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.

Hidden genetic variation in plasticity provides the potential for rapid adaptation to novel environments.

Rapid environmental change is forcing populations into environments where plasticity will no longer maintain fitness. When populations are exposed to novel environments, evolutionary theory predicts that genetic variation in fitness will increase and should be associated with genetic differences in plasticity. If true, then genetic variation in plasticity can increase adaptive potential in novel environments, and population persistence via evolutionary rescue is more likely. To test whether genetic variation in fitness increases in novel environments and is associated with plasticity, we transplanted 8149 clones of 314 genotypes of a Sicilian daisy (Senecio chrysanthemifolius) within and outside its native range, and quantified genetic variation in fitness, and plasticity in leaf traits and gene expression. Although mean fitness declined by 87% in the novel environment, genetic variance in fitness increased threefold and was correlated with plasticity in leaf traits. High fitness genotypes showed greater plasticity in gene expression, but lower plasticity in most leaf traits. Interestingly, genotypes with the highest fitness in the novel environment had the lowest fitness at the native site. These results suggest that standing genetic variation in plasticity could help populations to persist and adapt to novel environments, despite remaining hidden in native environments.

Ecological Speciation Promoted by Divergent Regulation of Functional Genes Within African Cichlid Fishes.

Rapid ecological speciation along depth gradients has taken place repeatedly in freshwater fishes, yet molecular mechanisms facilitating such diversification are typically unclear. In Lake Masoko, an African crater lake, the cichlid Astatotilapia calliptera has diverged into shallow-littoral and deep-benthic ecomorphs with strikingly different jaw structures within the last 1,000 years. Using genome-wide transcriptome data, we explore two major regulatory transcriptional mechanisms, expression and splicing-QTL variants, and examine their contributions to differential gene expression underpinning functional phenotypes. We identified 7,550 genes with significant differential expression between ecomorphs, of which 5.4% were regulated by cis-regulatory expression QTLs, and 9.2% were regulated by cis-regulatory splicing QTLs. We also found strong signals of divergent selection on differentially expressed genes associated with craniofacial development. These results suggest that large-scale transcriptome modification plays an important role during early-stage speciation. We conclude that regulatory variants are important targets of selection driving ecologically relevant divergence in gene expression during adaptive diversification.

The importance of eco-evolutionary dynamics for predicting and managing insect range shifts.

Evolutionary change impacts the rate at which insect pests, pollinators, or disease vectors expand or contract their geographic ranges. Although evolutionary changes, and their ecological feedbacks, strongly affect these risks and associated ecological and economic consequences, they are often underappreciated in management efforts. Greater rigor and scope in study design, coupled with innovative technologies and approaches, facilitates our understanding of the causes and consequences of eco-evolutionary dynamics in insect range shifts. Future efforts need to ensure that forecasts allow for demographic and evolutionary change and that management strategies will maximize (or minimize) the adaptive potential of range-shifting insects, with benefits for biodiversity and ecosystem services.

Adaptive divergence generates distinct plastic responses in two closely related Senecio species.

The evolution of plastic responses to external cues allows species to maintain fitness in response to the environmental variations they regularly experience. However, it remains unclear how plasticity evolves during adaptation. To test whether distinct patterns of plasticity are associated with adaptive divergence, we quantified plasticity for two closely related but ecologically divergent Sicilian daisy species (Senecio, Asteraceae). We sampled 40 representative genotypes of each species from their native range on Mt. Etna and then reciprocally transplanted multiple clones of each genotype into four field sites along an elevational gradient that included the native elevational range of each species, and two intermediate elevations. At each elevation, we quantified survival and measured leaf traits that included investment (specific leaf area), morphology, chlorophyll fluorescence, pigment content, and gene expression. Traits and differentially expressed genes that changed with elevation in one species often showed little changes in the other species, or changed in the opposite direction. As evidence of adaptive divergence, both species performed better at their native site and better than the species from the other habitat. Adaptive divergence is, therefore, associated with the evolution of distinct plastic responses to environmental variation, despite these two species sharing a recent common ancestor.

