• Energy Research

ABSTRACTInvasive species with native ranges spanning strong environmental gradients are well suited for examining the roles of selection and population history in rapid adaptation to new habitats, providing insight into potential evolutionary responses to climate change. The Atlantic oyster drill (Urosalpinx cinerea) is a marine snail whose native range spans the strongest coastal latitudinal temperature gradient in the world, with invasive populations established on the US Pacific coast. Here, we leverage this system using genome‐wide SNPs and environmental data to examine invasion history and identify genotype–environment associations indicative of local adaptation across the native range, and then assess evidence for allelic frequency shifts that would signal rapid adaptation within invasive populations. We demonstrate strong genetic structuring among native regions which aligns with life history expectations, identifying southern New England as the source of invasive populations. Then, we identify putatively thermally adaptive loci across the native range but find no evidence of allele frequency shifts in invasive populations that suggest rapid adaptation to new environments. Our results indicate that while these loci may underpin local thermal adaptation in their native range, selection is relaxed in invasive populations, perhaps due to complex polygenic architecture underlying thermal traits and/or standing capacity for phenotypic plasticity. Given the prolific invasion of Urosalpinx, our study suggests population success in new environments is influenced by factors other than selection on standing genetic variation that underlies local adaptation in the native range and highlights the importance of considering population history and environmental selection pressures when evaluating adaptive capacity.

Populations within species often exhibit variation in traits that reflect local adaptation and further shape existing adaptive potential for species to respond to climate change. However, our mechanistic understanding of how the environment shapes trait variation remains poor. Here, we used common garden experiments to quantify thermal performance in eight populations of the marine snailUrosalpinx cinereaacross thermal gradients on the Atlantic and the Pacific coasts of North America. We then evaluated the relationship between thermal performance and environmental metrics derived from time-series data. Our results reveal a novel pattern of ‘mixed’ trait performance adaptation, where thermal optima were positively correlated with spawning temperature (cogradient variation), while maximum trait performance was negatively correlated with season length (countergradient variation). This counterintuitive pattern probably arises because of phenological shifts in the spawning season, whereby ‘cold’ populations delay spawning until later in the year when temperatures are warmer compared to ‘warm’ populations that spawn earlier in the year when temperatures are cooler. Our results show that variation in thermal performance can be shaped by multiple facets of the environment and are linked to organismal phenology and natural history. Understanding the impacts of climate change on organisms, therefore, requires the knowledge of how climate change will alter different aspects of the thermal environment.

A formidable challenge for global change biologists is to predict how natural populations will respond to the emergence of conditions not observed at present, termed novel climates. Popular approaches to predict population vulnerability are based on the expected degree of novelty relative to the amplitude of historical climate fluctuations experienced by a population. Here, we argue that predictions focused on amplitude may be inaccurate because they ignore the predictability of environmental fluctuations in driving patterns of evolution and responses to climate change. To address this disconnect, we review major findings of evolutionary theory demonstrating the conditions under which phenotypic plasticity is likely to evolve in natural populations, and how plasticity decreases population vulnerability to novel environments. We outline key criteria that experimental studies should aim for to effectively test theoretical predictions, while controlling for the degree of climate novelty. We show that such targeted tests of evolutionary theory are rare, with marine systems being overall underrepresented in this venture despite exhibiting unique opportunities to test theory. We conclude that with more robust experimental designs that manipulate both the amplitude and predictability of fluctuations, while controlling for the degree of novelty, we may better predict population vulnerability to climate change.

AbstractCapacity to cope with warming temperatures is a key determining factor of species' persistence under global climate change. Many successful invasive species have heightened thermal tolerance relative to their native counterparts, which may provide competitive advantages for habitat utilization and resource acquisition under warming scenarios, ultimately contributing to radically altered community composition. Enhanced transcriptional plasticity may be an important factor conferring superior abilities to cope with environmental stress, but the molecular mechanisms driving key differences of organismal traits in invasive versus native species are not well known. Although it is predicted that established invaders will evolve canalized phenotypes well‐adapted to new environments, it is not clear whether the same expectations are true for invaders of variable thermal environments or under climate warming scenarios where abilities to cope with fluctuating and increasing temperatures may provide fitness advantages. Here, we compare a highly successful invasive fish and a sympatric endangered native fish living in a dynamic estuarine environment that is projected to warm under climate change. We linked organismal physiological limits with global transcriptional responses at multiple common relative and absolute temperature thresholds and determined that heightened thermal tolerance of invasive Inland Silversides (Menidia beryllina) is associated with transcriptional changes that are greater both in the number of genes and the magnitude of response relative to native Delta Smelt (Hypomesus transpacificus). Modulated genes contributed to the enrichment of biological processes that differed between species and generally increased with temperature. These results are in concordance with the hypothesis that transcriptional plasticity may play a key role in determining population persistence, species interactions, and shaping community assemblages under climate change. Future studies encompassing a wider range of species and taxa are needed to determine whether this is a general pattern found between native and invasive species more broadly.