Evolutionary Rescue Research Articles

Sharp habitat shifts, evolutionary tipping points and rescue: Quantifying the perilous path of a specialist species towards a refugium in a changing environment

Specialist species thriving under specific environmental conditions in narrow geographic ranges are widely recognized as heavily threatened by climate deregulation. Many might rely on both their potential to adapt and to disperse towards a refugium to avoid extinction. It is thus crucial to understand the influence of environmental conditions on the unfolding process of adaptation. Here, I study the eco-evolutionary dynamics of a sexually reproducing specialist species in a two-patch quantitative genetic model with moving optima. Thanks to a separation of ecological and evolutionary time scales and the phase-line study of the selection gradient, I derive the critical environmental speed for persistence, which reflects how the existence of a refugium impacts extinction patterns and how it relates to the cost of dispersal. Moreover, the analysis provides key insights about the dynamics that arise on the path towards this refugium. I show that after an initial increase of population size, there exists a critical environmental speed above which the species crosses a tipping point, resulting into an abrupt habitat switch. In addition, when selection for local adaptation is strong, this habitat switch passes through an evolutionary “death valley”, leading to a phenomenon related to evolutionary rescue, which can promote extinction for lower environmental speeds than the critical one.

Evolutionary Adaptation in Heterogeneous and Changing Environments.

Organisms that are adapting to long term environmental change almost always deal with mul- tiple environments and trade-offs that affect their optimal phenotypic strategy. Here we combine the idea of repeated variation or heterogeneity, like seasonal shifts, with long-term directional dy- namics. Using the framework of fitness sets, we determine the dynamics of the optimal phenotype in two competing environments encountered with different frequencies, one of which changes with time. When such an optimal strategy is selected for in simulations of evolving populations, we observe rich behavior that is qualitatively different from and more complex than adaptation to long-term change in a single environment. The probability of survival and the critical rate of environmental change above which populations go extinct depend crucially on the relative fre- quency of the two environments and the strength and asymmetry of their selection pressures. We identify a critical frequency for the stationary environment, above which populations can escape the pressure to constantly evolve by adapting to the stationary optimum. In the neighborhood of this critical frequency, we also find the counter-intuitive possibility of a lower bound on the rate of environmental change, below which populations go extinct, and above which a process of evolutionary rescue is possible.

Warmer is better for evolutionary rescue, driving a warm-to-cold bias in habitat colonization dynamics.

Evolutionary rescue occurs when populations survive lethal environmental stresses through the rising and fixation of tolerant genotypes. Temperature has long been believed to determine the evolutionary speed of populations and species. Here, we suggest that warmer temperatures can facilitate evolutionary rescue. Moreover, with dispersal among habitats, the advantage in evolutionary rescue for warmer populations may cause a bias in habitat colonization dynamics towards the warm-to-cold direction. We experimentally tested these hypotheses with a model microbial system. Our first experiment showed that bacterial populations at warmer temperatures had a greater chance to evolve resistance and escape the fate of extinction under an antibiotic treatment. In the second experiment, metapopulations that consisted of warm and cold habitats were exposed to the antibiotic stress; local populations that went extinct might be recolonized, and such recolonization events were biased to the warm-to-cold direction. We also examined possible mechanisms underlying the temperature effect on the rapid evolution of resistance in our study system. Our results may help to understand the mechanisms of maintenance of biodiversity and patterns of gene flow among climatic regions, particularly in pest species subject to chemical control treatments.

The potential for evolutionary rescue in an Arctic seashore plant threatened by climate change.

The impacts of climate change may be particularly severe for geographically isolated populations, which must adjust through plastic responses or evolve. Here, we study an endangered Arctic plant, Primula nutans ssp. finmarchica, confined to Fennoscandian seashores and showing indications of maladaptation to warming climate. We evaluate the potential of these populations to evolve to facilitate survival in the rapidly warming Arctic (i.e. evolutionary rescue) by utilizing manual crossing experiments in a nested half-sibling breeding design. We estimate G-matrices, evolvability and genetic constraints in traits with potentially conflicting selection pressures. To explicitly evaluate the potential for climate change adaptation, we infer the expected time to evolve from a northern to a southern phenotype under different selection scenarios, using demographic and climatic data to relate expected evolutionary rates to projected rates of climate change. Our results indicate that, given the nearly 10-fold greater evolvability of vegetative than of floral traits, adaptation in these traits may take place nearly in concert with changing climate, given effective climate mitigation. However, the comparatively slow expected evolutionary modification of floral traits may hamper the evolution of floral traits to track climate-induced changes in pollination environment, compromising sexual reproduction and thus reducing the likelihood of evolutionary rescue.

