Between migration load and evolutionary rescue: dispersal,adaptation and the response of spatially structured populations to environmental change

The evolutionary potential of populations is mainly determined by population size and available genetic variance. However, the adaptability of spatially structured populations may also be affected by dispersal: positively by spreading beneficial mutations across sub-populations, but negatively by moving locally adapted alleles between demes. We develop an individual-based, two-patch, allelic model to investigate the balance between these opposing effects on a population''s evolutionary response to rapid climate change. Individual fitness is controlled by two polygenic traits coding for local adaptation either to the environment or to climate. Under conditions of selection that favour the evolution of a generalist phenotype (i.e. weak divergent selection between patches) dispersal has an overall positive effect on the persistence of the population. However, when selection favours locally adapted specialists, the beneficial effects of dispersal outweigh the associated increase in maladaptation for a narrow range of parameter space only (intermediate selection strength and low linkage among loci), where the spread of beneficial climate alleles is not strongly hampered by selection against non-specialists. Given that local selection across heterogeneous and fragmented landscapes is common, the complex effect of dispersal that we describe will play an important role in determining the evolutionary dynamics of many species under rapidly changing climate.     

Opinion: Is gene mapping in wild populations useful for understanding and predicting adaptation to global change?

Changing environmental conditions will inevitably alter selection pressures. Over the long term, populations have to adapt to these altered conditions by evolutionary change to avoid extinction. Quantifying the ‘evolutionary potential’ of populations to predict whether they will be able to adapt fast enough to forecasted changes is crucial to fully assess the threat for biodiversity posed by climate change. Technological advances in sequencing and high‐throughput genotyping have now made genomic studies possible in a wide range of species. Such studies, in theory, allow an unprecedented understanding of the genomics of ecologically relevant traits and thereby a detailed assessment of the population's evolutionary potential. Aimed at a wider audience than only evolutionary geneticists, this paper gives an overview of how gene‐mapping studies have contributed to our understanding and prediction of evolutionary adaptations to climate change, identifies potential reasons why their contribution to understanding adaptation to climate change may remain limited, and highlights approaches to study and predict climate change adaptation that may be more promising, at least in the medium term.     

Non-climatic thermal adaptation: implications for species' responses to climate warming

There is considerable interest in understanding how ectothermic animals may physiologically and behaviourally buffer the effects of climate warming. Much less consideration is being given to how organisms might adapt to non-climatic heat sources in ways that could confound predictions for responses of species and communities to climate warming. Although adaptation to non-climatic heat sources (solar and geothermal) seems likely in some marine species, climate warming predictions for marine ectotherms are largely based on adaptation to climatically relevant heat sources (air or surface sea water temperature). Here, we show that non-climatic solar heating underlies thermal resistance adaptation in a rocky–eulittoral-fringe snail. Comparisons of the maximum temperatures of the air, the snail''s body and the rock substratum with solar irradiance and physiological performance show that the highest body temperature is primarily controlled by solar heating and re-radiation, and that the snail''s upper lethal temperature exceeds the highest climatically relevant regional air temperature by approximately 22°C. Non-climatic thermal adaptation probably features widely among marine and terrestrial ectotherms and because it could enable species to tolerate climatic rises in air temperature, it deserves more consideration in general and for inclusion into climate warming models.     

Mutational collapse of fitness in marginal habitats and the evolution of ecological specialisation

In spatially heterogeneous environments, natural selection for maintenance of adaptation to habitats that contribute little to the population's reproduction is weak. In this paper we model a mechanism that can result in loss of fitness in such marginal habitats, and thus lead to specialisation on the main habitat. It involves accumulation of mutations that are deleterious in the marginal habitat but neutral or nearly so in the main habitat (mutations deleterious in the main habitat and neutral in the marginal habitat have a negligible influence). If the contribution of the marginal habitat to total reproduction in the absence of the mutations is less than a threshold value, selection is too weak to counter accumulation of such mutations. A positive feedback then results in loss of fitness in the marginal habitat. This mechanism does not require antagonistic pleiotropy in adaptation to different habitats, although antagonistic pleiotropy facilitates the mutational collapse of fitness in the marginal habitat. We suggest that deleterious mutations with habitat-specific expression may play a role in the evolution of ecological specialisation and promote evolutionary conservatism of ecological niches.     

