Eco‐evolutionary dynamics in restored communities and ecosystems

Recent ecological studies have revealed that rapid evolution within populations can have significant impacts on the ecological dynamics of communities and ecosystems. These eco‐evolutionary dynamics (EED) are likely to have substantial and quantifiable effects in restored habitats over timescales that are relevant for the conservation and restoration of small populations and threatened communities. Restored habitats may serve as “hotspots” for EED due to mismatches between transplanted genotypes and the restored environment, and novel interactions among lineages that do not share a coevolutionary history, both of which can generate strong selection for rapid evolutionary change that has immediate demographic consequences. Rapid evolution that influences population dynamics and community processes is likely to have particularly large effects during the establishment phase of restoration efforts. Finally, restoration activities and their associated long‐term monitoring programs provide outstanding opportunities for using eco‐evolutionary experimental approaches. Results from such studies will address questions about the effects of rapid evolutionary change on the ecological dynamics of populations and interacting species, while simultaneously providing critical, but currently overlooked, information for conservation practices.     

Experimental evolution

Experimental evolution is the study of evolutionary processes occurring in experimental populations in response to conditions imposed by the experimenter. This research approach is increasingly used to study adaptation, estimate evolutionary parameters, and test diverse evolutionary hypotheses. Long applied in vaccine development, experimental evolution also finds new applications in biotechnology. Recent technological developments provide a path towards detailed understanding of the genomic and molecular basis of experimental evolutionary change, while new findings raise new questions that can be addressed with this approach. However, experimental evolution has important limitations, and the interpretation of results is subject to caveats resulting from small population sizes, limited timescales, the simplified nature of laboratory environments, and, in some cases, the potential to misinterpret the selective forces and other processes at work.     

Population genomics of marine fishes: identifying adaptive variation in space and time

Studies of adaptive evolution have experienced a recent revival in population genetics of natural populations and there is currently much focus on identifying genomic signatures of selection in space and time. Insights into local adaptation, adaptive response to global change and evolutionary consequences of selective harvesting can be generated through population genomics studies, allowing the separation of the effects invoked by neutral processes (drift-migration) from those due to selection. Such knowledge is important not only for improving our basic understanding of natural as well as human-induced evolutionary processes, but also for predicting future trajectories of biodiversity and for setting conservation priorities. Marine fishes possess a number of features rendering them well suited for providing general insights into adaptive genomic evolution in natural populations. These include well-described population structures, substantial and rapidly developing genomic resources and abundant archived samples enabling temporal studies. Furthermore, superior possibilities for conducting large-scale experiments under controlled conditions, due to the economic resources provided by the large and growing aquaculture industry, hold great promise for utilizing recent technological developments. Here, we review achievements in marine fish genomics to date and highlight potential avenues for future research, which will provide both general insights into evolution in high gene flow species, as well as specific knowledge which can lead to improved management of marine organisms.     

The consequence of natural selection on genetic variation in the mouse

Laboratory mouse strains are known to have emerged from recent interbreeding between individuals of Mus musculus isolated populations. As a result of this breeding history, the collection of polymorphisms observed between laboratory mouse strains is likely to harbor the effects of natural selection between reproductively isolated populations. Until now no study has systematically investigated the consequences of this breeding history on gene evolution. Here we have used a novel, unbiased evolutionary approach to predict the founder origin of laboratory mouse strains and to assess the balance between ancient and newly emerged mutations in the founder subspecies. Our results confirm a contribution from at least four distinct subspecies. Additionally, our method allowed us to identify regions of relaxed selective constraint among laboratory mouse strains. This unique structure of variation is likely to have significant consequences on the use of mouse to find genes underlying phenotypic variation.     

Rapid divergence and convergence of life‐history in experimentally evolved Drosophila melanogaster

Laboratory selection experiments are alluring in their simplicity, power, and ability to inform us about how evolution works. A longstanding challenge facing evolution experiments with metazoans is that significant generational turnover takes a long time. In this work, we present data from a unique system of experimentally evolved laboratory populations of Drosophila melanogaster that have experienced three distinct life‐history selection regimes. The goal of our study was to determine how quickly populations of a certain selection regime diverge phenotypically from their ancestors, and how quickly they converge with independently derived populations that share a selection regime. Our results indicate that phenotypic divergence from an ancestral population occurs rapidly, within dozens of generations, regardless of that population's evolutionary history. Similarly, populations sharing a selection treatment converge on common phenotypes in this same time frame, regardless of selection pressures those populations may have experienced in the past. These patterns of convergence and divergence emerged much faster than expected, suggesting that intermediate evolutionary history has transient effects in this system. The results we draw from this system are applicable to other experimental evolution projects, and suggest that many relevant questions can be sufficiently tested on shorter timescales than previously thought.     

