STRESS, EXTINCTIONS AND EVOLUTIONARY CHANGE: FROM LIVING ORGANISMS TO FOSSILS

1. Natural populations are exposed to environmental stress of varying intensities. This provides a reference point for extrapolations from the living biota to fossils and vice versa. 2. Evolutionary change is likely when there are resources in excess of maintenance and survival needs. It is largely precluded at species borders by the metabolic costs of stress; from this follows climatic tracking by species. 3. A relatively small increase in abiotic stress could underlie extinctions of stress-sensitive endemic species and the spread of stress-resistant generalist and widespread species. Widespread fossil species appear resistant to extinction under the stress level of normal background extinctions. 4. Synergistic interactions among generalized stresses should increase the likelihood of extinctions, especially for stresses with energetic consequences. 5. Some marine organisms survived the K-T mass extinction event because of stress-evasion mechanisms such as stress-resistant life-cycle stages with low metabolic rates. 6. In moderately stressed and narrowly fluctuating environments, sufficient genetic variability and metabolic energy should be available to permit adaptation. In these environments phyletic gradualism is expected. 7. In highly stressed and widely fluctuating environments, a punctuated evolutionary pattern is expected whereby stasis occurs most of the time. 8. Evolutionary patterns therefore can vary depending on the details of the interaction between stress, environmental fluctuations, energy availability and genetic variability. 9. Little evolutionary change is expected when the availability of energy is severely restricted. Examples include cave animals in stable but stressed environments and ‘living fossils’ in widely fluctuating but stressed environments. 10. Since the primary effect of abiotic stress may be at the level of energy carriers, a reductionist approach permits generalisations in considering extinctions and conditions under which diversification is likely.     

Environmental uncertainty, autocorrelation and the evolution of survival

Survival is a key fitness component and the evolution of age- and stage-specific patterns in survival is a central question in evolutionary biology. In variable environments, favouring chances of survival at the expense of other fitness components could increase fitness by spreading risk across uncertain conditions, especially if environmental conditions improve in the future. Both the magnitude of environmental variation and temporal autocorrelation in the environment might therefore affect the evolution of survival patterns. Despite this, the influence of temporal autocorrelation on the evolution of survival patterns has not been addressed. Here, we use a trade-off structure which reflects the empirically inspired paradigm of acquisition and allocation of resources to investigate how the evolutionarily stable survival probability is shaped in variable, density-dependent environments. We show that temporal autocorrelation is likely to be an important aspect of environmental variability that contributes to shaping age- and stage-specific patterns of survival probabilities in nature.     

No need for speed: slow development of fungi in extreme environments

Microbial growth under extreme conditions is often slow. This is partly because large amounts of energy are diverted into cellular mechanisms that allow survival under hostile conditions. Because this challenge is universal and diversity in extreme environments is low compared to non-extreme environments, slow-growing microorganisms are not overgrown by other species. In some cases, especially when nutrients are scarce, slow growth was even shown to increase stress tolerance. And in at least some species of extremotolerant and extremophilic fungi, growth rate appears to be coupled with their very unusual morphologies, which in turn may be an adaptation to extreme conditions. However, there is more than one strategy of survival in extreme environments. Fungi that thrive in extremes can be divided into (i) ubiquitous and polyextremotolerant generalists and (ii) rarely isolated specialists with narrow ecological amplitudes. While generalists can compete with mesophilic species, specialists cannot. When adapting to extreme conditions, the risk of an evolutionary trade-off in the form of reduced fitness under mesophilic conditions may limit the maximum stress tolerance achievable by polyextremotolerant generalists. At the same time, specialists are rarely found in mesophilic environments, which allows them to evolve to ever greater extremotolerance, since a reduction of mesophilic fitness is likely to have little impact on their evolutionary success.     

Constraints on adaptation of Escherichia coli to mixed‐resource environments increase over time

Can a population evolved in two resources reach the same fitness in both as specialist populations evolved in each of the individual resources? This question is central to theories of ecological specialization, the maintenance of genetic variation, and sympatric speciation, yet relatively few experiments have examined costs of generalism over long‐term adaptation. We tested whether selection in environments containing two resources limits a population's ability to adapt to the individual resources by comparing the fitness of replicate Escherichia coli populations evolved for 6000 generations in the presence of glucose or lactose alone (specialists), or in varying presentations of glucose and lactose together (generalists). We found that all populations had significant fitness increases in both resources, though the magnitude and rate of these increases differed. For the first 4000 generations, most generalist populations increased in fitness as quickly in the individual resources as the corresponding specialist populations. From 5000 generations, however, a widespread cost of adaptation affected all generalists, indicating a growing constraint on their abilities to adapt to two resources simultaneously. Our results indicate that costs of generalism are prevalent, but may influence evolutionary trajectories only after a period of cost‐free adaptation.     