Environmental variation and biotic interactions limit adaptation at ecological margins: lessons from rainforest Drosophila and European butterflies.

Models of local adaptation to spatially varying selection predict that maximum rates of evolution are determined by the interaction between increased adaptive potential owing to increased genetic variation, and the cost genetic variation brings by reducing population fitness. We discuss existing and new results from our laboratory assays and field transplants of rainforest Drosophila and UK butterflies along environmental gradients, which try to test these predictions in natural populations. Our data suggest that: (i) local adaptation along ecological gradients is not consistently observed in time and space, especially where biotic and abiotic interactions affect both gradient steepness and genetic variation in fitness; (ii) genetic variation in fitness observed in the laboratory is only sometimes visible to selection in the field, suggesting that demographic costs can remain high without increasing adaptive potential; and (iii) antagonistic interactions between species reduce local productivity, especially at ecological margins. Such antagonistic interactions steepen gradients and may increase the cost of adaptation by increasing its dimensionality. However, where biotic interactions do evolve, rapid range expansion can follow. Future research should test how the environmental sensitivity of genotypes determines their ecological exposure, and its effects on genetic variation in fitness, to predict the probability of evolutionary rescue at ecological margins. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

Understanding the biology of species' ranges: when and how does evolution change the rules of ecological engagement?

Understanding processes that limit species' ranges has been a core issue in ecology and evolutionary biology for many decades, and has become increasingly important given the need to predict the responses of biological communities to rapid environmental change. However, we still have a poor understanding of evolution at range limits and its capacity to change the ecological 'rules of engagement' that define these communities, as well as the time frame over which this occurs. Here we link papers in the current volume to some key concepts involved in the interactions between evolutionary and ecological processes at species' margins. In particular, we separate hypotheses about species' margins that focus on hard evolutionary limits, which determine how genotypes interact with their environment, from those concerned with soft evolutionary limits, which determine where and when local adaptation can persist in space and time. We show how theoretical models and empirical studies highlight conditions under which gene flow can expand local limits as well as contain them. In doing so, we emphasize the complex interplay between selection, demography and population structure throughout a species' geographical and ecological range that determines its persistence in biological communities. However, despite some impressively detailed studies on range limits, particularly in invertebrates and plants, few generalizations have emerged that can predict evolutionary responses at ecological margins. We outline some directions for future work such as considering the impact of structural genetic variants and metapopulation structure on limits, and the interaction between range limits and the evolution of mating systems and non-random dispersal. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

Climate-driven variation in biotic interactions provides a narrow and variable window of opportunity for an insect herbivore at its ecological margin.

Climate-driven geographic range shifts have been associated with transitions between dietary specialism and generalism at range margins. The mechanisms underpinning these often transient niche breadth modifications are poorly known, but utilization of novel resources likely depends on phenological synchrony between the consumer and resource. We use a climate-driven range and host shift by the butterfly Aricia agestis to test how climate-driven changes in host phenology and condition affect phenological synchrony, and consider implications for host use. Our data suggest that the perennial plant that was the primary host before range expansion is a more reliable resource than the annual Geraniaceae upon which the butterfly has become specialized in newly colonized parts of its range. In particular, climate-driven phenological variation in the novel host Geranium dissectum generates a narrow and variable 'window of opportunity' for larval productivity in summer. Therefore, although climatic change may allow species to shift hosts and colonise novel environments, specialization on phenologically limited hosts may not persist at ecological margins as climate change continues. We highlight the potential role for phenological (a)synchrony in determining lability of consumer-resource associations at range margins and the importance of considering causes of synchrony in biotic interactions when predicting range shifts. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

Social and physical environment independently affect oviposition decisions in Drosophila.

