The importance of marginal population hotspots of cold‐adapted species for research on climate change and conservation

Areas hosting hotspots of low‐latitude marginal populations of cold‐adapted plant species could be key areas for understanding geographical attributes that result in refugia during climatic shifts as well as the conservation of genetic diversity in the face of climate change. Low‐latitude populations of cold‐adapted plants are important because they may harbour the combination of alleles that foster persistence in a warmer climate. Consequently, identification of areas where arctic‐alpine, circumpolar and circumboreal species reach the low‐latitude ends of their distribution will present a unique opportunity to uncover processes that shaped current biogeographical patterns, as well as prepare for future scenarios. Here, we identify 35 main marginal population hotspots (19 and 16 areas in North America and Europe, respectively) of 183 plant taxa. These hotspots represent areas where southern marginal populations of cold‐adapted species co‐occur. The identification of hotspots was based on geographic overlap of southernmost locations of the target species, in a 50 × 50 km grid. With a threshold of two species in a single grid cell or in two contiguous cells, the analysis revealed that hotspots are in most cases located in the southern portion of major mountain chains. However, hotspots also occur in lowland areas at high latitudes (Fennoscandia, Alaska, Hudson Bay) which do not necessarily correspond to known cold‐ or warm‐stage refugia (e.g. Alps). Rockies and Sierra Nevada both in California and Spain, Apennines, and the southern Scandes, maintain their hotspot status even with more stringent cut‐off thresholds (>3 and >5 species per cell group). From a conservation point of view, our analysis reveals that only a small portion of the hotspots are currently included within protected areas. We discuss the importance of marginal population hotspots to future research on climate change and, finally, outline how conservation strategies can capitalize on the knowledge gained from studying climate change effects on cold‐adapted plants.     

Eco‐evolution on the edge during climate change

We urgently need to predict species responses to climate change to minimize future biodiversity loss and ensure we do not waste limited resources on ineffective conservation strategies. Currently, most predictions of species responses to climate change ignore the potential for evolution. However, evolution can alter species ecological responses, and different aspects of evolution and ecology can interact to produce complex eco‐evolutionary dynamics under climate change. Here we review how evolution could alter ecological responses to climate change on species warm and cool range margins, where evolution could be especially important. We discuss different aspects of evolution in isolation, and then synthesize results to consider how multiple evolutionary processes might interact and affect conservation strategies. On species cool range margins, the evolution of dispersal could increase range expansion rates and allow species to adapt to novel conditions in their new range. However, low genetic variation and genetic drift in small range‐front populations could also slow or halt range expansions. Together, these eco‐evolutionary effects could cause a three‐step, stop‐and‐go expansion pattern for many species. On warm range margins, isolation among populations could maintain high genetic variation that facilitates evolution to novel climates and allows species to persist longer than expected without evolution. This ‘evolutionary extinction debt’ could then prevent other species from shifting their ranges. However, as climate change increases isolation among populations, increasing dispersal mortality could select for decreased dispersal and cause rapid range contractions. Some of these eco‐evolutionary dynamics could explain why many species are not responding to climate change as predicted. We conclude by suggesting that resurveying historical studies that measured trait frequencies, the strength of selection, or heritabilities could be an efficient way to increase our eco‐evolutionary knowledge in climate change biology.     

The adaptive value of epigenetic mutation: Limited in large but high in small peripheral populations