Evolved dispersal strategies at range margins

Dispersal is a key component of a species''s ecology and will be under different selection pressures in different parts of the range. For example, a long-distance dispersal strategy suitable for continuous habitat at the range core might not be favoured at the margin, where the habitat is sparse. Using a spatially explicit, individual-based, evolutionary simulation model, the dispersal strategies of an organism that has only one dispersal event in its lifetime, such as a plant or sessile animal, are considered. Within the model, removing habitat, increasing habitat turnover, increasing the cost of dispersal, reducing habitat quality or altering vital rates imposes range limits. In most cases, there is a clear change in the dispersal strategies across the range, although increasing death rate towards the margin has little impact on evolved dispersal strategy across the range. Habitat turnover, reduced birth rate and reduced habitat quality all increase evolved dispersal distances at the margin, while increased cost of dispersal and reduced habitat density lead to lower evolved dispersal distances at the margins. As climate change shifts suitable habitat poleward, species ranges will also start to shift, and it will be the dispersal capabilities of marginal populations, rather than core populations, that will influence the rate of range shifting.     

Evolution of local facilitation in arid ecosystems

In harsh environments, sessile organisms can make their habitat more hospitable by buffering environmental stress or increasing resource availability. Although the ecological significance of such local facilitation is widely established, the evolutionary aspects have been seldom investigated. Yet addressing the evolutionary aspects of local facilitation is important because theoretical studies show that systems with such positive interactions can exhibit alternative stable states and that such systems may suddenly become extinct when they evolve (evolutionary suicide). Arid ecosystems currently experience strong changes in climate and human pressures, but little is known about the effects of these changes on the selective pressures exerted on the vegetation. Here, we focus on the evolution of local facilitation in arid ecosystems, using a lattice-structured model explicitly considering local interactions among plants. We found that the evolution of local facilitation depends on the seed dispersal strategy. In systems characterized by short-distance seed dispersal, adaptation to a more stressful environment leads to high local facilitation, allowing the population to escape extinction. In contrast, systems characterized by long-distance seed dispersal become extinct under increased stress even when allowed to adapt. In this case, adaptation in response to climate change and human pressures could give the final push to the desertification of arid ecosystems.     

Predicting patterns of long‐term adaptation and extinction with population genetics

Population genetics struggles to model extinction; standard models track the relative rather than absolute fitness of genotypes, while the exceptions describe only the short‐term transition from imminent doom to evolutionary rescue. But extinction can result from failure to adapt not only to catastrophes, but also to a backlog of environmental challenges. We model long‐term adaptation to long series of small challenges, where fitter populations reach higher population sizes. The population's long‐term fitness dynamic is well approximated by a simple stochastic Markov chain model. Long‐term persistence occurs when the rate of adaptation exceeds the rate of environmental deterioration for some genotypes. Long‐term persistence times are consistent with typical fossil species persistence times of several million years. Immediately preceding extinction, fitness declines rapidly, appearing as though a catastrophe disrupted a stably established population, even though gradual evolutionary processes are responsible. New populations go through an establishment phase where, despite being demographically viable, their extinction risk is elevated. Should the population survive long enough, extinction risk later becomes constant over time.     

