multivariate, are predictable to a degree. Our data also suggest that the potential for migration of individuals between different thermal habitats may enhance nonparallel evolution and reduce our ability to predict responses to climate change.