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.     

Terrestrial insects and climate change: adaptive responses in key traits

Understanding and predicting how adaptation will contribute to species' resilience to climate change will be paramount to successfully managing biodiversity for conservation, agriculture, and human health‐related purposes. Making predictions that capture how species will respond to climate change requires an understanding of how key traits and environmental drivers interact to shape fitness in a changing world. Current trait‐based models suggest that low‐ to mid‐latitude populations will be most at risk, although these models focus on upper thermal limits, which may not be the most important trait driving species' distributions and fitness under climate change. In this review, we discuss how different traits (stress, fitness and phenology) might contribute and interact to shape insect responses to climate change. We examine the potential for adaptive genetic and plastic responses in these key traits and show that, although there is evidence of range shifts and trait changes, explicit consideration of what underpins these changes, be that genetic or plastic responses, is largely missing. Despite little empirical evidence for adaptive shifts, incorporating adaptation into models of climate change resilience is essential for predicting how species will respond under climate change. We are making some headway, although more data are needed, especially from taxonomic groups outside of Drosophila, and across diverse geographical regions. Climate change responses are likely to be complex, and such complexity will be difficult to capture in laboratory experiments. Moving towards well designed field experiments would allow us to not only capture this complexity, but also study more diverse species.     

The Definition and Measurement of Individual Condition in Evolutionary Studies

Over the past four decades, as the use of the term condition has become more frequent, the meaning of the term has become increasingly vague. This is especially true in evolutionary theory where condition is now equated with reproductive value, genetic quality, or defined as the ‘total pool of resources available for reproduction.’ Condition with the latter meaning is essentially impossible to measure empirically because it is associated with multiple attributes, such as nutritional state, health, experience, foraging success, ability to cope with environmental pressures, and social status, that collectively affect individual fitness. The addition of qualifying terms that often precede condition (e.g., phenotypic, energetic, and nutritional) and the usage of terms that describe an individual's state (e.g., physiological state, energetic state, and nutritional state) add confusion to the issue. It is therefore important to evaluate the meaning of condition, the limits of its usefulness, and how it can be best measured. We suggest using a more narrow definition of condition, amenable to empirical study, would benefit evolutionary and behavioral studies.     

Selection history and epistatic interactions impact dynamics of adaptation to novel environmental stresses

In rapidly changing environments, selection history may impact the dynamics of adaptation. Mutations selected in one environment may result in pleiotropic fitness trade-offs in subsequent novel environments, slowing the rates of adaptation. Epistatic interactions between mutations selected in sequential stressful environments may slow or accelerate subsequent rates of adaptation, depending on the nature of that interaction. We explored the dynamics of adaptation during sequential exposure to herbicides with different modes of action in Chlamydomonas reinhardtii. Evolution of resistance to two of the herbicides was largely independent of selection history. For carbetamide, previous adaptation to other herbicide modes of action positively impacted the likelihood of adaptation to this herbicide. Furthermore, while adaptation to all individual herbicides was associated with pleiotropic fitness costs in stress-free environments, we observed that accumulation of resistance mechanisms was accompanied by a reduction in overall fitness costs. We suggest that antagonistic epistasis may be a driving mechanism that enables populations to more readily adapt in novel environments. These findings highlight the potential for sequences of xenobiotics to facilitate the rapid evolution of multiple-drug and -pesticide resistance, as well as the potential for epistatic interactions between adaptive mutations to facilitate evolutionary rescue in rapidly changing environments.     

