How much can history constrain adaptive evolution? A real‐time evolutionary approach of inversion polymorphisms in Drosophila subobscura

Chromosomal inversions are present in a wide range of animals and plants, having an important role in adaptation and speciation. Although empirical evidence of their adaptive value is abundant, the role of different processes underlying evolution of chromosomal polymorphisms is not fully understood. History and selection are likely to shape inversion polymorphism variation to an extent yet largely unknown. Here, we perform a real‐time evolution study addressing the role of historical constraints and selection in the evolution of these polymorphisms. We founded laboratory populations of Drosophila subobscura derived from three locations along the European cline and followed the evolutionary dynamics of inversion polymorphisms throughout the first 40 generations. At the beginning, populations were highly differentiated and remained so throughout generations. We report evidence of positive selection for some inversions, variable between foundations. Signs of negative selection were more frequent, in particular for most cold‐climate standard inversions across the three foundations. We found that previously observed convergence at the phenotypic level in these populations was not associated with convergence in inversion frequencies. In conclusion, our study shows that selection has shaped the evolutionary dynamics of inversion frequencies, but doing so within the constraints imposed by previous history. Both history and selection are therefore fundamental to predict the evolutionary potential of different populations to respond to global environmental changes.     

Evolution of mating behavior between two populations adapting to common environmental conditions

Populations from the same species may be differentiated across contrasting environments, potentially affecting reproductive isolation among them. When such populations meet in a novel common environment, this isolation may be modified by biotic or abiotic factors. Curiously, the latter have been overlooked. We filled this gap by performing experimental evolution of three replicates of two populations of Drosophila subobscura adapting to a common laboratorial environment, and simulated encounters at three time points during this process. Previous studies showed that these populations were highly differentiated for several life‐history traits and chromosomal inversions. First, we show initial differentiation for some mating traits, such as assortative mating and male mating rate, but not others (e.g., female mating latency). Mating frequency increased during experimental evolution in both sets of populations. The assortative mating found in one population remained constant throughout the adaptation process, while disassortative mating of the other population diminished across generations. Additionally, differences in male mating rate were sustained across generations. This study shows that mating behavior evolves rapidly in response to adaptation to a common abiotic environment, although with a complex pattern that does not correspond to the quick convergence seen for life‐history traits.     

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.     

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.     

What paths do advantageous alleles take during short‐term evolutionary change?

Combining experimental evolution with whole‐genome resequencing is a promising new strategy for investigating the dynamics of evolutionary change. Published studies that have resequenced laboratory‐selected populations of sexual organisms have typically focused on populations sampled at the end of an evolution experiment. These studies have attempted to associate particular alleles with phenotypic change and attempted to distinguish between different theoretical models of adaptation. However, neither the population used to initiate the experiment nor multiple time points sampled during the evolutionary trajectory are generally available for examination. In this issue of Molecular Ecology, Orozco‐terWengel et al. (2012) take a significant step forward by estimating genome‐wide allele frequencies at the start, 15 generations into and at the end of a 37‐generation Drosophila experimental evolution study. The authors identify regions of the genome that have responded to laboratory selection and describe the temporal dynamics of allele frequency change. They identify two common trajectories for putatively adaptive alleles: alleles either gradually increase in frequency throughout the entire 37 generations or alleles plateau at a new frequency by generation 15. The identification of complex trajectories of alleles under selection contributes to a growing body of literature suggesting that simple models of adaptation, whereby beneficial alleles arise and increase in frequency unimpeded until they become fixed, may not adequately describe short‐term response to selection.     

FUNCTIONAL GENETIC DIVERGENCE IN HIGH CO2 ADAPTED EMILIANIA HUXLEYI POPULATIONS

Predicting the impacts of environmental change on marine organisms, food webs, and biogeochemical cycles presently relies almost exclusively on short‐term physiological studies, while the possibility of adaptive evolution is often ignored. Here, we assess adaptive evolution in the coccolithophore Emiliania huxleyi, a well‐established model species in biological oceanography, in response to ocean acidification. We previously demonstrated that this globally important marine phytoplankton species adapts within 500 generations to elevated CO₂. After 750 and 1000 generations, no further fitness increase occurred, and we observed phenotypic convergence between replicate populations. We then exposed adapted populations to two novel environments to investigate whether or not the underlying basis for high CO₂‐adaptation involves functional genetic divergence, assuming that different novel mutations become apparent via divergent pleiotropic effects. The novel environment “high light” did not reveal such genetic divergence whereas growth in a low‐salinity environment revealed strong pleiotropic effects in high CO₂ adapted populations, indicating divergent genetic bases for adaptation to high CO₂. This suggests that pleiotropy plays an important role in adaptation of natural E. huxleyi populations to ocean acidification. Our study highlights the potential mutual benefits for oceanography and evolutionary biology of using ecologically important marine phytoplankton for microbial evolution experiments.     