Analyses of physiological evolutionary response

Selection studies are useful if they can provide us with insights into the patterns and processes of evolution in populations under controlled conditions. In this context it is particularly valuable to be able to analyze the limitations of and constraints on evolutionary responses to allow predictions concerning evolutionary change. The concept of a selection pathway is presented as a means of visualizing this predictive process and the constraints that help define the population's response to selection. As pointed out by Gould and Lewontin, history and chance are confounding forces that can mask or distort the adaptive response. Students of the evolutionary responses of organisms are very interested in the effects of these confounding forces, since they play a critical role not only in the laboratory but also in natural selection in the field. In this article, we describe some methods that are a bit different from those used in most studies for examining data from laboratory selection studies. These analytical methods are intended to provide insights into the physiological mechanisms by which evolutionary responses to the environment proceed. Interestingly, selection studies often exhibit disparate responses in replicate populations. We offer methods for analyzing these disparate responses in replicate populations to better understand this very important source of variability in the evolutionary response. We review the techniques of Travisano et al. and show that these approaches can be used to investigate the relative roles of adaptation, history, and chance in the evolutionary responses of populations of Drosophila melanogaster to selection for enhanced desiccation resistance. We anticipate that a wider application of these techniques will provide valuable insights into the organismal, genetic, and molecular nature of the constraints, as well as the factors that serve to enhance or, conversely, to mask the effects of chance. Such studies should help to provide a more detailed understanding of the processes producing evolutionary change in populations.     

Adaptation and constraint in a stickleback radiation

The evolution of threespine sticklebacks in freshwater lakes constitutes a well‐studied example of a phenotypic radiation that has produced numerous instances of parallel evolution, but the exact selective agents that drive these changes are not yet fully understood. We present a comparative study across 74 freshwater populations of threespine stickleback in Norway to test whether evolutionary changes in stickleback morphology are consistent with adaptations to physical parameters such as lake depth, lake area, lake perimeter and shoreline complexity, variables thought to reflect different habitats and feeding niches. Only weak indications of adaptation were found. Instead, populations seem to have diversified in phenotypic directions consistent with allometric scaling relationships. This indicates that evolutionary constraints may have played a role in structuring phenotypic variation across freshwater populations of stickleback. We also tested whether the number of lateral plates evolved in response to lake calcium levels, but found no evidence for this hypothesis.     

Trends and rates of microevolution in plants

Evidence for rapid evolutionary change in plants in response to changing environmental conditions is widespread in the literature. However, evolutionary change in plant populations has not been quantified using a rate metric that allows for comparisons between and within studies. One objective of this paper is to estimate rates of evolution using data from previously published studies to begin a foundation for comparison and to examine trends and rates of microevolution in plants. We use data gathered from studies of plant adaptations in response to heavy metals, herbicide, pathogens, changes in pH, global change, and novel environments. Rates of evolution are estimated in the form of two metrics, darwins and haldanes. A second objective is to demonstrate how estimated rates could be used to address specific microevolutionary questions. For example, we examine how evolutionary rate changes with time, life history correlates of evolutionary rates, and whether some types of traits evolve faster than others. We also approach the question of how rates can be used to predict patterns of evolution under novel selection pressures using two contemporary examples: introductions of non-native species to alien environments and global change.     