The fate of populations during range expansions, invasions and environmental changes is largely influenced by their ability to adapt to peripheral habitats. Recent models demonstrate that stable epigenetic modifications of gene expression that occur more frequently than genetic mutations can both help and hinder adaptation in panmictic populations. However, these models do not consider interactions between epimutations and evolutionary forces in peripheral populations. Here, we use mainland–island mathematical models and simulations to explore how the faster rate of epigenetic mutation compared to genetic mutations interacts with migration, selection and genetic drift to affect adaptation in peripheral populations. Our model focuses on cases where epigenetic marks are stably inherited. In a large peripheral population, where the effect of genetic drift is negligible, our analyses suggest that epimutations with random fitness impacts that occur at rates as high as 10^–3 increase local adaptation when migration is strong enough to overwhelm divergent selection. When migration is weak relative to selection and epimutations with random fitness impacts decrease adaptation, we find epigenetic modifications must be highly adaptively biased to enhance adaptation. Finally, in small peripheral populations, where genetic drift is strong, epimutations contribute to adaptation under a wider range of evolutionary conditions. Overall, our results suggest that epimutations can change outcomes of adaptation in peripheral populations, which has implications for understanding conservation and range expansions and contractions, especially of small populations.     

Reduced variability in range‐edge butterfly populations over three decades of climate warming

Populations at the high latitude edge of species’ geographical ranges are thought to show larger interannual population fluctuations, with subsequent higher local extinction risk, than those within the ‘core’ climatic range. As climate envelopes shift northward under climate warming, however, we would expect populations to show dampened variability. We test this hypothesis using annual abundance indices from 19 butterfly species across 79 British monitoring sites between 1976 and 2009, a period of climatic warming. We found that populations in the latter (warmer) half of the recording period show reduced interannual population variability. Species with more southerly European distributions showed the greatest dampening in population variability over time. Our results suggest that increases in population variability occur towards climatic range boundaries. British sites, previously existing at the margins of suitable climate space, now appear to fall closer to the core climatic range for many butterfly species.     

Hiding from the climate: Characterizing microrefugia for boreal forest understory species

Climate warming is likely to shift the range margins of species poleward, but fine‐scale temperature differences near the ground (microclimates) may modify these range shifts. For example, cold‐adapted species may survive in microrefugia when the climate gets warmer. However, it is still largely unknown to what extent cold microclimates govern the local persistence of populations at their warm range margin. We located 99 microrefugia, defined as sites with edge populations of 12 widespread boreal forest understory species (vascular plants, mosses, liverworts and lichens) in an area of ca. 24,000 km² along the species' southern range margin in central Sweden. Within each population, a logger measured temperature eight times per day during one full year. Using univariate and multivariate analyses, we examined the differences of the populations' microclimates with the mean and range of microclimates in the landscape, and identified the typical climate, vegetation and topographic features of these habitats. Comparison sites were drawn from another logger data set (n = 110), and from high‐resolution microclimate maps. The microrefugia were mainly places characterized by lower summer and autumn maximum temperatures, late snow melt dates and high climate stability. Microrefugia also had higher forest basal area and lower solar radiation in spring and autumn than the landscape average. Although there were common trends across northern species in how microrefugia differed from the landscape average, there were also interspecific differences and some species contributed more than others to the overall results. Our findings provide biologically meaningful criteria to locate and spatially predict potential climate microrefugia in the boreal forest. This opens up the opportunity to protect valuable sites, and adapt forest management, for example, by keeping old‐growth forests at topographically shaded sites. These measures may help to mitigate the loss of genetic and species diversity caused by rear‐edge contractions in a warmer climate.     

Trade‐offs between life‐history traits at range‐edge and central locations

The allocation of resources to different life‐history traits should represent the best compromise in fitness investment for organisms in their local environment. When resources are limiting, the investment in a specific trait must carry a cost that is expressed in trade‐offs with other traits. In this study, the relative investment in the fitness‐related traits, growth, reproduction and defence were compared at central and range‐edge locations, using the seaweed Ascophyllum nodosum as a model system. Individual growth rates were similar at both sites, whereas edge populations showed a higher relative investment in reproduction (demonstrated by a higher reproductive allocation and extended reproductive periods) when compared to central populations that invested more in defence. These results show the capability of A. nodosum to differentially allocate resources for different traits under different habitat conditions, suggesting that reproduction and defence have different fitness values under the specific living conditions experienced at edge and central locations. However, ongoing climate change may threaten edge populations by increasing the selective pressure on specific traits, forcing these populations to lower the investment in other traits that are also potentially important for population fitness.     

