Cryptic Evolution: Does Environmental Deterioration Have a Genetic Basis?

Cryptic evolution has been defined as adaptive evolutionary change being masked by concurrent environmental change. Empirical studies of cryptic evolution have usually invoked a changing climate and/or increasing population density as the form of detrimental environmental change experienced by a population undergoing cryptic evolution. However, Fisher (1958) emphasized that evolutionary change in itself is likely to be an important component of "environmental deterioration," a point restated by Cooke et al. (1990) in the context of intraspecific competition. In this form, environmental deterioration arises because a winning lineage has to compete against more winners in successive generations as the population evolves. This "evolutionary environmental deterioration" has different implications for the selection and evolution of traits influenced by resource competition than general environmental change. We reformulate Cooke's model as a quantitative genetic model to show that it is identical in form to more recent developments proposed by quantitative geneticists. This provides a statistical framework for discriminating between the alternative hypotheses of environmental change and environmental deterioration caused by evolutionary change. We also demonstrate that in systems where no phenotypic change has occurred, there are many reasonable biological processes that will generate patterns in predicted breeding values that are consistent with what has been interpreted as cryptic evolution, and care needs to be taken when interpreting these patterns. These processes include mutation, sib competition, and invisible fractions.     

Ancient origin of high taxonomic richness among insects

Insects are a hyper-diverse group, comprising nearly three-quarters of all named animal species on the Earth, but the environmental drivers of their richness and the roles of ecological interactions and evolutionary innovations remain unclear. Previous studies have argued that family-level insect richness increased continuously over the evolutionary history of the group, but inclusion of extant family records artificially inflated the relative richness of younger time intervals. Here we apply sampling-standardization methods to a species-level database of fossil insect occurrences, removing biases present in previous richness curves. We show that insect family-richness peaked 125 Ma and that Recent values are only 1.5–3 times as high as the Late Palaeozoic. Rarefied species-richness data also tentatively suggest little or no net increase in richness over the past 125 Myr. The Cretaceous peak in family richness was coincident with major radiations within extant groups but occurred prior to extinctions within more basal groups. Those extinctions may in part be linked to mid-Cretaceous floral turnover following the evolution of flowering plants. Negligible net richness change over the past 125 Myr implies that major radiations within extant groups were offset by reduced richness within groups that are now relict or extinct.     

Potential rapid evolution of foot morphology in Italian plethodontid salamanders (Hydromantes strinatii) following the colonization of an artificial cave

How organisms respond to environmental change is a long‐standing question in evolutionary biology. Species invading novel habitats provide an opportunity to examine contemporary evolution in action and decipher the pace of evolutionary change over short timescales. Here, we characterized phenotypic evolution in the Italian plethodontid salamander, Hydromantes strinatii, following the recent colonization of an artificial cave by a forest floor population. When compared with a nearby and genetically related population in the natural forest floor and a nearby cave population, the artificial cave population displayed significant differences in overall foot shape, with more interdigital webbing relative to the other populations. Further, this population evolved significantly larger feet, which corresponded more closely to those found in other cave populations than to forest floor populations to which the cave population is closely related. Finally, we quantified the rate of evolution for both foot shape and foot area, and found that both traits displayed large and significant evolutionary rates, at levels corresponding to other classic cases of rapid evolution in vertebrates. Together, these findings reveal that the response to novel environmental pressures can be large and rapid and that the anatomical shifts observed in the artificial cave population of H. strinatii may represent a case of rapid evolution in response to novel environmental pressures.     

Eco‐evolutionary dynamics in response to selection on life‐history

Understanding the consequences of environmental change on ecological and evolutionary dynamics is inherently problematic because of the complex interplay between them. Using invertebrates in microcosms, we characterise phenotypic, population and evolutionary dynamics before, during and after exposure to a novel environment and harvesting over 20 generations. We demonstrate an evolved change in life‐history traits (the age‐ and size‐at‐maturity, and survival to maturity) in response to selection caused by environmental change (wild to laboratory) and to harvesting (juvenile or adult). Life‐history evolution, which drives changes in population growth rate and thus population dynamics, includes an increase in age‐to‐maturity of 76% (from 12.5 to 22 days) in the unharvested populations as they adapt to the new environment. Evolutionary responses to harvesting are outweighed by the response to environmental change (~ 1.4 vs. 4% change in age‐at‐maturity per generation). The adaptive response to environmental change converts a negative population growth trajectory into a positive one: an example of evolutionary rescue.     