SHORT-TERM EVOLUTION IN THE SIZE AND SHAPE OF PEA APHIDS

Phenotypic evolution in contemporary populations can generally be witnessed only when novel selective forces produce rapid evolution. Examples of conditions that have led to rapid evolution include drastic environmental change, invasion of a new predator, or a host-range expansion. In cyclical parthenogens, however, yearly cycles of phenotypic evolution may occur due to the loss of adaptation during recombination in the sexual phase (genetic slippage), permitting an opportunity to observe adaptive evolutionary change in contemporary populations that are not necessarily subject to new patterns of natural selection. In insect herbivores, comparative studies suggest that morphological features that aid individuals in remaining on the plant or exploiting it as a food source are likely targets for selection. Here, we estimated the genetic variability of morphological traits in a cyclical parthenogen, the pea aphid (Acyrthosiphon pisum), to determine the potential for their evolution and we tested the hypothesis that size and/or shape evolves by clonal selection during one season of parthenogenetic reproduction. Genetic variation in a set of morphological traits was estimated using laboratory-reared descendents of clones collected from a single alfalfa field in May 1988 and April 1989 (henceforth, the “early” collections). In both years, there was significant clonal heritability early in the season both for overall morphology and for several individual aspects of size and shape. Because the course of short-term evolutionary change in the multivariate phenotype is a function of patterns of genetic covariance among characters, genetic correlations between size and 12 shape variables were also estimated for these early collections. A comparison between the mean phenotype of each early collection and that of a corresponding “late” collection made from the same field seven to eight clonal generations later in the same years revealed qualitatively similar changes in the average multivariate morphological phenotypes between the time periods in both years, although the difference was only significant for the 1989 samples. The pattern of genetic correlations that we estimated early in the 1989 season between overall size and various shape variables suggests that the observed short-term evolutionary changes in shape could have been due to natural selection acting only to increase overall size. We tested this hypothesis by estimating selection on size using a separate data set in which both demographic and morphological variables were measured on individuals reared under field conditions. Highly significant regressions of individual relative fitness on size were found for two major fitness components. Thus, it is likely that the evolutionary change in morphology that we observed is attributable to natural selection, possibly acting primarily through body size. A shift back to smaller size between the late 1988 and early 1989 collections from the same field suggests that either a cost of recombination or opposing selective forces during overwintering may produce persistent yearly cycles of morphological evolution in this cyclically parthenogenetic species.     

Divergent life histories among populations of the fish Brachyrhaphis rhabdophora: detecting putative agents of selection by candidate model analysis

Studies of natural selection in the wild almost always begin by examining patterns of association between phenotypic adaptations and environmental factors thought to shape evolutionary change. Unfortunately, many studies pay little attention to the effects of model selection on the evolutionary inferences drawn from such correlative data. In this study, I employed a candidate model analysis to examine four potential causes of life-history evolution in the livebearing fish Brachyrhaphis rhabdophora . Combining factor analysis with path analysis, I constructed a nested set of 17 models that represent the hypothetical effects of four putative selective agents (mortality, density, resource availability, and habitat stability) on life-history evolution in this species. These models represent both direct and indirect effects of selection on the life history. Using the Akaike Information Criterion to distinguish among models, I found that simple models that contained only single selective agents most parsimoniously explained life-history divergence among 27 B. rhabdophora populations. Surprisingly, the four putative selective agents could not be distinguished, suggesting that the selective environment could be composed of a single selective agent confounded with other environmental factors, or could be composed of a suite of environmental factors that act in concert to shape the life history. In addition, comparisons among more complex models indicated that direct effects of selective agents appear to have primacy over combinations of indirect selective interactions in explaining intraspecific variation in B. rhabdophora life histories.     

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.     

Which evolutionary processes influence natural genetic variation for phenotypic traits?

Although many studies provide examples of evolutionary processes such as adaptive evolution, balancing selection, deleterious variation and genetic drift, the relative importance of these selective and stochastic processes for phenotypic variation within and among populations is unclear. Theoretical and empirical studies from humans as well as natural animal and plant populations have made progress in examining the role of these evolutionary forces within species. Tentative generalizations about evolutionary processes across species are beginning to emerge, as well as contrasting patterns that characterize different groups of organisms. Furthermore, recent technical advances now allow the combination of ecological measurements of selection in natural environments with population genetic analysis of cloned QTLs, promising advances in identifying the evolutionary processes that influence natural genetic variation.     