Latitudinal variation in soil nematode communities under climate warming‐related range‐expanding and native plants

Current climate change has led to latitudinal and altitudinal range expansions of numerous species. During such range expansions, plant species are expected to experience changes in interactions with other organisms, especially with belowground biota that have a limited dispersal capacity. Nematodes form a key component of the belowground food web as they include bacterivores, fungivores, omnivores and root herbivores. However, their community composition under climate change‐driven intracontinental range‐expanding plants has been studied almost exclusively under controlled conditions, whereas little is known about actual patterns in the field. Here, we use novel molecular sequencing techniques combined with morphological quantification in order to examine nematode communities in the rhizospheres of four range‐expanding and four congeneric native species along a 2,000 km latitudinal transect from South‐Eastern to North‐Western Europe. We tested the hypotheses that latitudinal shifts in nematode community composition are stronger in range‐expanding plant species than in congeneric natives and that in their new range, range‐expanding plant species accumulate fewest root‐feeding nematodes. Our results show latitudinal variation in nematode community composition of both range expanders and native plant species, while operational taxonomic unit richness remained the same across ranges. Therefore, range‐expanding plant species face different nematode communities at higher latitudes, but this is also the case for widespread native plant species. Only one of the four range‐expanding plant species showed a stronger shift in nematode community composition than its congeneric native and accumulated fewer root‐feeding nematodes in its new range. We conclude that variation in nematode community composition with increasing latitude occurs for both range‐expanding and native plant species and that some range‐expanding plant species may become released from root‐feeding nematodes in the new range.     

Fitness declines towards range limits and local adaptation to climate affect dispersal evolution during climate‐induced range shifts

Dispersal ability will largely determine whether species track their climatic niches during climate change, a process especially important for populations at contracting (low‐latitude/low‐elevation) range limits that otherwise risk extinction. We investigate whether dispersal evolution at contracting range limits is facilitated by two processes that potentially enable edge populations to experience and adjust to the effects of climate deterioration before they cause extinction: (i) climate‐induced fitness declines towards range limits and (ii) local adaptation to a shifting climate gradient. We simulate a species distributed continuously along a temperature gradient using a spatially explicit, individual‐based model. We compare range‐wide dispersal evolution during climate stability vs. directional climate change, with uniform fitness vs. fitness that declines towards range limits (RLs), and for a single climate genotype vs. multiple genotypes locally adapted to temperature. During climate stability, dispersal decreased towards RLs when fitness was uniform, but increased when fitness declined towards RLs, due to highly dispersive genotypes maintaining sink populations at RLs, increased kin selection in smaller populations, and an emergent fitness asymmetry that favoured dispersal in low‐quality habitat. However, this initial dispersal advantage at low‐fitness RLs did not facilitate climate tracking, as it was outweighed by an increased probability of extinction. Locally adapted genotypes benefited from staying close to their climate optima; this selected against dispersal under stable climates but for increased dispersal throughout shifting ranges, compared to cases without local adaptation. Dispersal increased at expanding RLs in most scenarios, but only increased at the range centre and contracting RLs given local adaptation to climate.     

Racing against change: understanding dispersal and persistence to improve species' conservation prospects

Climate change is contributing to the widespread redistribution, and increasingly the loss, of species. Geographical range shifts among many species were detected rapidly after predictions of the potential importance of climate change were specified 35 years ago: species are shifting their ranges towards the poles and often to higher elevations in mountainous areas. Early tests of these predictions were largely qualitative, though extraordinarily rapid and broadly based, and statistical tests distinguishing between climate change and other global change drivers provided quantitative evidence that climate change had already begun to cause species’ geographical ranges to shift. I review two mechanisms enabling this process, namely development of approaches for accounting for dispersal that contributes to range expansion, and identification of factors that alter persistence and lead to range loss. Dispersal in the context of range expansion depends on an array of processes, like population growth rates in novel environments, rates of individual species movements to new locations, and how quickly areas of climatically tolerable habitat shift. These factors can be tied together in well-understood mathematical frameworks or modelled statistically, leading to better prediction of extinction risk as climate changes. Yet, species'' increasing exposures to novel climate conditions can exceed their tolerances and raise the likelihood of local extinction and consequent range losses. Such losses are the consequence of processes acting on individuals, driven by factors, such as the growing frequency and severity of extreme weather, that contribute local extinction risks for populations and species. Many mechanisms can govern how species respond to climate change, and rapid progress in global change research creates many opportunities to inform policy and improve conservation outcomes in the early stages of the sixth mass extinction.     