In response to environmental stimuli, including variation in the presence of conspecifics, genotypes show highly plastic responses in behavioral and physiological traits influencing reproduction. Although extensively documented in males, such female responses are rather less studied. We expect females to be highly responsive to environmental variation and to differentially allocate resources to increase offspring fitness, given the major contribution of mothers to offspring number, size, and developmental conditions. Using Drosophila melanogaster, we (a) manipulate exposure to conspecific females, which mothers could use to anticipate the number of potential mates and larval density, and; (b) test how this interacts with the spatial distribution of potential oviposition sites, with females from higher densities expected to prefer clustered resources that can support a larger number of larvae. We found that high density females were slower to start copulating and reduced their copulation duration, the opposite effect to that observed in males. There was a parallel, perhaps related, effect on egg production: females previously housed in groups laid fewer eggs than those housed in solitude. Resource patchiness also influenced oviposition behavior: females preferred aggregated substrate, which attracted more females to lay eggs. However, we found no interaction between prior housing conditions and resource patchiness, indicating that females did not perceive the value of different resource distributions differently when exposed to environments that could signal expected levels of larval competition. We show that, although exposure to consexual competition changes copulatory behaviors of females, the distribution of oviposition resources has a greater effect on oviposition decisions.

Microclimate and resource quality determine resource use in a range-expanding herbivore.

The consequences of climate change for biogeographic range dynamics depend on the spatial scales at which climate influences focal species directly and indirectly via biotic interactions. An overlooked question concerns the extent to which microclimates modify specialist biotic interactions, with emergent properties for communities and range dynamics. Here, we use an in-field experiment to assess egg-laying behaviour of a range-expanding herbivore across a range of natural microclimatic conditions. We show that variation in microclimate, resource condition and individual fecundity can generate differences in egg-laying rates of almost two orders of magnitude in an exemplar species, the brown argus butterfly (Aricia agestis). This within-site variation in fecundity dwarfs variation resulting from differences in average ambient temperatures among populations. Although higher temperatures did not reduce female selection for host plants in good condition, the thermal sensitivities of egg-laying behaviours have the potential to accelerate climate-driven range expansion by increasing egg-laying encounters with novel hosts in increasingly suitable microclimates. Understanding the sensitivity of specialist biotic interactions to microclimatic variation is, therefore, critical to predict the outcomes of climate change across species' geographical ranges, and the resilience of ecological communities.

Haplotype tagging reveals parallel formation of hybrid races in two butterfly species.

Genetic variation segregates as linked sets of variants or haplotypes. Haplotypes and linkage are central to genetics and underpin virtually all genetic and selection analysis. Yet, genomic data often omit haplotype information due to constraints in sequencing technologies. Here, we present "haplotagging," a simple, low-cost linked-read sequencing technique that allows sequencing of hundreds of individuals while retaining linkage information. We apply haplotagging to construct megabase-size haplotypes for over 600 individual butterflies (Heliconius erato and H. melpomene), which form overlapping hybrid zones across an elevational gradient in Ecuador. Haplotagging identifies loci controlling distinctive high- and lowland wing color patterns. Divergent haplotypes are found at the same major loci in both species, while chromosome rearrangements show no parallelism. Remarkably, in both species, the geographic clines for the major wing-pattern loci are displaced by 18 km, leading to the rise of a novel hybrid morph in the center of the hybrid zone. We propose that shared warning signaling (Müllerian mimicry) may couple the cline shifts seen in both species and facilitate the parallel coemergence of a novel hybrid morph in both comimetic species. Our results show the power of efficient haplotyping methods when combined with large-scale sequencing data from natural populations.

Longer photoperiods through range shifts and artificial light lead to a destabilizing increase in host-parasitoid interaction strength.

Many organisms are experiencing changing daily light regimes due to latitudinal range shifts driven by climate change and increased artificial light at night (ALAN). Activity patterns are often driven by light cycles, which will have important consequences for species interactions. We tested whether longer photoperiods lead to higher parasitism rates by a day-active parasitoid on its host using a laboratory experiment in which we independently varied daylength and the presence of ALAN. We then tested whether reduced nighttime temperature tempers the effect of ALAN. We found that parasitism rate increased with daylength, with ALAN intensifying this effect only when the temperature was not reduced at night. The impact of ALAN was more pronounced under short daylength. Increased parasitoid activity was not compensated for by reduced life span, indicating that increased daylength leads to an increase in total parasitism effects on fitness. To test the significance of increased parasitism rate for population dynamics, we developed a host-parasitoid model. The results of the model predicted an increase in time-to-equilibrium with increased daylength and, crucially, a threshold daylength above which interactions are unstable, leading to local extinctions. Here we demonstrate that ALAN impact interacts with daylength and temperature by changing the interaction strength between a common day-active consumer species and its host in a predictable way. Our results further suggest that range expansion or ALAN-induced changes in light regimes experienced by insects and their natural enemies will result in unstable dynamics beyond key tipping points in daylength.