Evolutionarily stable range limits set by interspecific competition

A combination of abiotic and biotic factors probably restricts the range of many species. Recent evolutionary models and tests of those models have asked how a gradual change in environmental conditions can set the range limit, with a prominent idea being that gene flow disrupts local adaptation. We investigate how biotic factors, explicitly competition for limited resources, result in evolutionarily stable range limits even in the absence of the disruptive effect of gene flow. We model two competing species occupying different segments of the resource spectrum. If one segment of the resource spectrum declines across space, a species that specializes on that segment can be driven to extinction, even though in the absence of competition it would evolve to exploit other abundant resources and so be saved. The result is that a species range limit is set in both evolutionary and ecological time, as the resources associated with its niche decline. Factors promoting this outcome include: (i) inherent gaps in the resource distribution, (ii) relatively high fitness of the species when in its own niche, and low fitness in the alternative niche, even when resource abundances are similar in each niche, (iii) strong interspecific competition, and (iv) asymmetric interspecific competition. We suggest that these features are likely to be common in multispecies communities, thereby setting evolutionarily stable range limits.     

Evolutionary rescue and the limits of adaptation

Populations subject to severe stress may be rescued by natural selection, but its operation is restricted by ecological and genetic constraints. The cost of natural selection expresses the limited capacity of a population to sustain the load of mortality or sterility required for effective selection. Genostasis expresses the lack of variation that prevents many populations from adapting to stress. While the role of relative fitness in adaptation is well understood, evolutionary rescue emphasizes the need to recognize explicitly the importance of absolute fitness. Permanent adaptation requires a range of genetic variation in absolute fitness that is broad enough to provide a few extreme types capable of sustained growth under a stress that would cause extinction if they were not present. This principle implies that population size is an important determinant of rescue. The overall number of individuals exposed to selection will be greater when the population declines gradually under a constant stress, or is progressively challenged by gradually increasing stress. In gradually deteriorating environments, survival at lethal stress may be procured by prior adaptation to sublethal stress through genetic correlation. Neither the standing genetic variation of small populations nor the mutation supply of large populations, however, may be sufficient to provide evolutionary rescue for most populations.     

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     

Loss of adaptive variation during evolutionary responses to climate change

The changes in species' geographical distribution demanded by climate change are often critically limited by the availability of key interacting species. In such cases, species' persistence will depend on the rapid evolution of biotic interactions. Understanding evolutionary limits to such adaptation is therefore crucial for predicting biological responses to environmental change. The recent poleward range expansion of the UK brown argus butterfly has been associated with a shift in female preference from its main host plant, rockrose (Cistaceae), onto Geraniaceae host plants throughout its new distribution. Using reciprocal transplants onto natural host plants across the UK range, we demonstrate reduced fitness of females from recently colonised Geraniaceae‐dominated habitat when moved to ancestral rockrose habitats. By contrast, individuals from ancestral rockrose habitats show no reduction in fitness on Geraniaceae. Climate‐driven range expansion in this species is therefore associated with the rapid evolution of biotic interactions and a significant loss of adaptive variation.     

Testing for local adaptation and evolutionary potential along altitudinal gradients in rainforest Drosophila: beyond laboratory estimates

Predicting how species will respond to the rapid climatic changes predicted this century is an urgent task. Species distribution models (SDMs) use the current relationship between environmental variation and species’ abundances to predict the effect of future environmental change on their distributions. However, two common assumptions of SDMs are likely to be violated in many cases: (i) that the relationship of environment with abundance or fitness is constant throughout a species’ range and will remain so in future and (ii) that abiotic factors (e.g. temperature, humidity) determine species’ distributions. We test these assumptions by relating field abundance of the rainforest fruit fly Drosophila birchii to ecological change across gradients that include its low and high altitudinal limits. We then test how such ecological variation affects the fitness of 35 D. birchii families transplanted in 591 cages to sites along two altitudinal gradients, to determine whether genetic variation in fitness responses could facilitate future adaptation to environmental change. Overall, field abundance was highest at cooler, high‐altitude sites, and declined towards warmer, low‐altitude sites. By contrast, cage fitness (productivity) increased towards warmer, lower‐altitude sites, suggesting that biotic interactions (absent from cages) drive ecological limits at warmer margins. In addition, the relationship between environmental variation and abundance varied significantly among gradients, indicating divergence in ecological niche across the species’ range. However, there was no evidence for local adaptation within gradients, despite greater productivity of high‐altitude than low‐altitude populations when families were reared under laboratory conditions. Families also responded similarly to transplantation along gradients, providing no evidence for fitness trade‐offs that would favour local adaptation. These findings highlight the importance of (i) measuring genetic variation in key traits under ecologically relevant conditions, and (ii) considering the effect of biotic interactions when predicting species’ responses to environmental change.     