Modelling conservation management options for a southern range‐margin population of Golden Plover Pluvialis apricaria vulnerable to climate change

There is considerable interest in understanding how management may help species and populations cope with climate change (climate change adaptation). I used a population model describing the demography of a southern range‐margin European Golden Plover Pluvialis apricaria population vulnerable to climate change to assess the potential benefits associated with site‐based adaptation management. Two forms of management were simulated: (1) counteracting management to reduce the severity of the negative climate change impacts, simulated by increasing tipulid (cranefly) abundance, and (2) compensatory management to increase populations through an alternative mechanism, simulated by manipulating nest and chick predation rates. A 1 °C rise was estimated to require a doubling of cranefly abundance, or a 35% increase in nest and chick survival rates, to maintain a stable population. For a 2 °C rise, a four‐fold increase in craneflies or an 80% increase in survival rates would be required for population stability. A model based on likely realistic estimates of the magnitude of benefit associated with both adaptation management options showed that combined, they may significantly reduce the severity of population decline and risk of extinction associated with a relatively large increase in temperature of 5.8 °C above 1960–90 levels. Site‐based adaptation management may therefore increase the resistance of Golden Plovers to some degree of future climate change. This model framework for informing climate change adaptation decisions should be developed for other species and habitats.     

Signatures of local adaptation along environmental gradients in a range‐expanding damselfly (Ischnura elegans)

Insect distributions are shifting rapidly in response to climate change and are undergoing rapid evolutionary change. We investigate the molecular signatures underlying local adaptation in the range‐expanding damselfly, Ischnura elegans. Using a landscape genomic approach combined with generalized dissimilarity modelling (GDM), we detect selection signatures on loci via allelic frequency change along environmental gradients. We analyse 13,612 single nucleotide polymorphisms (SNPs), derived from restriction site‐associated DNA sequencing (RADseq), in 426 individuals from 25 sites spanning the I. elegans distribution in Sweden, including its expanding northern range edge. Environmental association analysis (EAA) and the magnitude of allele frequency change along the range expansion gradient revealed significant signatures of selection in relation to high maximum summer temperature, high mean annual precipitation and low wind speeds at the range edge. SNP annotations with significant signatures of selection revealed gene functions associated with ongoing range expansion, including heat shock proteins (HSP40 and HSP70), ion transport (V‐ATPase) and visual processes (long‐wavelength‐sensitive opsin), which have implications for thermal stress response, salinity tolerance and mate discrimination, respectively. We also identified environmental thresholds where climate‐mediated selection is likely to be strong, and indicate that I. elegans is rapidly adapting to the climatic environment during its ongoing range expansion. Our findings empirically validate an integrative approach for detecting spatially explicit signatures of local adaptation along environmental gradients.     

Conserving biodiversity under climate change: the rear edge matters

Modern climate change is producing poleward range shifts of numerous taxa, communities and ecosystems worldwide. The response of species to changing environments is likely to be determined largely by population responses at range margins. In contrast to the expanding edge, the low-latitude limit (rear edge) of species ranges remains understudied, and the critical importance of rear edge populations as long-term stores of species' genetic diversity and foci of speciation has been little acknowledged. We review recent findings from the fossil record, phylogeography and ecology to illustrate that rear edge populations are often disproportionately important for the survival and evolution of biota. Their ecological features, dynamics and conservation requirements differ from those of populations in other parts of the range, and some commonly recommended conservation practices might therefore be of little use or even counterproductive for rear edge populations.     