Population dynamics can be more important than physiological limits for determining range shifts under climate change

Evidence is accumulating that species' responses to climate changes are best predicted by modelling the interaction of physiological limits, biotic processes and the effects of dispersal‐limitation. Using commercially harvested blacklip (Haliotis rubra) and greenlip abalone (Haliotis laevigata) as case studies, we determine the relative importance of accounting for interactions among physiology, metapopulation dynamics and exploitation in predictions of range (geographical occupancy) and abundance (spatially explicit density) under various climate change scenarios. Traditional correlative ecological niche models (ENM) predict that climate change will benefit the commercial exploitation of abalone by promoting increased abundances without any reduction in range size. However, models that account simultaneously for demographic processes and physiological responses to climate‐related factors result in future (and present) estimates of area of occupancy (AOO) and abundance that differ from those generated by ENMs alone. Range expansion and population growth are unlikely for blacklip abalone because of important interactions between climate‐dependent mortality and metapopulation processes; in contrast, greenlip abalone should increase in abundance despite a contraction in AOO. The strongly non‐linear relationship between abalone population size and AOO has important ramifications for the use of ENM predictions that rely on metrics describing change in habitat area as proxies for extinction risk. These results show that predicting species' responses to climate change often require physiological information to understand climatic range determinants, and a metapopulation model that can make full use of this data to more realistically account for processes such as local extirpation, demographic rescue, source‐sink dynamics and dispersal‐limitation.     

Evolution in response to climate change: In pursuit of the missing evidence

Climate change is imposing intensified and novel selection pressures on organisms by altering abiotic and biotic environmental conditions on Earth, but studies demonstrating genetic adaptation to climate change mediated selection are still scarce. Evidence is accumulating to indicate that both genetic and ecological constrains may often limit populations' abilities to adapt to large scale effects of climate warming. These constraints may predispose many organisms to respond to climate change with range shifts and phenotypic plasticity, rather than through evolutionary adaptation. In general, broad conclusions about the role of evolutionary adaptation in mitigating climate change induced fitness loss in the wild are as yet difficult to make. Editor's suggested further reading in BioEssays: How will fish that evolved at constant sub‐zero temperatures cope with global warming? Notothenioids as a case study Abstract     

Wrong place,wrong time: climate change‐induced range shift across fragmented habitat causes maladaptation and declined population size in a modelled bird species

Many species are locally adapted to decreased habitat quality at their range margins, and therefore show genetic differences throughout their ranges. Under contemporary climate change, range shifts may affect evolutionary processes at the expanding range margin due to founder events. In addition, populations that are affected by such founder events will, in the course of time, become located in the range centre. Recent studies investigated evolutionary changes at the expanding range margin, but have not assessed eventual effects across the species' range. We explored the possible influence of range shift on the level of adaptation throughout the species' total range. For this we used a spatially explicit, individual‐based simulation model of a woodland bird, parameterized after the middle spotted woodpecker ( Dendrocopos medius) in fragmented habitat. We simulated its range under climate change, and incorporated genetic differences at a single locus that determined the individual's degree of adaptation to optimal temperature conditions. Generalist individuals had a large thermal tolerance, but relatively low overall fitness, whereas climate specialists had high fitness combined with a small thermal tolerance. In equilibrium, the populations in the range centre were comprised of the specialists, whereas the generalists dominated the margins. In contrast, under temperature increase, the generalist numbers increased at the expanding margin and eventually also occupied the centre of the shifting range, whereas the specialists were located in the retracting margins. This was caused by founder events and led to overall maladaptation of the species, which resulted in a reduced metapopulation size and thus impeded the species' persistence. We therefore found no evidence for a complementary effect of local adaptation and range shifts on species' survival. Instead, we showed that founder events can cause local maladaptation which can amplify throughout the species' range, and, as such, hamper the species' persistence under climate change.     

Breeding ground temperature rises,more than habitat change,are associated with spatially variable population trends in two species of migratory bird