克隆植物的无性与有性繁殖对策

许多植物同时具有克隆生长与有性繁殖,两种繁殖方式间的平衡在不同物种间以及同一物种内不同种群间变化很大。旺盛的克隆生长可能会从多方面影响生活史进化。首先,许多克隆植物的有性繁殖与更新程度都很低,甚至有一些植物由于克隆生长而几乎完全放弃了有性过程,从而影响到克隆植物对局域环境的适应和地理范围进化。其次,克隆生长增大花展示进而增加了对传粉者的吸引,同时也增加了同株异花授粉的风险,而同株异花授粉往往会导致植物雄性和雌性适合度的下降。因此,克隆植物的空间结构与交配方式间可能存在着协同进化关系。最后,克隆生长与有性繁殖间可能存在着权衡关系:对克隆生长的资源投入将会减少对有性繁殖的资源投入。这种权衡关系可能是由环境条件、竞争力度、植物寿命和遗传等因素决定的。如果不同的繁殖方式是植物在不同环境下采取的适应性对策,那么我们可以预期:在波动和竞争力度大的生境中,植物应将大部分的繁殖资源分配给有性繁殖;而在相对稳定的环境中,克隆繁殖应该占据优势地位。但是自然选择对两种繁殖方式的选择结果是什么,以及控制这两种方式间平衡的生态和遗传因子究竟有哪些,到底是克隆生长单向地影响了植物的有性繁殖,还是与有性过程相伴随的选择压力同时塑造了植物的克隆习性?目前尚不清楚。同时从无性与有性繁殖两个方面综合考察克隆植物的繁殖对策是今后亟待加强的工作。     

Climate change and evolution: disentangling environmental and genetic responses

Rapid climate change is likely to impose strong selection pressures on traits important for fitness, and therefore, microevolution in response to climate-mediated selection is potentially an important mechanism mitigating negative consequences of climate change. We reviewed the empirical evidence for recent microevolutionary responses to climate change in longitudinal studies emphasizing the following three perspectives emerging from the published data. First, although signatures of climate change are clearly visible in many ecological processes, similar examples of microevolutionary responses in literature are in fact very rare. Second, the quality of evidence for microevolutionary responses to climate change is far from satisfactory as the documented responses are often - if not typically - based on nongenetic data. We reinforce the view that it is as important to make the distinction between genetic (evolutionary) and phenotypic (includes a nongenetic, plastic component) responses clear, as it is to understand the relative roles of plasticity and genetics in adaptation to climate change. Third, in order to illustrate the difficulties and their potential ubiquity in detection of microevolution in response to natural selection, we reviewed the quantitative genetic studies on microevolutionary responses to natural selection in the context of long-term studies of vertebrates. The available evidence points to the overall conclusion that many responses perceived as adaptations to changing environmental conditions could be environmentally induced plastic responses rather than microevolutionary adaptations. Hence, clear-cut evidence indicating a significant role for evolutionary adaptation to ongoing climate warming is conspicuously scarce.     

Many Possible Worlds: Expanding the Ecological Scenarios in Experimental Evolution

Experimental microbial evolution has focused on the particular ecological scenario where a population is placed suddenly in an environment where its fitness is low, and then adapts while the environment remains stable. In line with this, most microbial evolution studies use fitness measures that report how evolved genotypes fare when competed directly against their own distant ancestor while other studies compare life history traits (such as growth rates) of ancestral and evolved genotypes. This standard way of measuring and reporting changes in fitness has resulted in a consistent body of literature that explains adaptation when populations evolve in this “standard ecological scenario.” Here, I suggest that for experimental evolution to investigate adaptation in other ecological scenarios, such as fluctuating or persistently changing environments, measures of fitness must be expanded such that they not only continue to be comparable between experiments, but also account for evolution and demographic effects in all environments that an evolving lineage experiences. I examine two non-standard measures of fitness—fitness flux and the total number of reproductive events—as potential ways to quantify adaptation by integrating historical information about selection over many environments. This approach could allow us to make quantitative and biologically-meaningful comparisons of adaptation across diverse ecological scenarios. I use the case study of understanding how phytoplankton communities may respond to global change, where environmental variables change continuously, to explore concrete ways of using non-standard fitness measures that consider both demographic effects and selection in changing, rather than in changed, environments.     