Rapid evolution of cold tolerance in stickleback

Climate change is predicted to lead to increased average temperatures and greater intensity and frequency of high and low temperature extremes, but the evolutionary consequences for biological communities are not well understood. Studies of adaptive evolution of temperature tolerance have typically involved correlative analyses of natural populations or artificial selection experiments in the laboratory. Field experiments are required to provide estimates of the timing and strength of natural selection, enhance understanding of the genetics of adaptation and yield insights into the mechanisms driving evolutionary change. Here, we report the experimental evolution of cold tolerance in natural populations of threespine stickleback fish (Gasterosteus aculeatus). We show that freshwater sticklebacks are able to tolerate lower minimum temperatures than marine sticklebacks and that this difference is heritable. We transplanted marine sticklebacks to freshwater ponds and measured the rate of evolution after three generations in this environment. Cold tolerance evolved at a rate of 0.63 haldanes to a value 2.5°C lower than that of the ancestral population, matching values found in wild freshwater populations. Our results suggest that cold tolerance is under strong selection and that marine sticklebacks carry sufficient genetic variation to adapt to changes in temperature over remarkably short time scales.     

New model systems for studying the evolutionary biology of aging: Crustacea

Progress in any area of biology has generally required work on a variety of organisms. This is true because particular species often have characteristics that make them especially useful for addressing specific questions. Recent progress in studying the evolutionary biology of senescence has been made through the use of new species, such asCaenorhabditis elegans andDrosophila melanogaster, because of the ease of working with them in the laboratory and because investigators have used theories for the evolution of aging as a basis for discovering the underlying mechanisms.I describe ways of finding new model systems for studying the evolutionary mechanisms of aging by combining the predictions of theory with existing information about the natural history of organisms that are well-suited to laboratory studies. Properties that make organisms favorable for laboratory studies include having a short generation time, high fecundity, small body size, and being easily cultured in a laboratory environment. It is also desirable to begin with natural populations that differ in their rate of aging. I present three scenarios and four groups of organisms which fulfill these requirements. The first two scenarios apply to well-documented differences in age/size specific predation among populations of guppies and microcrustacea. The third is differences among populations of fairy shrimp (anostraca) in habitat permanence. In all cases, there is an environmentla factor that is likely to select for changes in the life history, including aging, plus a target organism which is well-suited for laboratory studies of aging.     

Anthropogenic evolution in an insect wing polymorphism following widespread deforestation

Anthropogenic environmental change can underpin major shifts in natural selective regimes, and can thus alter the evolutionary trajectories of wild populations. However, little is known about the evolutionary impacts of deforestation—one of the most pervasive human-driven changes to terrestrial ecosystems globally. Absence of forest cover (i.e. exposure) has been suggested to play a role in selecting for insect flightlessness in montane ecosystems. Here, we capitalize on human-driven variation in alpine treeline elevation in New Zealand to test whether anthropogenic deforestation has caused shifts in the distributions of flight-capable and flightless phenotypes in a wing-polymorphic lineage of stoneflies from the Zelandoperla fenestrata species complex. Transect sampling revealed sharp transitions from flight-capable to flightless populations with increasing elevation. However, these phenotypic transitions were consistently delineated by the elevation of local treelines, rather than by absolute elevation, providing a novel example of human-driven evolution in response to recent deforestation. The inferred rapid shifts to flightlessness in newly deforested regions have implications for the evolution and conservation of invertebrate biodiversity.     

Strong artificial selection in the wild results in predicted small evolutionary change

Estimates of genetic variation and selection allow for quantitative predictions of evolutionary change, at least in controlled laboratory experiments. Natural populations are, however, different in many ways, and natural selection on heritable traits does not always result in phenotypic change. To test whether we were able to predict the evolutionary dynamics of a complex trait measured in a natural, heterogeneous environment, we performed, over an 8-year period, a two-way selection experiment on clutch size in a subdivided island population of great tits (Parus major). Despite strong artificial selection, there was no clear evidence for evolutionary change at the phenotypic level. Environmentally induced differences in clutch size among years are, however, large and can mask evolutionary changes. Indeed, genetic changes in clutch size, inferred from a statistical model, did not deviate systematically from those predicted. Although this shows that estimates of genetic variation and selection can indeed provide quantitative predictions of evolutionary change, also in the wild, it also emphasizes that demonstrating evolution in wild populations is difficult, and that the interpretation of phenotypic trends requires great care.     