Habitat loss and climate change are key drivers of global biodiversity declines but their relative importance has rarely been examined. We attempted to attribute spatially divergent population trends of two Afro-Palaearctic migrant warbler species, Willow Warbler Phylloscopus trochilus and Common Chiffchaff Phylloscopus collybita, to changes in breeding grounds climate or habitat. We used bird counts from over 4000 sites across the UK between 1994 and 2017, monitored as part of the BTO/JNCC/RSPB Breeding Bird Survey. We modelled Willow Warbler and Common Chiffchaff population size and growth in relation to habitat, climate and weather. We then used the abundance model coefficients and observed environmental changes to determine the extent to which spatially varying population trends in England and Scotland were consistent with attribution to climate and habitat changes. Both species' population size and growth correlated with habitat, climate and weather on their breeding grounds. Changes in habitat, in particular woodland expansion, could be linked to small population increases for both species in England and Scotland. Both species' populations correlated more strongly with climate than weather, and both had an optimum breeding season temperature: 11°C for Willow Warbler and around 13.5°C for Common Chiffchaff (with marginally different predictions from population size and growth models). Breeding ground temperature increases, therefore, had the potential to have caused some of the observed Willow Warbler declines in England (where the mean breeding season temperature was 12.7°C) and increases in Scotland (mean breeding season temperature was 10.2°C), and some of the differential rates of increase for Common Chiffchaff. However, much of the variation in species' population abundance and trends were not well predicted by our models and could be due to other factors, such as species interactions, habitat and climate change in their wintering grounds and on migration. This study provides evidence that the effect of climate change on a species may vary spatially and may switch from being beneficial to being detrimental if a temperature threshold is exceeded.     

The Speed of Range Shifts in Fragmented Landscapes

Species may be driven extinct by climate change, unless their populations are able to shift fast enough to track regions of suitable climate. Shifting will be faster as the proportion of suitable habitat in the landscape increases. However, it is not known how the spatial arrangement of habitat will affect the speed of range advance, especially when habitat is scarce, as is the case for many specialist species. We develop methods for calculating the speed of advance that are appropriate for highly fragmented, stochastic systems. We reveal that spatial aggregation of habitat tends to reduce the speed of advance throughout a wide range of species parameters: different dispersal distances and dispersal kernel shapes, and high and low extinction probabilities. In contrast, aggregation increases the steady-state proportion of habitat that is occupied (without climate change). Nonetheless, we find that it is possible to achieve both rapid advance and relatively high patch occupancy when the habitat has a “channeled” pattern, resembling corridors or chains of stepping stones. We adapt techniques from electrical circuit theory to predict the rate of advance efficiently for complex, realistic landscape patterns, whereas the rate cannot be predicted by any simple statistic of aggregation or fragmentation. Conservationists are already advocating corridors and stepping stones as important conservation tools under climate change, but they are vaguely defined and have so far lacked a convincing basis in fundamental population biology. Our work shows how to discriminate properties of a landscape''s spatial pattern that affect the speed of colonization (including, but not limited to, patterns like corridors and chains of stepping stones), and properties that affect a species'' probability of persistence once established. We can therefore point the way to better land use planning approaches, which will provide functional habitat linkages and also maintain local population viability.     

Dispersal is associated with morphological innovation,but not increased diversification,in Cyphostemma (Vitaceae)

Multiple processes − including dispersal, morphological innovation, and habitat change − are frequently cited as catalysts for increased diversification. We investigate these processes and the causal linkages among them in the genus Cyphostemma (Vitaceae), a clade comprising ∼200 species that is unique in the Vitaceae for its diversity of growth habits. We reconstruct time‐calibrated evolutionary relationships among 64 species in the genus using five nuclear and chloroplast markers and infer the group's morphological and biogeographic history. We test for changes in speciation rate and evaluate the temporal association and sequencing of events with respect to dispersal, habitat change, and morphological evolution using a Monte Carlo simulation approach. In Cyphostemma, neither dispersal nor morphological evolution is associated with shifts in speciation rate, but dispersal is associated with evolutionary shifts in growth form. Evolution of stem succulence, in particular, is associated with adaptation to local, pre‐existing conditions following long‐distance dispersal, not habitat change in situ. We suggest that the pattern of association between dispersal, morphological innovation, and diversification may depend on the particular characters under study. Lineages with evolutionarily labile characters, such as stem succulence, do not necessarily conform to the notion of niche conservatism and instead demonstrate remarkable morphological adaptation to local climate and edaphic conditions following dispersal.     