Natural history collections as windows on evolutionary processes

Natural history collections provide an immense record of biodiversity on Earth. These repositories have traditionally been used to address fundamental questions in biogeography, systematics and conservation. However, they also hold the potential for studying evolution directly. While some of the best direct observations of evolution have come from long‐term field studies or from experimental studies in the laboratory, natural history collections are providing new insights into evolutionary change in natural populations. By comparing phenotypic and genotypic changes in populations through time, natural history collections provide a window into evolutionary processes. Recent studies utilizing this approach have revealed some dramatic instances of phenotypic change over short timescales in response to presumably strong selective pressures. In some instances, evolutionary change can be paired with environmental change, providing a context for potential selective forces. Moreover, in a few cases, the genetic basis of phenotypic change is well understood, allowing for insight into adaptive change at multiple levels. These kinds of studies open the door to a wide range of previously intractable questions by enabling the study of evolution through time, analogous to experimental studies in the laboratory, but amenable to a diversity of species over longer timescales in natural populations.     

SLOWLY SWITCHING BETWEEN ENVIRONMENTS FACILITATES REVERSE EVOLUTION IN SMALL POPULATIONS

Natural populations must constantly adapt to ever‐changing environmental conditions. A particularly interesting question is whether such adaptations can be reversed by returning the population to an ancestral environment. Such evolutionary reversals have been observed in both natural and laboratory populations. However, the factors that determine the reversibility of evolution are still under debate. The time scales of environmental change vary over a wide range, but little is known about how the rate of environmental change influences the reversibility of evolution. Here, we demonstrate computationally that slowly switching between environments increases the reversibility of evolution for small populations that are subject to only modest clonal interference. For small populations, slow switching reduces the mean number of mutations acquired in a new environment and also increases the probability of reverse evolution at each of these “genetic distances.” As the population size increases, slow switching no longer reduces the genetic distance, thus decreasing the evolutionary reversibility. We confirm this effect using both a phenomenological model of clonal interference and also a Wright–Fisher stochastic simulation that incorporates genetic diversity. Our results suggest that the rate of environmental change is a key determinant of the reversibility of evolution, and provides testable hypotheses for experimental evolution.     

Evolutionary rescue can prevent extinction following environmental change

The ubiquity of global change and its impacts on biodiversity poses a clear and urgent challenge for evolutionary biologists. In many cases, environmental change is so widespread and rapid that individuals can neither accommodate to them physiologically nor migrate to a more favourable site. Extinction will ensue unless the population adapts fast enough to counter the rate of decline. According to theory, whether populations can be rescued by evolution depends upon several crucial variables: population size, the supply of genetic variation, and the degree of maladaptation to the new environment. Using techniques in experimental evolution we tested the conditions for evolutionary rescue (ER). Hundreds of yeast populations were exposed to normally lethal concentrations of salt in conditions, where the frequency of rescue mutations was estimated and population size was manipulated. In a striking match with theory, we show that ER is possible, and that the recovery of the population may occur within 25 generations. We observed a clear threshold in population size for ER whereby the ancestral population size must be sufficiently large to counter stochastic extinction and contain resistant individuals. These results demonstrate that rapid evolution is an important component of the response of small populations to environmental change.     

Mechanisms of regulation of the speed of evolution: The population level

This article concentrates on modeling the evolution of a population in a changing environment. We raise the optimization problem, which reflects the mechanisms of regulation of the speed of evolution that provide an adequate population response in correspondence with the direction and rate of environmental change. The numerical experiment results show plausible age–specific fertility dependences on the rate of environmental changes, as well as describing and explaining a number of evolutionary effects.     

The evolution of photosynthesis…again?

‘Replaying the tape’ is an intriguing ‘would it happen again?’ exercise. With respect to broad evolutionary innovations, such as photosynthesis, the answers are central to our search for life elsewhere. Photosynthesis permits a large planetary biomass on Earth. Specifically, oxygenic photosynthesis has allowed an oxygenated atmosphere and the evolution of large metabolically demanding creatures, including ourselves. There are at least six prerequisites for the evolution of biological carbon fixation: a carbon-based life form; the presence of inorganic carbon; the availability of reductants; the presence of light; a light-harvesting mechanism to convert the light energy into chemical energy; and carboxylating enzymes. All were present on the early Earth. To provide the evolutionary pressure, organic carbon must be a scarce resource in contrast to inorganic carbon. The probability of evolving a carboxylase is approached by creating an inventory of carbon-fixation enzymes and comparing them, leading to the conclusion that carbon fixation in general is basic to life and has arisen multiple times. Certainly, the evolutionary pressure to evolve new pathways for carbon fixation would have been present early in evolution. From knowledge about planetary systems and extraterrestrial chemistry, if organic carbon-based life occurs elsewhere, photosynthesis—although perhaps not oxygenic photosynthesis—would also have evolved.     