Senecio as a model system for integrating studies of genotype, phenotype and fitness.

Two major developments have made it possible to use examples of ecological radiations as model systems to understand evolution and ecology. First, the integration of quantitative genetics with ecological experiments allows detailed connections to be made between genotype, phenotype, and fitness in the field. Second, dramatic advances in molecular genetics have created new possibilities for integrating field and laboratory experiments with detailed genetic sequencing. Combining these approaches allows evolutionary biologists to better study the interplay between genotype, phenotype, and fitness to explore a wide range of evolutionary processes. Here, we present the genus Senecio (Asteraceae) as an excellent system to integrate these developments, and to address fundamental questions in ecology and evolution. Senecio is one of the largest and most phenotypically diverse genera of flowering plants, containing species ranging from woody perennials to herbaceous annuals. These Senecio species exhibit many growth habits, life histories, and morphologies, and they occupy a multitude of environments. Common within the genus are species that have hybridized naturally, undergone polyploidization, and colonized diverse environments, often through rapid phenotypic divergence and adaptive radiation. These diverse experimental attributes make Senecio an attractive model system in which to address a broad range of questions in evolution and ecology.

Population variation in early development can determine ecological resilience in response to environmental change.

As climate change transforms seasonal patterns of temperature and precipitation, germination success at marginal temperatures will become critical for the long-term persistence of many plant species and communities. If populations vary in their environmental sensitivity to marginal temperatures across a species' geographical range, populations that respond better to future environmental extremes are likely to be critical for maintaining ecological resilience of the species. Using seeds from two to six populations for each of nine species of Mediterranean plants, we characterized patterns of among-population variation in environmental sensitivity by quantifying genotype-by-environment interactions (G × E) for germination success at temperature extremes, and under two light regimes representing conditions below and above the soil surface. For eight of nine species tested at hot and cold marginal temperatures, we observed substantial among-population variation in environmental sensitivity for germination success, and this often depended on the light treatment. Importantly, different populations often performed best at different environmental extremes. Our results demonstrate that ongoing changes in temperature regime will affect the phenology, fitness, and demography of different populations within the same species differently. We show that quantifying patterns of G × E for multiple populations, and understanding how such patterns arise, can test mechanisms that promote ecological resilience.

Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna.

Recently diverged species present particularly informative systems for studying speciation and maintenance of genetic divergence in the face of gene flow. We investigated speciation in two closely related Senecio species, S. aethnensis and S. chrysanthemifolius, which grow at high and low elevations, respectively, on Mount Etna, Sicily and form a hybrid zone at intermediate elevations. We used a newly generated genome-wide single nucleotide polymorphism (SNP) dataset from 192 individuals collected over 18 localities along an elevational gradient to reconstruct the likely history of speciation, identify highly differentiated SNPs, and estimate the strength of divergent selection. We found that speciation in this system involved heterogeneous and bidirectional gene flow along the genome, and species experienced marked population size changes in the past. Furthermore, we identified highly-differentiated SNPs between the species, some of which are located in genes potentially involved in ecological differences between species (such as photosynthesis and UV response). We analysed the shape of these SNPs' allele frequency clines along the elevational gradient. These clines show significantly variable coincidence and concordance, indicative of the presence of multifarious selective forces. Selection against hybrids is estimated to be very strong (0.16-0.78) and one of the highest reported in literature. The combination of strong cumulative selection across the genome and previously identified intrinsic incompatibilities probably work together to maintain the genetic and phenotypic differentiation between these species - pointing to the importance of considering both intrinsic and extrinsic factors when studying divergence and speciation.