Recurrent adaptation in a low‐dispersal trait

The study of natural populations from contrasting environments has greatly enhanced our understanding of ecological‐dependent selection, adaptation and speciation. Cases of parallel evolution in particular have facilitated the study of the molecular and genetic basis of adaptive variation. This includes the type and number of genes underlying adaptive traits, as well as the extent to which these genes are exchanged among populations and contribute repeatedly to parallel evolution. Yet, surprisingly few studies provide a comprehensive view on the evolutionary history of adaptive traits from mutation to widespread adaptation. When did key mutations arise, how did they increase in frequency, and how did they spread? In this issue of Molecular Ecology, Van Belleghem et al. ( 2015 ) reconstruct the evolutionary history of a gene associated with wing size in the salt marsh beetle Pogonus chalceus. Screening the entire distribution range of this species, they found a single origin for the allele associated with the short‐winged ecotype. This allele seemingly evolved in an isolated population and rapidly introgressed into other populations. These findings suggest that the adaptive genetic variation found in sympatric short‐ and long‐winged populations has an allopatric origin, confirming that allopatric phases may be important at early stages of speciation.     

Rapid,broad‐scale gene expression evolution in experimentally harvested fish populations

Gene expression changes potentially play an important role in adaptive evolution under human‐induced selection pressures, but this has been challenging to demonstrate in natural populations. Fishing exhibits strong selection pressure against large body size, thus potentially inducing evolutionary changes in life history and other traits that may be slowly reversible once fishing ceases. However, there is a lack of convincing examples regarding the speed and magnitude of fisheries‐induced evolution, and thus, the relevant underlying molecular‐level effects remain elusive. We use wild‐origin zebrafish (Danio rerio) as a model for harvest‐induced evolution. We experimentally demonstrate broad‐scale gene expression changes induced by just five generations of size‐selective harvesting, and limited genetic convergence following the cessation of harvesting. We also demonstrate significant allele frequency changes in genes that were differentially expressed after five generations of size‐selective harvesting. We further show that nine generations of captive breeding induced substantial gene expression changes in control stocks likely due to inadvertent selection in the captive environment. The large extent and rapid pace of the gene expression changes caused by both harvest‐induced selection and captive breeding emphasizes the need for evolutionary enlightened management towards sustainable fisheries.     

Quality–quantity trade‐offs drive functional trait evolution in a model microalgal ‘climate change winner’

Phytoplankton are the unicellular photosynthetic microbes that form the base of aquatic ecosystems, and their responses to global change will impact everything from food web dynamics to global nutrient cycles. Some taxa respond to environmental change by increasing population growth rates in the short‐term and are projected to increase in frequency over decades. To gain insight into how these projected ‘climate change winners’ evolve, we grew populations of microalgae in ameliorated environments for several hundred generations. Most populations evolved to allocate a smaller proportion of carbon to growth while increasing their ability to tolerate and metabolise reactive oxygen species (ROS). This trade‐off drives the evolution of traits that underlie the ecological and biogeochemical roles of phytoplankton. This offers evolutionary and a metabolic frameworks for understanding trait evolution in projected ‘climate change winners’ and suggests that short‐term population booms have the potential to be dampened or reversed when environmental amelioration persists.     

Keeping your options open: Maintenance of thermal plasticity during adaptation to a stable environment

Phenotypic plasticity may allow species to cope with environmental variation. The study of thermal plasticity and its evolution helps understanding how populations respond to variation in temperature. In the context of climate change, it is essential to realize the impact of historical differences in the ability of populations to exhibit a plastic response to thermal variation and how it evolves during colonization of new environments. We have analyzed the real‐time evolution of thermal reaction norms of adult and juvenile traits in Drosophila subobscura populations from three locations of Europe in the laboratory. These populations were kept at a constant temperature of 18ºC, and were periodically assayed at three experimental temperatures (13ºC, 18ºC, and 23ºC). We found initial differentiation between populations in thermal plasticity as well as evolutionary convergence in the shape of reaction norms for some adult traits, but not for any of the juvenile traits. Contrary to theoretical expectations, an overall better performance of high latitude populations across temperatures in early generations was observed. Our study shows that the evolution of thermal plasticity is trait specific, and that a new stable environment did not limit the ability of populations to cope with environmental challenges.     

Adaptation in a spider mite population after long-term evolution on a single host plant

Evolution in a single environment is expected to erode genetic variability, thereby precluding adaptation to novel environments. To test this, a large population of spider mites kept on cucumber for approximately 300 generations was used to establish populations on novel host plants (tomato or pepper), and changes in traits associated to adaptation were measured after 15 generations. Using a half-sib design, we investigated whether trait changes were related to genetic variation in the base population. Juvenile survival and fecundity exhibited genetic variation and increased in experimental populations on novel hosts. Conversely, no variation was detected for host choice and developmental time and these traits did not evolve. Longevity remained unchanged on novel hosts despite the presence of genetic variation, suggesting weak selection for this trait. Hence, patterns of evolutionary changes generally matched those of genetic variation, and changes in some traits were not hindered by long-term evolution in a constant environment.     