Species’ traits as predictors of range shifts under contemporary climate change: A review and meta‐analysis

A growing body of literature seeks to explain variation in range shifts using species’ ecological and life‐history traits, with expectations that shifts should be greater in species with greater dispersal ability, reproductive potential, and ecological generalization. Despite strong theoretical support for species’ traits as predictors of range shifts, empirical evidence from contemporary range shift studies remains limited in extent and consensus. We conducted the first comprehensive review of species’ traits as predictors of range shifts, collecting results from 51 studies across multiple taxa encompassing over 11,000 species’ responses for 54 assemblages of taxonomically related species occurring together in space. We used studies of assemblages that directly compared geographic distributions sampled in the 20th century prior to climate change with resurveys of distributions after contemporary climate change and then tested whether species traits accounted for heterogeneity in range shifts. We performed a formal meta‐analysis on study‐level effects of body size, fecundity, diet breadth, habitat breadth, and historic range limit as predictors of range shifts for a subset of 21 studies of 26 assemblages with sufficient data. Range shifts were consistent with predictions based on habitat breadth and historic range limit. However, body size, fecundity, and diet breadth showed no significant effect on range shifts across studies, and multiple studies reported significant relationships that contradicted predictions. Current understanding of species’ traits as predictors of range shifts is limited, and standardized study is needed for traits to be valid indicators of vulnerability in assessments of climate change impacts.     

Detrital traits affect substitutability of a range‐expanding foundation species across latitude

Climate‐driven range shifts of foundation species could alter ecosystem processes and community composition by providing different resources than resident foundation species. Along the US Atlantic coast, the northward expanding foundation species, black mangrove Avicennia germinans, is replacing the dominant salt marsh foundation species, marsh cordgrass Spartina alterniflora. These species have distinct detrital attributes that ostensibly provide different resources to epifauna. We experimentally examined how detritus of these species affects decomposition and community composition in different habitat contexts at regional and local scales. First, we manipulated detritus identity (Avicennia, Spartina) at 13 sites across a 5° latitudinal gradient spanning mangrove, mixed marsh‐mangrove and salt marsh habitats. Across latitude, we found that Avicennia detritus decomposed 2–4 times faster than Spartina detritus, suggesting that detrital turnover will increase with mangrove expansion. Epifaunal abundance and richness increased 2–7 times from south to north (mangrove to salt marsh) and were equivalent between Avicennia and Spartina detritus except for crabs, a dominant taxonomic group that preferred Spartina detritus. Second, to examine the whether changing habitat context affected regional patterns, we manipulated detritus identity and surrounding habitat type (mangrove, salt marsh) at a single mixed site, also including inert mimics to separate structural and nutritional roles of detritus. Epifaunal richness was similar between the two detrital types, but crabs were 2–7 times more abundant in Spartina detritus due to its structural attributes. Surrounding habitat type did not influence decomposition rate or community patterns, which suggests that latitudinal influences, not surrounding habitat, drove the regional community patterns in the first experiment. Overall, mangrove expansion could alter epifaunal communities due to the lower structural value and faster turnover of mangrove detritus. As species shift with changing climate, understanding foundation species substitutability is critical to predict community change, but we must account for concomitant environmental changes that also modify communities.     

Impacts of past habitat loss and future climate change on the range dynamics of South African Proteaceae

Aim

To assess how habitat loss and climate change interact in affecting the range dynamics of species and to quantify how predicted range dynamics depend on demographic properties of species and the severity of environmental change.

Location

South African Cape Floristic Region.

Methods

We use data‐driven demographic models to assess the impacts of past habitat loss and future climate change on range size, range filing and abundances of eight species of woody plants (Proteaceae). The species‐specific models employ a hybrid approach that simulates population dynamics and long‐distance dispersal on top of expected spatio‐temporal dynamics of suitable habitat.