Rapid evolution and the convergence of ecological and evolutionary time

Recent studies have documented rates of evolution of ecologically important phenotypes sufficiently fast that they have the potential to impact the outcome of ecological interactions while they are underway. Observations of this type go against accepted wisdom that ecological and evolutionary dynamics occur at very different time scales. While some authors have evaluated the rapidity of a measured evolutionary rate by comparing it to the overall distribution of measured evolutionary rates, we believe that ecologists are mainly interested in rapid evolution because of its potential to impinge on ecological processes. We therefore propose that rapid evolution be defined as a genetic change occurring rapidly enough to have a measurable impact on simultaneous ecological change. Using this definition we propose a framework for decomposing rates of ecological change into components driven by simultaneous evolutionary change and by change in a non‐evolutionary factor (e.g. density dependent population dynamics, abiotic environmental change). Evolution is judged to be rapid in this ecological context if its contribution to ecological change is large relative to the contribution of other factors. We provide a worked example of this approach based on a theoretical predator–prey interaction [ Abrams, P. & Matsuda, H. (1997) . Evolution, 51, 1740], and find that in this system the impact of prey evolution on predator per capita growth rate is 63% that of internal ecological dynamics. We then propose analytical methods for measuring these contributions in field situations, and apply them to two long‐term data sets for which suitable ecological and evolutionary data exist. For both data sets relatively high rates of evolutionary change have been found when measured as character change in standard deviations per generation (haldanes). For Darwin's finches evolving in response to fluctuating rainfall [ Grant, P.R. & Grant, B.R. (2002) . Science, 296, 707], we estimate that evolutionary change has been more rapid than ecological change by a factor of 2.2. For a population of freshwater copepods whose life history evolves in response to fluctuating fish predation [ Hairston, N.G. Jr & Dillon, T.A. (1990) . Evolution, 44, 1796], we find that evolutionary change has been about one quarter the rate of ecological change – less than in the finch example, but nevertheless substantial. These analyses support the view that in order to understand temporal dynamics in ecological processes it is critical to consider the extent to which the attributes of the system under investigation are simultaneously changing as a result of rapid evolution.     

Evolution in a changing environment: a case study with great tit fledging mass

Heritable phenotypic traits under significant and consistent directional selection often fail to show the expected evolutionary response. A potential explanation for this contradiction is that because environmental conditions change constantly, environmental change can mask an evolutionary response to selection. We combined an "animal model" analysis with 36 years of data from a long-term study of great tits (Parus major) to explore selection on and evolution of a morphological trait: body mass at fledging. We found significant heritability of this trait, but despite consistent positive directional selection on both the phenotypic and the additive genetic component of body mass, the population mean phenotypic value declined rather than increased over time. However, the mean breeding value for body mass at fledging increased over time, presumably in response to selection. We show that the divergence between the response to selection observed at the levels of genotype and phenotype can be explained by a change in environmental conditions over time, that is, related both to increased spring temperature before breeding and elevated population density. Our results support the suggestion that measuring phenotypes may not always give a reliable impression of evolutionary trajectories and that understanding patterns of phenotypic evolution in nature requires an understanding of how the environment has itself changed.     

Cooperation can promote rescue or lead to evolutionary suicide during environmental change

The adaptation of populations to changing conditions may be affected by interactions between individuals. For example, when cooperative interactions increase fecundity, they may allow populations to maintain high densities and thus keep track of moving environmental optima. Simultaneously, changes in population density alter the marginal benefits of cooperative investments, creating a feedback loop between population dynamics and the evolution of cooperation. Here we model how the evolution of cooperation interacts with adaptation to changing environments. We hypothesize that environmental change lowers population size and thus promotes the evolution of cooperation, and that this, in turn, helps the population keep up with the moving optimum. However, we find that the evolution of cooperation can have qualitatively different effects, depending on which fitness component is reduced by the costs of cooperation. If the costs decrease fecundity, cooperation indeed speeds adaptation by increasing population density; if, in contrast, the costs decrease viability, cooperation may instead slow adaptation by lowering the effective population size, leading to evolutionary suicide. Thus, cooperation can either promote or—counterintuitively—hinder adaptation to a changing environment. Finally, we show that our model can also be generalized to other social interactions by discussing the evolution of competition during environmental change.     