Climate-induced phenology shifts linked to range expansions in species with multiple reproductive cycles per year.

Advances in phenology (the annual timing of species' life-cycles) in response to climate change are generally viewed as bioindicators of climate change, but have not been considered as predictors of range expansions. Here, we show that phenology advances combine with the number of reproductive cycles per year (voltinism) to shape abundance and distribution trends in 130 species of British Lepidoptera, in response to ~0.5 °C spring-temperature warming between 1995 and 2014. Early adult emergence in warm years resulted in increased within- and between-year population growth for species with multiple reproductive cycles per year (n = 39 multivoltine species). By contrast, early emergence had neutral or negative consequences for species with a single annual reproductive cycle (n = 91 univoltine species), depending on habitat specialisation. We conclude that phenology advances facilitate polewards range expansions in species exhibiting plasticity for both phenology and voltinism, but may inhibit expansion by less flexible species.

Local adaptation stops where ecological gradients steepen or are interrupted.

Population genetic models of evolution along linear environmental gradients cannot explain why adaptation stops at ecological margins. This is because, unless models impose reductions in carrying capacity at species' edges, the dominant effect of gene flow is to increase genetic variance and adaptive potential rather than swamping local adaptation. This allows the population to match even very steep changes in trait optima. We extend our previous simulations to explore two nonlinear models of ecological gradients: (a) a sigmoid (steepening) gradient and (b) a linear gradient with a flat centre of variable width. We compare the parameter conditions that allow local adaptation and range expansion from the centre, with those that permit the persistence of a perfectly adapted population distributed across the entire range. Along nonlinear gradients, colonization is easier, and extinction rarer, than along a linear gradient. This is because the shallow environmental gradient near the range centre does not cause gene flow to increase genetic variation, and so does not result in reduced population density. However, as gradient steepness increases, gene flow inflates genetic variance and reduces local population density sufficiently that genetic drift overcomes local selection, creating a finite range margin. When a flat centre is superimposed on a linear gradient, gene flow increases genetic variation dramatically at its edges, leading to an abrupt reduction in density that prevents niche expansion. Remarkably local interruptions in a linear ecological gradient (of a width much less than the mean dispersal distance) can prevent local adaptation beyond this flat centre. In contrast to other situations, this effect is stronger and more consistent where carrying capacity is high. Practically speaking, this means that habitat improvement at patch margins will make evolutionary rescue more likely. By contrast, even small improvements in habitat at patch centres may confine populations to limited areas of ecological space.

Evolutionary divergence in life history traits among populations of the Lake Malawi cichlid fish Astatotilapia calliptera.

During the early stages of adaptive radiation, populations diverge in life history traits such as egg size and growth rates, in addition to eco-morphological and behavioral characteristics. However, there are few studies of life history divergence within ongoing adaptive radiations. Here, we studied Astatotilapia calliptera, a maternal mouthbrooding cichlid fish within the Lake Malawi haplochromine radiation. This species occupies a rich diversity of habitats, including the main body of Lake Malawi, as well as peripheral rivers and shallow lakes. We used common garden experiments to test for life history divergence among populations, focussing on clutch size, duration of incubation, egg mass, offspring size, and growth rates. In a first experiment, we found significant differences among populations in average clutch size and egg mass, and larger clutches were associated with smaller eggs. In a second experiment, we found significant differences among populations in brood size, duration of incubation, juvenile length when released, and growth rates. Larger broods were associated with smaller juveniles when released and shorter incubation times. Although juvenile growth rates differed between populations, these were not strongly related to initial size on release. Overall, differences in life history characters among populations were not predicted by major habitat classifications (Lake Malawi or peripheral habitats) or population genetic divergence (microsatellite-based FST). We suggest that the observed patterns are consistent with local selective forces driving the observed patterns of trait divergence. The results provide strong evidence of evolutionary divergence and covariance of life history traits among populations within a radiating cichlid species, highlighting opportunities for further work to identify the processes driving the observed divergence.