Reverse evolution of fitness in Drosophila melanogaster

Abstract The evolution of fitness is central to evolutionary theory, yet few experimental systems allow us to track its evolution in genetically and environmentally relevant contexts. Reverse evolution experiments allow the study of the evolutionary return to ancestral phenotypic states, including fitness. This in turn permits well‐defined tests for the dependence of adaptation on evolutionary history and environmental conditions. In the experiments described here, 20 populations of heterogeneous evolutionary histories were returned to their common ancestral environment for 50 generations, and were then compared with both their immediate differentiated ancestors and populations which had remained in the ancestral environment. One measure of fitness returned to ancestral levels to a greater extent than other characters did. The phenotypic effects of reverse evolution were also contingent on previous selective history. Moreover, convergence to the ancestral state was highly sensitive to environmental conditions. The phenotypic plasticity of fecundity, a character directly selected for, evolved during the experimental time frame. Reverse evolution appears to force multiple, diverged populations to converge on a common fitness state through different life‐history and genetic changes.     

Epigenetics in natural animal populations

Phenotypic plasticity is an important mechanism for populations to buffer themselves from environmental change. While it has long been appreciated that natural populations possess genetic variation in the extent of plasticity, a surge of recent evidence suggests that epigenetic variation could also play an important role in shaping phenotypic responses. Compared with genetic variation, epigenetic variation is more likely to have higher spontaneous rates of mutation and a more sensitive reaction to environmental inputs. In our review, we first provide an overview of recent studies on epigenetically encoded thermal plasticity in animals to illustrate environmentally‐mediated epigenetic effects within and across generations. Second, we discuss the role of epigenetic effects during adaptation by exploring population epigenetics in natural animal populations. Finally, we evaluate the evolutionary potential of epigenetic variation depending on its autonomy from genetic variation and its transgenerational stability. Although many of the causal links between epigenetic variation and phenotypic plasticity remain elusive, new data has explored the role of epigenetic variation in facilitating evolution in natural populations. This recent progress in ecological epigenetics will be helpful for generating predictive models of the capacity of organisms to adapt to changing climates.     

RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY: MATERNAL EFFECTS AND SELECTION ON LIFE-HISTORY CHARACTERS AND PLASTICITIES IN MIMULUS GUTTATUS

Recent studies in plant populations have found that environmental heterogeneity and phenotypic selection vary at local spatial scales. In this study, I ask if there is evolutionary change in response to environmental heterogeneity and, if so, whether the response occurs for characters or character plasticities. I used vegetative clones of Mimulus guttatus to create replicate populations of 75 genotypes. These populations were planted into the natural habitat where they differed in mean growth, flowering phenology, and life span. This phenotypic variation was used to define selective environments. There was variation in fitness (flower production) among genotypes across all planting sites and in genotype response to the selective environment. Offspring from each site were grown in the greenhouse in two water treatments. Because each population initially had the same genetic composition, variation in the progeny between selective environments reveals either evolutionary change in response to environmental heterogeneity or environmental maternal effects. Plants from experimental sites that flowered earlier, had shorter life spans and were less productive, produced offspring that had more flowers, on average, and were less plastic in vegetative allocation than offspring of longer-lived plants from high-productivity areas. However, environmental maternal effects masked phenotypic differences in flower production. Therefore, although there was evidence of genetic differentiation in both life-history characters and their plasticities in response to small-scale environmental heterogeneity, environmental maternal effects may slow evolutionary change. Response to local-scale selective regimes suggests that environmental heterogeneity and local variation in phenotypic selection may act to maintain genetic variation.     

Does phenotypic plasticity initiate developmental bias?

The generation of variation is paramount for the action of natural selection. Although biologists are now moving beyond the idea that random mutation provides the sole source of variation for adaptive evolution, we still assume that variation occurs randomly. In this review, we discuss an alternative view for how phenotypic plasticity, which has become well accepted as a source of phenotypic variation within evolutionary biology, can generate nonrandom variation. Although phenotypic plasticity is often defined as a property of a genotype, we argue that it needs to be considered more explicitly as a property of developmental systems involving more than the genotype. We provide examples of where plasticity could be initiating developmental bias, either through direct active responses to similar stimuli across populations or as the result of programmed variation within developmental systems. Such biased variation can echo past adaptations that reflect the evolutionary history of a lineage but can also serve to initiate evolution when environments change. Such adaptive programs can remain latent for millions of years and allow development to harbor an array of complex adaptations that can initiate new bouts of evolution. Specifically, we address how ideas such as the flexible stem hypothesis and cryptic genetic variation overlap, how modularity among traits can direct the outcomes of plasticity, and how the structure of developmental signaling pathways is limited to a few outcomes. We highlight key questions throughout and conclude by providing suggestions for future research that can address how plasticity initiates and harbors developmental bias.