Results

Climate change was mainly predicted to reduce range size and range filling (because of a combination of strong habitat shifts with low migration ability). In contrast, habitat loss mostly decreased mean local abundance. For most species and response measures, the combination of habitat loss and climate change had the most severe effect. Yet, this combined effect was mostly smaller than expected from adding or multiplying effects of the individual environmental drivers. This seems to be because climate change shifts suitable habitats to regions less affected by habitat loss. Interspecific variation in range size responses depended mostly on the severity of environmental change, whereas responses in range filling and local abundance depended mostly on demographic properties of species. While most surviving populations concentrated in areas that remain climatically suitable, refugia for multiple species were overestimated by simply overlying habitat models and ignoring demography.

Main conclusions

Demographic models of range dynamics can simultaneously predict the response of range size, abundance and range filling to multiple drivers of environmental change. Demographic knowledge is particularly needed to predict abundance responses and to identify areas that can serve as biodiversity refugia under climate change. These findings highlight the need for data‐driven, demographic assessments in conservation biogeography.

     

Role of selection and gene flow in population differentiation at the edge vs. interior of the species range differing in climatic conditions

Evaluating the relative importance of neutral and adaptive processes as determinants of population differentiation across environments is a central theme of evolutionary biology. We applied the Q_ST–F_ST comparison flanked by a direct test for local adaptation to infer the role of climate‐driven selection and gene flow in population differentiation of an annual grass Avena sterilis in two distinct parts of the species range, edge and interior, which represent two globally different climates, desert and Mediterranean. In a multiyear reciprocal transplant experiment, the plants of desert and Mediterranean origin demonstrated home advantage, and population differentiation in several phenotypic traits related to reproduction exceeded neutral predictions, as determined by comparisons of Q_ST values with theoretical F_ST distributions. Thus, variation in these traits likely resulted from local adaptation to desert and Mediterranean environments. The two separate common garden experiments conducted with different experimental design revealed that two population comparisons, in contrast to multi‐population comparisons, are likely to detect population differences in virtually every trait, but many of these differences reflect effects of local rather than regional environment. We detected a general reduction in neutral (SSR) genetic variation but not in adaptive quantitative trait variation in peripheral desert as compared with Mediterranean core populations. On the other hand, the molecular data indicated intensive gene flow from the Mediterranean core towards desert periphery. Although species range position in our study (edge vs. interior) was confounded with climate (desert vs. Mediterranean), the results suggest that the gene flow from the species core does not have negative consequences for either performance of the peripheral plants or their adaptive potential.     

Will northern fish populations be in hot water because of climate change?

Predicted increases in water temperature in response to climate change will have large implications for aquatic ecosystems, such as altering thermal habitat and potential range expansion of fish species. Warmwater fish species, such as smallmouth bass, Micropterus dolomieu , may have access to additional favourable thermal habitat under increased surface-water temperatures, thereby shifting the northern limit of the distribution of the species further north in Canada and potentially negatively impacting native fish communities. We assembled a database of summer surface-water temperatures for over 13 000 lakes across Canada. The database consists of lakes with a variety of physical, chemical and biological properties. We used general linear models to develop a nation-wide maximum lake surface-water temperature model. The model was extended to predict surface-water temperatures suitable to smallmouth bass and under climate-change scenarios. Air temperature, latitude, longitude and sampling time were good predictors of present-day maximum surface-water temperature. We predicted lake surface-water temperatures for July 2100 using three climate-change scenarios. Water temperatures were predicted to increase by as much as 18 °C by 2100, with the greatest increase in northern Canada. Lakes with maximum surface-water temperatures suitable for smallmouth bass populations were spatially identified. Under several climate-change scenarios, we were able to identify lakes that will contain suitable thermal habitat and, therefore, are vulnerable to invasion by smallmouth bass in 2100. This included lakes in the Arctic that were predicted to have suitable thermal habitat by 2100.