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Abstract Populations across a species’ range may be locally adapted, and failure to recognize this variation can lead to inaccurate predictions of their resilience or vulnerability to climate change. Because life history traits are directly linked to fitness, life history theory can serve as a useful framework for evaluating how populations within species may respond to rapid environmental change. However, relatively few studies quantify multiple life history traits and their tradeoffs across many populations, especially in marine taxa. Here, we used a 10-month laboratory experiment to quantify a suite of reproductive traits in populations spanning the strongest latitudinal temperature gradient in the world’s coastal oceans. We examined reproductive traits in wild-captured adults exposed to simulated local conditions for 7 native Atlantic and 4 introduced Pacific populations of the marine predatory gastropodUrosalpinx cinerea. Our data reveals that reproductive season length, the number of reproductive attempts, and annual fecundity unimodally peaked at mid-latitude populations, the species’ range-center. Introduced populations had comparably few spawning attempts and low fecundity despite a longer reproductive period in a less seasonal environment. We then conducted a second experiment quantifying thermal tolerance of developing embryos from 3 native populations, which revealed high sensitivity to temperature at early life stages but weak population differentiation. Taken together, our data reveal stark differences in reproduction that appear to reflect “fast” and “slow” paced lifestyles, which may maximize fitness by spreading the risk of reproductive failure over a single season or lifetime. Our results indicate that warm range-edge populations are highly vulnerable to warming, as low embryonic thermal tolerance may shorten the spawning season and warming is likely to reduce fecundity. This study highlights heterogeneity in life history traits across marine populations that may underlie differential vulnerability to climate warming. Open research statementAll data and code will be publicly available via Figshare and the NSF Biological and Chemical Oceanography Data Management Office (BCO-DMO). 

ABSTRACT Invasive 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 ofUrosalpinx, 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. 

Understanding how latitudinal temperature variation shapes local adaptation of life history strategies is crucial for predicting future responses to warming. Contrasting predictive frameworks explain how growth and other life history traits may respond to differing selective pressures across latitude. However, these frameworks have rarely been explored within the context of fluctuating environmental temperatures across longer (i.e., seasonal) time scales experienced in nature. Furthermore, consequences of growth differences for other aspects of fitness, including reproductive output, remain unclear. Here, we conducted a long-term (17-month) simulated reciprocal transplant experiment to examine local adaptation in two populations of the predatory marine snail Urosalpinx cinerea separated by 8.6 degrees latitude (1000 km). We reared F1 offspring under two seasonally fluctuating temperature regimes (warm and cold, simulating field thermal conditions experienced by low and high latitude populations, respectively), quantifying temporal patterns in growth, maturation, and reproductive output. We identified striking divergence in life-history strategies between populations in the warm regime, with offspring from the low latitude population achieving greater growth in their first year, and high reproductive output coupled with reduced growth in their second year. In contrast, the high latitude population grew slower in their first year, but eventually attained larger sizes in their second year, at the expense of reduced reproductive output. Responses were consistent with this in the cold regime, although growth and reproductive output was reduced in both populations. Our data provides support for adaptive divergence across latitude consistent with the Pace-of-Life hypothesis, with the low latitude population selected for a fast-paced life characterized by rapid development and early reproduction. In contrast, the high latitude population exhibited slower growth and delayed maturation. Our results highlight the potential limitations of short-term comparisons of growth without considering processes over longer time scales that may exhibit seasonal temperature variation and ontogenetic shifts in energy allocation and imply a radical reshaping of physiological performance and life history traits across populations under climate change. 

Marine organisms frequently inhabit intertidal zones that serve as refuges from predation and competition but are not optimal physiologically. Restoration practitioners working with intertidal species may similarly have to consider whether restoration success will be greater where conditions are more benign (usually lower in the intertidal) or where negative biotic interactions are reduced (usually higher in the intertidal). In cases where a target species has greater desiccation tolerance than its enemies, restoration may be more successful higher in the intertidal zone, despite potential performance trade-offs. In many US West Coast estuaries, non-native drill species can decimate native oyster populations, posing a challenge to restoration. Given that native Olympia oystersOstrea luridashould be better able to withstand tidal emersion than the non-native Atlantic oyster drillUrosalpinx cinerea, we explored using the high intertidal as a refuge from predation as a potential restoration technique. Using surveys and a field experiment, we investigated the recruitment, growth, and survival of oysters as well as drill abundance and predation over 3 tidal elevations. Oysters recruited and survived equally well at +0.1, +0.5, and +0.8 m mean lower low water, but juvenile oyster growth decreased with increasing elevation. In our experiment, predation on oysters was lower at the highest elevation than at low and mid elevations, but in natural populations there was a near complete absence ofO. luridaat any elevation whereU. cinereawas present. This suggests that a higher tidal elevation refuge is not a viable approach for oyster restoration in our study area. 