Canids in a changing climate: predicting range shifts and evolutionary rescue under distinct future scenarios

Abstract Human land use and climate change have profoundly impacted species distributions, with approximately a quarter of all known mammal species currently facing extinction threats. In this study, we modelled both present and future potential distributions of all 36 extant Canidae species to assess their responses to moderate and pessimistic future climatic scenarios. Additionally, we investigated the likelihood of canids experiencing evolutionary rescue, which could facilitate adaptation to climate change for certain species. We gathered species occurrence data for all extant canids and corresponding environmental variables for these locations. Our modelling results reveal that 32 species (89% of Canidae species) are projected to undergo range contractions owing to climate change, whereas four species (11% of canids) are expected to expand their ranges. Evolutionary analyses suggest that some canids might lack the capacity to adapt to the rapid pace of climate change, particularly Atelocynus microtis and Vulpes velox. Furthermore, our findings underscore the critical importance of incorporating variables related to proximity to water bodies to predict the future distributions of South American canids accurately.

Genetic Independence of Naturally Correlated Variation in Resistance to Endemic and Novel Pathogens.

The emergence of new diseases is an urgent concern, but hosts can also vary in resistance to pathogens that are novel to them, facilitating evolutionary rescue. However, little is known about the genetic source for polymorphic resistance to novel pathogens or its relationship to defences against endemic diseases. With anther-smut disease from wild plant populations, we used selection experiments and genetic analyses to show that resistances to novel and endemic pathogens are genetically independent, despite being positively correlated in nature. Moreover, novel-pathogen resistance presented a much simpler genetic basis and more rapid response to selection. We demonstrate that polymorphic resistance to a newly introduced disease is genetically determined and not an extension of defences against the related endemic pathogen, challenging the conventional view of nonhost resistance.

Resource-based modelling approach to studying evolutionary rescue.

In this paper, we present an in-depth investigation into the dynamics of evolutionary rescue using a resource-based modelling approach. Utilizing classical consumer-resource models, we aim to understand how species can adapt to abrupt environmental changes that alter the availability of substitutable resources. Through both analytical solutions and simulation-based techniques, we explore the conditions under which populations can recover from critical sizes and avoid extinction. Our findings highlight the importance of minimum viable population sizes, mutation rates, and the adaptive capacity of metabolic strategies in influencing population resilience. We demonstrate that while increased mutation rates can facilitate faster recovery by enabling populations to evolve new metabolic strategies suited to the altered resource landscape, populations starting with smaller sizes or facing severe reductions in resource availability are more susceptible to extinction. This study offers valuable insights into the interplay between ecological dynamics and evolutionary mechanisms, providing a comprehensive framework for predicting population persistence and informing conservation strategies under changing environmental conditions.

Preventing evolutionary rescue in cancer.

First-line cancer treatment frequently fails due to initially rare therapeutic resistance. An important clinical question is then how to schedule subsequent treatments to maximize the probability of tumour eradication. Here, we provide a theoretical solution to this problem by using mathematical analysis and extensive stochastic simulations within the framework of evolutionary rescue theory to determine how best to exploit the vulnerability of small tumours to stochastic extinction. Whereas standard clinical practice is to wait for evidence of relapse, we confirm a recent hypothesis that the optimal time to switch to a second treatment is when the tumour is close to its minimum size before relapse, when it is likely undetectable. This optimum can lie slightly before or slightly after the nadir, depending on tumour parameters. Given that this exact time point may be difficult to determine in practice, we study windows of high extinction probability that lie around the optimal switching point, showing that switching after the relapse has begun is typically better than switching too early. We further reveal how treatment dose and tumour demographic and evolutionary parameters influence the predicted clinical outcome, and we determine how best to schedule drugs of unequal efficacy. Our work establishes a foundation for further experimental and clinical investigation of this evolutionarily-informed "extinction therapy" strategy.