Mechanisms of thermal adaptation and evolutionary potential of conspecific populations to changing environments

Heterogeneous and ever‐changing thermal environments drive the evolution of populations and species, especially when extreme conditions increase selection pressure for traits influencing fitness. However, projections of biological diversity under scenarios of climate change rarely consider evolutionary adaptive potential of natural species. In this study, we tested for mechanistic evidence of evolutionary thermal adaptation among ecologically divergent redband trout populations (Oncorhynchus mykiss gairdneri) in cardiorespiratory function, cellular response and genomic variation. In a common garden environment, fish from an extreme desert climate had significantly higher critical thermal maximum (p < .05) and broader optimum thermal window for aerobic scope (>3°C) than fish from cooler montane climate. In addition, the desert population had the highest maximum heart rate during warming (20% greater than montane populations), indicating improved capacity to deliver oxygen to internal tissues. In response to acute heat stress, distinct sets of cardiac genes were induced among ecotypes, which helps to explain the differences in cardiorespiratory function. Candidate genomic markers and genes underlying these physiological adaptations were also pinpointed, such as genes involved in stress response and metabolic activity (hsp40, ldh‐b and camkk2). These markers were developed into a multivariate model that not only accurately predicted critical thermal maxima, but also evolutionary limit of thermal adaptation in these specific redband trout populations relative to the expected limit for the species. This study demonstrates mechanisms and limitations of an aquatic species to evolve under changing environments that can be incorporated into advanced models to predict ecological consequences of climate change for natural organisms.     

Genetic and environment-induced pathways to innovation: on the possibility of a universal relationship between robustness and adaptation in complex biological systems

Recently, there has been considerable interest in the idea that mutational robustness enhances the propensity for future adaptations, i.e. evolvability, if evolution proceeds over a neutral network that extends far throughout a fitness landscape. While the genetic neutral network (NN-G) model may have important implications to our understanding of evolution, little has been done to integrate these theoretical developments with empirical evidence that heritable phenotypes can also originate and become fixated as a result of changes in the environment. In this brief commentary, I reconsider the role of environmental change in the adaptation of species and ask whether positive robustness-evolvability relationships might exist not only for genetic but also environmental buffering. In particular, I ask whether the insensitivity of species fitness towards variability in its environment can have a positive influence on the likelihood of future environment-induced adaptations (i.e. ecological opportunities) in a manner analogous to that proposed by the NN-G model. After outlining scenarios where such a counter-intuitive relationship appears plausible, I comment on the merits of evolutionary theories that can integrate complementary pathways to adaptation under static and time-variant environments. I also speculate on some of the features that such a theory might have.     

Simulation of the evolution of genomic complexity.

A general evolutionary trend is the generation of organisms of increasing complexity, notwithstanding that reduction and simplification phenomena do occur in the evolutionary process. This paper proposes an evolutionary model incorporating the mechanisms of gene amplification and deletion. The evolutionary process leading to genomic complexity and the coexistence of simpler organisms with complicated ones were both simulated using the proposed model. The model was also used to investigate the influence of various factors on the evolution of complexity. The simulations indicated that the evolution of complexity is largely influenced by adaptation to complicated environments. Nevertheless, complex organisms require relatively more resources for survival and replication, which limits the on going tendency towards complexity. Moreover, the analysis showed that if the environment varies rapidly and the profit obtained from complexity is greater than the resources consumed, selection will tend to favor complexity. However, high living cost will tend to limit the trend of complexity and if the environment is relatively stable, reduction and simplification will become the dominant trends.     

Can punishment maintain sex?

Individuals who reproduce asexually have a two-fold advantage over their sexually-reproducing counterparts as they are able to reproduce twice as fast. Explaining why sexual reproduction is favoured over asexual reproduction therefore remains an important challenge in evolutionary biology. Various mechanisms involving resistance to parasites, adaptation to novel environments and helping to purge the genome of deleterious mutations have all been proposed as potential mechanisms which could promote the evolution of sex. A recent article has suggested that spiteful males may help to reduce the two-fold advantage of asexual females. Here I discuss this idea, and further ask whether punishment of asexual females by sexual females could be one way in which sexual reproduction could be maintained in groups of animals; in light of recent research on the repression of competition, it could be possible that asexual females which reproduce faster than their sexual counterparts will be punished for using group resources. It may therefore be possible that the behaviour of sexual individuals towards asexual females could have fitness consequences which could potentially reduce the two-fold advantage they gain from reproducing parthenogenetically.