Fluctuation Induces Evolutionary Branching in a Mathematical Model of Ecosystems

Ecological systems are always subjected to various environmental fluctuations. They evolve under these fluctuations and the resulting systems are robust against them. The diversity in ecological systems is also acquired through the evolution. How do the fluctuations affect the evolutionary processes? Do the fluctuations have direct impact on the species diversity in ecological systems? In the present paper, we investigate the relation between the environmental fluctuation and the evolution of species diversity with a mathematical model of evolutionary ecology. In the model, individual organisms compete for a single restricted resource and the temporal fluctuation in the resource supply is introduced as the environmental fluctuation. The evolutionary process is represented by the mutational change of genotypes which determines their resource utilization strategies. We found that when the environmental state is switched form static to fluctuating conditions, the initial closely related population distributed around the genotype adapted for the static environment is destabilized and divided into two groups in the genotype space; i.e., the evolutionary branching is induced by the environmental fluctuation. The consequent multiple species structures is evolutionary stable at the presence of the fluctuation. We perform the evolutionary invasion analysis for the phenomena and illustrate the mechanisms of the branchings. The results indicate a novel process of increasing the species diversity via evolutionary branching, and the analysis reveals the mechanisims of the branching preocess as the response to the environmental fluctuation. The robustness of the evolutionary process is also discussed.     

FOUNDER EFFECTS AND PEAK SHIFTS WITHOUT GENETIC DRIFT: ADAPTIVE PEAK SHIFTS OCCUR EASILY WHEN ENVIRONMENTS FLUCTUATE SLIGHTLY

Two similar evolutionary theories, the shifting balance theory and founder-flush models, invoke random genetic drift to allow evolution on complex adaptive landscapes. These models, in their usual incarnations, deal with fitness as a static entity, and the probability of transition from one form to another is predicted to be quite small by analysis of these models. Fitness itself can change, however, and the amount of change in the parameters of the fitness functions required to allow deterministic evolution to new adaptive peaks is very small. The probability of environmental changes sufficient to allow substantial morphological evolution or reproductive isolation is large relative to the probability that similar changes could occur by processes requiring genetic drift, even with very small population sizes. The rapid evolution or speciation following a population founding event is more closely linked with environmental changes than genetic drift.     

Population and evolutionary dynamics in spatially structured seasonally varying environments

Increasingly imperative objectives in ecology are to understand and forecast population dynamic and evolutionary responses to seasonal environmental variation and change. Such population and evolutionary dynamics result from immediate and lagged responses of all key life‐history traits, and resulting demographic rates that affect population growth rate, to seasonal environmental conditions and population density. However, existing population dynamic and eco‐evolutionary theory and models have not yet fully encompassed within‐individual and among‐individual variation, covariation, structure and heterogeneity, and ongoing evolution, in a critical life‐history trait that allows individuals to respond to seasonal environmental conditions: seasonal migration. Meanwhile, empirical studies aided by new animal‐tracking technologies are increasingly demonstrating substantial within‐population variation in the occurrence and form of migration versus year‐round residence, generating diverse forms of ‘partial migration’ spanning diverse species, habitats and spatial scales. Such partially migratory systems form a continuum between the extreme scenarios of full migration and full year‐round residence, and are commonplace in nature. Here, we first review basic scenarios of partial migration and associated models designed to identify conditions that facilitate the maintenance of migratory polymorphism. We highlight that such models have been fundamental to the development of partial migration theory, but are spatially and demographically simplistic compared to the rich bodies of population dynamic theory and models that consider spatially structured populations with dispersal but no migration, or consider populations experiencing strong seasonality and full obligate migration. Second, to provide an overarching conceptual framework for spatio‐temporal population dynamics, we define a ‘partially migratory meta‐population’ system as a spatially structured set of locations that can be occupied by different sets of resident and migrant individuals in different seasons, and where locations that can support reproduction can also be linked by dispersal. We outline key forms of within‐individual and among‐individual variation and structure in migration that could arise within such systems and interact with variation in individual survival, reproduction and dispersal to create complex population dynamics and evolutionary responses across locations, seasons, years and generations. Third, we review approaches by which population dynamic and eco‐evolutionary models could be developed to test hypotheses regarding the dynamics and persistence of partially migratory meta‐populations given diverse forms of seasonal environmental variation and change, and to forecast system‐specific dynamics. To demonstrate one such approach, we use an evolutionary individual‐based model to illustrate that multiple forms of partial migration can readily co‐exist in a simple spatially structured landscape. Finally, we summarise recent empirical studies that demonstrate key components of demographic structure in partial migration, and demonstrate diverse associations with reproduction and survival. We thereby identify key theoretical and empirical knowledge gaps that remain, and consider multiple complementary approaches by which these gaps can be filled in order to elucidate population dynamic and eco‐evolutionary responses to spatio‐temporal seasonal environmental variation and change.     