Increasing environmental variability inhibits evolutionary rescue in a long-lived vertebrate

Evolutionary rescue, whereby adaptive evolutionary change rescues populations from extinction, is theorized to enable imperiled animal populations to persist under increasing anthropogenic change. Despite a large body of evidence in theoretical and laboratory settings, the potential for evolutionary rescue to be a viable adaptation process for free-ranging animals remains unknown. Here, we leverage a 38-year dataset following the fates of 53,959 Magellanic penguins (Spheniscus magellanicus) to investigate whether a free-ranging vertebrate species can morphologically adapt to long-term environmental change sufficiently to promote population persistence. Despite strong selective pressures, we found that penguins did not adapt morphologically to long-term environmental changes, leading to projected population extirpation. Fluctuating selection benefited larger penguins in some environmental contexts, and smaller penguins in others, ultimately mitigating their ability to adapt under increasing environmental variability. Under future climate projections, we found that the species cannot be rescued by adaptation, suggesting similar constraints for other long-lived species. Such results reveal how fluctuating selection driven by environmental variability can inhibit adaptation under long-term environmental change. Our eco-evolutionary approach helps explain the lack of adaptation and evolutionary rescue in response to environmental change observed in many animal species.

Neutral genetic structuring of pathogen populations during rapid adaptation.

Pathogen species are experiencing strong joint demographic and selective events, especially when they adapt to a new host, for example through overcoming plant resistance. Stochasticity in the founding event and the associated demographic variations hinder our understanding of the expected evolutionary trajectories and the genetic structure emerging at both neutral and selected loci. What would be the typical genetic signatures of such a rapid adaptation event is not elucidated. Here, we build a demogenetic model to monitor pathogen population dynamics and genetic evolution on two host compartments (susceptible and resistant). We design our model to fit two plant pathogen life cycles, 'with' and 'without' host alternation. Our aim is to draw a typology of eco-evolutionary dynamics. Using time-series clustering, we identify three main scenarios: 1) small variations in the pathogen population size and small changes in genetic structure, 2) a strong founder event on the resistant host that in turn leads to the emergence of genetic structure on the susceptible host, and 3) evolutionary rescue that results in a strong founder event on the resistant host, preceded by a bot- tleneck on the susceptible host. We pinpoint differences between life cycles with notably more evolutionary rescue 'with' host alternation. Beyond the selective event itself, the demographic trajectory imposes specific changes in the genetic structure of the pathogen population. Most of these genetic changes are transient, with a signature of resistance overcoming that vanishes within a few years only. Considering time-series is therefore of utmost importance to accurately decipher pathogen evolution.

The genetics of phenotypic plasticity. XVIII. Developmental limits restrict adaptive plasticity.

After environmental change, the trait evolution needed to rescue a population depends on the functional form of the plastic change (reaction norm) of that trait. Nearly all previous models of plasticity evolution for continuous traits have assumed that the functional form is linear, i.e., no limits on the range of plasticity. This paper examines the effect of developmental limits, modeled as a sigmoidal reaction norm, on evolutionary rescue after an abrupt environmental change and the subsequent evolution of plasticity, including genetic assimilation. We examined four different scenarios: (1) developmental limits only, (2) developmental limits plus a cost of plasticity, (3) developmental limits with developmental noise, and (4) developmental limits plus environmental variation. The probability of evolutionary rescue increased with an increase in phenotypic variation allowed by plastic development. With a smaller limit to the range of the plastic phenotype, the evolution of adaptive plasticity was limited, meaning the evolution of non-plastic genes was necessary. The addition of developmental constraints to the model did not speed up genetic assimilation, suggesting new theory is needed to understand empirical observations. The modeling framework presented here could be extended to different ecological and evolutionary conditions, alternative reaction norm shapes, the evolution of additional reaction norm parameters such as the range or the location of the inflection point on the environmental axis, or other function-valued traits.

Geographic variation in evolutionary rescue under climate change in a crop pest-predator system.

Species distribution models (SDMs) are often built upon the "niche conservatism" assumption, such that they ignore the possibility of "evolutionary rescue" and may underestimate species' future range limits under climate change. We select aphids and ladybirds as model species and develop an eco-evolutionary model to explore evolutionary rescue in a predator-prey system under climate change. We model the adaptive change of species' thermal performances, accounting for biotic interactions. Our study suggests that, without considering evolutionary adaptation, the warming climate will result in a reduction in aphid populations and the extinction of ladybirds in large parts of the United States. However, when incorporating evolutionary adaptation into the model, aphids can adapt to climate change, whereas ladybirds demonstrate geographic variation in their evolutionary rescue potential. Specifically, ladybirds in southern regions are more likely to be rescued than those in the north. In certain northern regions, ladybirds do not avoid extinction due to severe warming trends and seasonality of the climate. While higher warming trends do prompt stronger evolutionary changes in phenotype, they also lead to reduced aphid population abundance such that ecology constrains ladybird population growth. Higher seasonality induces an ecological effect by limiting the length of reproductive season, thereby reducing the capacity for evolutionary rescue. Together, these findings reveal the complex interplay between ecological and evolutionary dynamics in the context of evolutionary adaptation to climate change.