Adaptation of timing of life history traits and population dynamic responses to climate change in spatially structured populations

Changes in the seasonal timing of life history events are documented effects of climate change. We used a general model to study how dispersal and competitive interactions affect eco-evolutionary responses to changes in the temporal distribution of resources over the season. Specifically, we modeled adaptation of the timing of reproduction and population dynamic responses in two competing populations that disperse between two habitats characterized by an early and late resource peak. We investigated three scenarios of environmental change: (1) food peaks advance in both habitats, (2) in the late habitat only and (3) in the early habitat only. At low dispersal rates the evolutionarily stable timing of reproduction closely matched the local resource peak and the environmental change typically caused population decline. Larger dispersal rates rendered less intuitive eco-evolutionary population responses. First, dispersal caused mismatch between evolutionarily stable timing of reproduction and local resource peaks and as a result, reproductive output for subpopulations could increase as well as decrease when resource availability underwent temporal shifts. Second, population responses were contingent on competition between populations. This could accelerate population declines and cause extinctions or even reverse population trends from negative to positive compared to the low dispersal case. When dispersal rate was large and the early resource peak was advanced available niche space was reduced. Hence, even when a population survived the environmental change and obtained positive equilibrium population density, subsequent adaptation of competing populations could drive it to extinction due to convergent evolution and competitive exclusion. These results shed new light on the role of competition and dispersal for the evolution of timing of life history events and provide guidelines for understanding short and long-term population response to climate change.     

Intact landscape promotes gene flow and low genetic structuring in the threatened Eastern Massasauga Rattlesnake

Genetic structuring of wild populations is dependent on environmental, ecological, and life‐history factors. The specific role environmental context plays in genetic structuring is important to conservation practitioners working with rare species across areas with varying degrees of fragmentation. We investigated fine‐scale genetic patterns of the federally threatened Eastern Massasauga Rattlesnake (Sistrurus catenatus) on a relatively undisturbed island in northern Michigan, USA. This species often persists in habitat islands throughout much of its distribution due to extensive habitat loss and distance‐limited dispersal. We found that the entire island population exhibited weak genetic structuring with spatially segregated variation in effective migration and genetic diversity. The low level of genetic structuring contrasts with previous studies in the southern part of the species’ range at comparable fine scales (~7 km), in which much higher levels of structuring were documented. The island population''s genetic structuring more closely resembles that of populations from Ontario, Canada, that occupy similarly intact habitats. Intrapopulation variation in effective migration and genetic diversity likely corresponds to the presence of large inland lakes acting as barriers and more human activity in the southern portion of the island. The observed genetic structuring in this intact landscape suggests that the Eastern Massasauga is capable of sufficient interpatch movements to reduce overall genetic structuring and colonize new habitats. Landscape mosaics with multiple habitat patches and localized barriers (e.g., large water bodies or roads) will promote gene flow and natural colonization for this declining species.     

ROLE OF SEX AND MIGRATION IN ADAPTATION TO SINK ENVIRONMENTS

Understanding the effects of sex and migration on adaptation to novel environments remains a key problem in evolutionary biology. Using a single‐cell alga Chlamydomonas reinhardtii, we investigated how sex and migration affected rates of evolutionary rescue in a sink environment, and subsequent changes in fitness following evolutionary rescue. We show that sex and migration affect both the rate of evolutionary rescue and subsequent adaptation. However, their combined effects change as the populations adapt to a sink habitat. Both sex and migration independently increased rates of evolutionary rescue, but the effect of sex on subsequent fitness improvements, following initial rescue, changed with migration, as sex was beneficial in the absence of migration but constraining adaptation when combined with migration. These results suggest that sex and migration are beneficial during the initial stages of adaptation, but can become detrimental as the population adapts to its environment.     