Toward an integration of evolutionary biology and ecosystem science

At present, the disciplines of evolutionary biology and ecosystem science are weakly integrated. As a result, we have a poor understanding of how the ecological and evolutionary processes that create, maintain, and change biological diversity affect the flux of energy and materials in global biogeochemical cycles. The goal of this article was to review several research fields at the interfaces between ecosystem science, community ecology and evolutionary biology, and suggest new ways to integrate evolutionary biology and ecosystem science. In particular, we focus on how phenotypic evolution by natural selection can influence ecosystem functions by affecting processes at the environmental, population and community scale of ecosystem organization. We develop an eco-evolutionary model to illustrate linkages between evolutionary change (e.g. phenotypic evolution of producer), ecological interactions (e.g. consumer grazing) and ecosystem processes (e.g. nutrient cycling). We conclude by proposing experiments to test the ecosystem consequences of evolutionary changes.     

Whither life? Conjectures on the future evolution of biochemistry

Life has existed on the Earth for approximately four billion years. The sheer depth of evolutionary time, and the diversity of extant species, makes it tempting to assume that all the key biochemical innovations underpinning life have already happened. But we are only a little over halfway through the trajectory of life on our planet. In this Opinion piece, we argue: (i) that sufficient time remains for the evolution of new processes at the heart of metabolic biochemistry and (ii) that synthetic biology is providing predictive insights into the nature of these innovations. By way of example, we focus on engineered solutions to existing inefficiencies in energy generation, and on the complex, synthetic regulatory circuits that are currently being implemented.     

Spatiotemporal landscape genetics: Investigating ecology and evolution through space and time

Genetic time‐series data from historical samples greatly facilitate inference of past population dynamics and species evolution. Yet, although climate and landscape change are often touted as post‐hoc explanations of biological change, our understanding of past climate and landscape change influences on evolutionary processes is severely hindered by the limited application of methods that directly relate environmental change to species dynamics through time. Increased integration of spatiotemporal environmental and genetic data will revolutionize the interpretation of environmental influences on past population processes and the quantification of recent anthropogenic impacts on species, and vastly improve prediction of species responses under future climate change scenarios, yielding widespread revelations across evolutionary biology, landscape ecology and conservation genetics. This review encourages greater use of spatiotemporal landscape genetic analyses that explicitly link landscape, climate and genetic data through time by providing an overview of analytical approaches for integrating historical genetic and environmental data in five key research areas: population genetic structure, demography, phylogeography, metapopulation connectivity and adaptation. We also include a tabular summary of key methodological information, suggest approaches for mitigating the particular difficulties in applying these techniques to ancient DNA and palaeoclimate data, and highlight areas for future methodological development.     

EXPERIMENTAL EVOLUTION MEETS MARINE PHYTOPLANKTON

Our perspective highlights potentially important links between disparate fields—biological oceanography, climate change research, and experimental evolutionary biology. We focus on one important functional group—photoautotrophic microbes (phytoplankton), which are responsible for ～50% of global primary productivity. Global climate change currently results in the simultaneous change of several conditions such as warming, acidification, and nutrient supply. It thus has the potential to dramatically change phytoplankton physiology, community composition, and may result in adaptive evolution. Although their large population sizes, standing genetic variation, and rapid turnover time should promote swift evolutionary change, oceanographers have focussed on describing patterns of present day physiological differentiation rather than measure potential adaptation in evolution experiments, the only direct way to address whether and at which rate phytoplankton species will adapt to environmental change. Important open questions are (1) is adaptation limited by existing genetic variation or fundamental constraints? (2) Will complex ecological settings such as gradual versus abrupt environmental change influence adaptation processes? (3) How will increasing environmental variability affect the evolution of phenotypic plasticity patterns? Because marine phytoplankton species display rapid acclimation capacity (phenotypic buffering), a systematic study of reaction norms renders them particularly interesting to the evolutionary biology research community.