The role of epistasis in evolutionary rescue.

The process by which adaptive evolution preserves a population threatened with extinction due to environmental changes is known as evolutionary rescue. Several factors determine the fate of those populations, including demography and genetic factors, such as standing genetic variation, gene flow, availability of de novo mutations, and so on. Despite the extensive debate about evolutionary rescue in the current literature, a study about the role of epistasis and the topography of the fitness landscape on the fate of dwindling populations is missing. In the current work, we aim to fill this gap and study the influence of epistasis on the probability of extinction of populations. We present simulation results, and analytical approximations are derived. Counterintuitively, we show that the likelihood of extinction is smaller when the degree of epistasis is higher. The reason underneath is twofold: first, higher epistasis can promote mutations of more significant phenotypic effects, but also, the incongruence between the maps genotype-phenotype and phenotype-fitness turns the fitness landscape at low epistasis more rugged, thus curbing some of its advantages.

The limit to evolutionary rescue depends on ploidy in yeast exposed to nystatin.

The number of copies of each chromosome, or ploidy, of an organism is a major genomic factor affecting adaptation. We set out to determine how ploidy can impact the outcome of evolution, as well as the likelihood of evolutionary rescue, using short-term experiments with yeast (Saccharomyces cerevisiae) in a high concentration of the fungicide nystatin. In similar experiments using haploid yeast, the genetic changes underlying evolutionary rescue were highly repeatable, with all rescued lines containing a single mutation in the ergosterol biosynthetic pathway. All of these beneficial mutations were recessive, which led to the expectation that diploids would find alternative genetic routes to adaptation. To test this, we repeated the experiment using both haploid and diploid strains and found that diploid populations did not evolve resistance. Although diploids are able to adapt at the same rate as haploids to a lower, not fully inhibitory, concentration of nystatin, the present study suggests that diploids are limited in their ability to adapt to an inhibitory concentration of nystatin, while haploids may undergo evolutionary rescue. These results demonstrate that ploidy can tip the balance between adaptation and extinction when organisms face an extreme environmental change.

Evolutionary rescue in resistance to pesticides.

Evolutionary rescue occurs when the genetic evolution of adaptation saves a population from decline or extinction after environmental change. The evolution of resistance to pesticides is a special scenario of abrupt environmental change, where rescue occurs under (very) strong selection for one or a few de novo resistance mutations of large effect. Here, a population genetic model of evolutionary rescue with density-dependent population change is developed, with a focus on deriving results that are important to resistance management. Massive stochastic simulations are used to generate observations, which are accurately predicted using analytical approximations. Key results include the probability density function for the time to resistance and the probability of population extinction. The distribution of resistance times shows a lag period, a narrow peak and a long tail. Surprisingly, the mean time to resistance can increase with the strength of selection because, if a mutation does not occur early on, then its emergence is delayed by the pesticide reducing the population size. The probability of population extinction shows a sharp transition, in that when extinction is possible, it is also highly likely. Consequently, population suppression and (local) eradication can be theoretically achievable goals, as novel strategies to delay resistance evolution.

Deforestation limits evolutionary rescue under climate change in Amazonian lizards

AbstractAimThe impact of climate change on biodiversity is often analysed under a stable evolutionary perspective focused on whether species can currently tolerate warmer climates. However, species may adapt to changes, and particularly under conditions of low habitat fragmentation, standing adaptive genetic variation can spread across populations tracking changing climates, increasing the potential for evolutionary rescue. Here, our aim is to integrate genomic data, niche modelling and landscape ecology to predict range shifts and the potential for evolutionary rescue.LocationThe megadiverse Amazonian rainforest.MethodsWe use genome–environment association analyses to search for candidate loci under environmental selection, while accounting for neutral genetic variation in a widespread Amazonian whiptail lizard (Teiidae: Kentropyx calcarata). We then model the distribution of individuals with genotypes adapted to different climate conditions. We predict range shifts for each genotype in distinct future climate change scenarios by integrating this information with dispersal constraints based on predicted scenarios of forest cover across Amazonia. The predicted ranges of each genotype were then overlapped to infer the potential for evolutionary rescue.ResultsWe find that the potential for evolutionary rescue and, therefore, a smaller degree of range loss buffering extinction risk in the future is considerably high, provided that current forest cover is retained and climate change is not extreme. However, under extreme environmental change scenarios, range loss will be high in central and southern Amazonia, irrespective of the degree of deforestation.Main ConclusionsOur results suggest that protecting the Amazonian rainforest against further deforestation and mitigating climate change to moderate scenarios until 2070 could foster evolutionary rescue of ectothermic organisms. These actions could prevent substantial biodiversity loss in Amazonia, emphasizing the importance of understanding species adaptability in maintaining biodiversity.