Ancient woodland indicators signal the climate change risk for dispersal-limited species

The climate change risk to biodiversity operates alongside a range of anthropogenic pressures. These include habitat loss and fragmentation, which may prevent species from migrating between isolated habitat patches in order to track their suitable climate space. Predictive modelling has advanced in scope and complexity to integrate: (i) projected shifts in climate suitability, with (ii) spatial patterns of landscape habitat quality and rates of dispersal. This improved ecological realism is suited to data-rich model species, though its broader generalisation comes with accumulated uncertainties, e.g. incomplete knowledge of species response to variable habitat quality, parameterisation of dispersal kernels etc. This study adopts ancient woodland indicator species (lichen epiphytes) as a guild that couples relative simplicity with biological rigour. Subjectively-assigned indicator species were statistically tested against a binary habitat map of woodlands of known continuity (>250 yr), and bioclimatic models were used to demonstrate trends in their increased/decreased environmental suitability under conditions of ‘no dispersal’. Given the expectation of rapid climate change on ecological time-scales, no dispersal for ancient woodland indicators becomes a plausible assumption. The risk to ancient woodland indicators is spatially structured (greater in a relative continental compared to an oceanic climatic zone), though regional differences are weakened by significant variation (within regions) in woodland extent. As a corollary, ancient woodland indicators that are sensitive to projected climate change scenarios may be excellent targets for monitoring climate change impacts for biodiversity at a site-scale, including the outcome of strategic habitat management (climate change adaptation) designed to offset risk for dispersal-limited species.     

Habitat selection and the value of information in heterogenous landscapes

Despite the wide usage of the term information in evolutionary ecology, there is no general treatise between fitness (i.e. density‐dependent population growth) and selection of the environment sensu lato. Here we 1) initiate the building of a quantitative framework with which to examine the relationship between information use in spatially heterogeneous landscapes and density‐dependent population growth, and 2) illustrate its utility by applying the framework to an existing model of breeding habitat selection. We begin by linking information, as a process of narrowing choice, to population growth/fitness. Second, we define a measure of a population's penalty of ignorance based on the Kullback–Leibler index that combines the contributions of resource selection (i.e. biased use of breeding sites) and density‐dependent depletion. Third, we quantify the extent to which environmental heterogeneity (i.e. mean and variance within a landscape) constrains sustainable population growth of unbiased agents. We call this the heterogeneity‐based fitness deficit, and combine this with population simulations to quantify the independent contribution of information‐use strategies to the total population growth rate. We further capitalize on this example to highlight the interactive effects of information between ecological scales when fear affects individual fitness through phenotypic plasticity. Informed breeding habitat selection moderates the demographic cost of fear commensurate with density‐dependent information use. Thus, future work should attempt to differentiate between phenotypic plasticity (i.e. acute fear) and demographic responses (i.e. chronic changes in population size). We conclude with a broader discussion of information in alternative contexts, and explore some evolutionary considerations for information use. We note how competition among individuals may constrain the information state among individuals, and the implications of this constraint under environmental change.     

Synchrony of butterfly populations across species' geographic ranges

Understanding the mechanisms by which global climate change and habitat loss impact upon biodiversity is essential in order to mitigate any negative impacts. One such impact may be changes to population synchrony (defined as correlated fluctuations in the density of separate populations). It is well established that synchrony depends on both dispersal ability and correlated environmental conditions, for example shared climate. However, what is not clear is whether differences in habitat or position within a species' range also mediate synchrony. Since synchronous metapopulations are thought to be more extinction‐prone, establishing the drivers of synchrony has clear conservation implications. Using three butterfly species (Maniola jurtina, Pyronia tithonus and Aphantopus hyperantus) we investigated the effects of habitat similarity and range position on population synchrony, after accounting for the effects of distance and climate. Range position was present in all minimum adequate models, though non‐significant using Mantel randomization tests in one case. We show that M. jurtina and P. tithonus synchrony is not consistent across species' ranges, with marginal populations showing more synchronous dynamics. Increased climatic constraints on marginal populations, leading to a narrower range of suitable microhabitats may be responsible for this, which is supported by the result that habitat similarity between sites was also positively correlated with population synchrony. As the landscape becomes increasingly homogeneous, overall population synchrony may be expected to rise. We conclude that habitat modification and climate change have the capacity to drive changes in population synchrony that could make species more vulnerable to extinction.