Established non-native species can have significant impacts on native biodiversity without any possibility of complete eradication. In such cases, one management approach is functional eradication, the reduction of introduced species density below levels that cause unacceptable effects on the native community. Functional eradication may be particularly effective for species with reduced dispersal ability, which may limit rates of reinvasion from distant populations. Here, we evaluate the potential for functional eradication of introduced predatory oyster drills (Urosalpinx cinerea) using a community science approach in San Francisco Bay. We combined observational surveys, targeted removals, and a caging experiment to evaluate the effectiveness of this approach in mitigating the mortality of prey Olympia oysters (Ostrea lurida), a conservation and restoration priority species. Despite the efforts of over 300 volunteers that removed over 30,000 oyster drills, we report limited success. We also found a strong negative relationship between oyster drills and oysters, showing virtually no coexistence across eight sites. At experimental sites, there was no effect of oyster drill removal on oyster survival in a caging experiment, but strong effects of caging treatment on oyster survival (0 and 1.6% survival in open and partial cage treatments, as compared to 89.1% in predator exclusion treatments). We conclude that functional eradication of this species requires significantly greater effort and may not be a viable management strategy in this system. We discuss several possible mechanisms for this result with relevance to management for this and other introduced species. Oyster restoration efforts should not be undertaken where Urosalpinx is established or is likely to invade. 

Many species face extinction risks owing to climate change, and there is an urgent need to identify which species' populations will be most vulnerable. Plasticity in heat tolerance, which includes acclimation or hardening, occurs when prior exposure to a warmer temperature changes an organism's upper thermal limit. The capacity for thermal acclimation could provide protection against warming, but prior work has found few generalizable patterns to explain variation in this trait. Here, we report the results of, to our knowledge, the first meta-analysis to examine within-species variation in thermal plasticity, using results from 20 studies (19 species) that quantified thermal acclimation capacities across 78 populations. We used meta-regression to evaluate two leading hypotheses. The climate variability hypothesis predicts that populations from more thermally variable habitats will have greater plasticity, while the trade-off hypothesis predicts that populations with the lowest heat tolerance will have the greatest plasticity. Our analysis indicates strong support for the trade-off hypothesis because populations with greater thermal tolerance had reduced plasticity. These results advance our understanding of variation in populations' susceptibility to climate change and imply that populations with the highest thermal tolerance may have limited phenotypic plasticity to adjust to ongoing climate warming. 

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 snail Urosalpinx cinerea across 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. 

Abstract Models of species response to climate change often assume that physiological traits are invariant across populations. Neglecting potential intraspecific variation may overlook the possibility that some populations are more resilient or susceptible than others, creating inaccurate predictions of climate impacts. In addition, phenotypic plasticity can contribute to trait variation and may mediate sensitivity to climate. Quantifying such forms of intraspecific variation can improve our understanding of how climate can affect ecologically important species, such as invasive predators. Here, we quantified thermal performance (tolerance, acclimation capacity, developmental traits) across seven populations of the predatory marine snail (Urosalpinx cinerea) from native Atlantic and non-native Pacific coast populations in the USA. Using common garden experiments, we assessed the effects of source population and developmental acclimation on thermal tolerance and developmental traits of F1 snails. We then estimated climate sensitivity by calculating warming tolerance (thermal tolerance − habitat temperature), using field environmental data. We report that low-latitude populations had greater thermal tolerance than their high latitude counterparts. However, these same low-latitude populations exhibited decreased thermal tolerance when exposed to environmentally realistic higher acclimation temperatures. Low-latitude native populations had the greatest climate sensitivity (habitat temperatures near thermal limits). In contrast, invasive Pacific snails had the lowest climate sensitivity, suggesting that these populations are likely to persist and drive negative impacts on native biodiversity. Developmental rate significantly increased in embryos sourced from populations with greater habitat temperature but had variable effects on clutch size and hatching success. Thus, warming can produce widely divergent responses within the same species, resulting in enhanced impacts in the non-native range and extirpation in the native range. Broadly, our results highlight how intraspecific variation can alter management decisions, as this may clarify whether management efforts should be focused on many or only a few populations.