Effect of the Seed Bank on Evolutionary Rescue in Small Populations: Univariate and Multivariate Demogenetic Dynamics.

AbstractUnder global change, the impact of seed banks on evolutionary rescue is uncertain. They buffer plant populations from demographic and genetic stochasticity but extend generation time and can become a reservoir of maladapted alleles. We built analytical and individual-based models to predict the effect of seed banks on the persistence of small annual plant populations facing an abrupt or sustained directional change in uni- or multivariate trait optima. Demogenetic dynamics predict that under most scenarios seed banks increase the lag yet enhance persistence to 200-250 years by absorbing demographic losses. Simulations indicate that the seed bank has a minimal impact on the genetic skew, although we suggest that this result could depend on the fitness component under selection. Our multivariate model reveals that by enlarging and reshaping the G matrix, seed banks can diminish the impact of mutational correlation and even accelerate adaptation under antagonistic pleiotropy relative to populations without a bank. We illustrate how the magnitude of optimum fluctuations, type and degree of optimum change, selection strength, and vital rates are weights that tip the scales determining persistence. Finally, our work highlights that migration from the past is not maladaptative when optimum fluctuations are large enough to create stepping stones to the new optimum.

Understanding Evolutionary Rescue and Parallelism in Response to Environmental Stress.

Evolutionary rescue, the process by which populations facing environmental stress avoid extinction through genetic adaptation, is a critical area of study in evolutionary biology. The order in which mutations arise and get established will be relevant to the population's rescue. This study investigates the degree of parallel evolution at the genotypic level between independent populations fac- ing environmental stress and subject to different demographic regimes. Under density regulation, two regimes exist: in the first, the population can restore positive growth rates by adjusting its population size or through adaptive mu- tations, whereas in the second regime, the population is doomed to extinction unless a rescue mutation occurs. Analytical approximations for the likelihood of evolutionary rescue are obtained and contrasted with simulation results. We show that the initial level of maladaptation and the demographic regime signifi- cantly affect the level of parallelism. There is an evident transition between these two regimes. Whereas in the first regime, parallelism decreases with the level of maladaptation, it displays the opposite behavior in the rescue/extinction regime. These findings have important implications for understanding population persis- tence and the degree of parallelism in evolutionary responses as they integrate demographic effects and evolutionary processes.

Pollution offsets the rapid evolution of increased heat tolerance in a natural population

Despite the increasing evidence for rapid thermal evolution in natural populations, evolutionary rescue under global warming may be constrained by the presence of other stressors. Highly relevant in our polluted planet, is the largely ignored evolutionary trade-off between heat tolerance and tolerance to pollutants. By using two subpopulations (separated 40 years in time) from a resurrected natural population of the water flea Daphnia magna that experienced a threefold increase in heat wave frequency during this period, we tested whether rapid evolution of heat tolerance resulted in reduced tolerance to the widespread metal zinc and whether this would affect heat tolerance upon exposure to the pollutant. Our results revealed rapid evolution of increased heat tolerance in the recent subpopulation. Notably, the sensitivity to the metal tended to be stronger (reduction in net energy budget) or was only present (reductions in heat tolerance and in sugar content) in the recent subpopulation. As a result, the rapidly evolved higher heat tolerance of the recent subpopulation was fully offset when exposed to zinc. Our results highlight that the many reports of evolutionary rescue to global change stressors may give a too optimistic view as our warming planet is polluted by metals and other pollutants.

Synergistic epistasis among cancer drivers can rescue early tumors from the accumulation of deleterious passengers.

Epistasis among driver mutations is pervasive and explains relevant features of cancer, such as differential therapy response and convergence towards well-characterized molecular subtypes. Furthermore, a growing body of evidence suggests that tumor development could be hampered by the accumulation of slightly deleterious passenger mutations. In this work, we combined empirical epistasis networks, computer simulations, and mathematical models to explore how synergistic interactions among driver mutations affect cancer progression under the burden of slightly deleterious passengers. We found that epistasis plays a crucial role in tumor development by promoting the transformation of precancerous clones into rapidly growing tumors through a process that is analogous to evolutionary rescue. The triggering of epistasis-driven rescue is strongly dependent on the intensity of epistasis and could be a key rate-limiting step in many tumors, contributing to their unpredictability. As a result, central genes in cancer epistasis networks appear as key intervention targets for cancer therapy.