Evidence for rapid evolution of phenology in an invasive grass

Evolutionary dynamics of integrative traits such as phenology are predicted to be critically important to range expansion and invasion success, yet there are few empirical examples of such phenomena. In this study, we used multiple common gardens to examine the evolutionary significance of latitudinal variation in phenology of a widespread invasive species, the Asian short‐day flowering annual grass Microstegium vimineum. In environmentally controlled growth chambers, we grew plants from seeds collected from multiple latitudes across the species' invasive range. Flowering time and biomass were both strongly correlated with the latitude of population origin such that populations collected from more northern latitudes flowered significantly earlier and at lower biomass than populations from southern locations. We suggest that this pattern may be the result of rapid adaptive evolution of phenology over a period of less than one hundred years and that such changes have likely promoted the northward range expansion of this species. We note that possible barriers to gene flow, including bottlenecks and inbreeding, have apparently not forestalled evolutionary processes for this plant. Furthermore, we hypothesize that evolution of phenology may be a widespread and potentially essential process during range expansion for many invasive plant species.     

Positive selection and convergent evolution shape molecular phenotypic traits of innate immunity receptors in tits (Paridae)

Despite widespread variability and redundancy abounding animal immunity, little is currently known about the rate of evolutionary convergence (functionally analogous traits not inherited from a common ancestor) in host molecular adaptations to parasite selective pressures. Toll‐like receptors (TLRs) provide the molecular interface allowing hosts to recognize pathogenic structures and trigger early danger signals initiating an immune response. Using a novel combination of bioinformatic approaches, here we explore genetic variation in ligand‐binding regions of bacteria‐sensing TLR4 and TLR5 in 29 species belonging to the tit family of passerine birds (Aves: Paridae). Three out of the four consensual positively selected sites in TLR4 and six out of 14 positively selected positions in TLR5 were located on the receptor surface near the functionally important sites, and based on the phylogenetic pattern evolved in a convergent (parallel) manner. This type of evolution was also seen at one N‐glycosylation site and two positively selected phosphorylation sites, providing the first evidence of convergence in post‐translational modifications in evolutionary immunology. Finally, the overall mismatch between phylogeny and the clustering of surface charge distribution demonstrates that convergence is common in overall TLR4 and TLR5 molecular phenotypes involved in ligand binding. Our analysis did not reveal any broad ecological traits explaining the convergence observed in electrostatic potentials, suggesting that information on microbial symbionts may be needed to explain TLR evolution. Adopting state‐of‐the‐art predictive structural bionformatics, we have outlined a new broadly applicable methodological approach to estimate the functional significance of positively selected variation and test for the adaptive molecular convergence in protein‐coding polymorphisms.     

Environmental effects on the structure of the G‐matrix

Genetic correlations between traits determine the multivariate response to selection in the short term, and thereby play a causal role in evolutionary change. Although individual studies have documented environmentally induced changes in genetic correlations, the nature and extent of environmental effects on multivariate genetic architecture across species and environments remain largely uncharacterized. We reviewed the literature for estimates of the genetic variance–covariance ( G ) matrix in multiple environments, and compared differences in G between environments to the divergence in G between conspecific populations (measured in a common garden). We found that the predicted evolutionary trajectory differed as strongly between environments as it did between populations. Between‐environment differences in the underlying structure of G (total genetic variance and the relative magnitude and orientation of genetic correlations) were equal to or greater than between‐population differences. Neither environmental novelty, nor the difference in mean phenotype predicted these differences in G . Our results suggest that environmental effects on multivariate genetic architecture may be comparable to the divergence that accumulates over dozens or hundreds of generations between populations. We outline avenues of future research to address the limitations of existing data and characterize the extent to which lability in genetic correlations shapes evolution in changing environments.     

Selection in a fluctuating environment and the evolution of sexual dimorphism in the seed beetle Callosobruchus maculatus

Temperature changes in the environment, which realistically include environmental fluctuations, can create both plastic and evolutionary responses of traits. Sexes might differ in either or both of these responses for homologous traits, which in turn has consequences for sexual dimorphism and its evolution. Here, we investigate both immediate changes in and the evolution of sexual dimorphism in response to a changing environment (with and without fluctuations) using the seed beetle Callosobruchus maculatus. We investigate sex differences in plasticity and also the genetic architecture of body mass and developmental time dimorphism to test two existing hypotheses on sex differences in plasticity (adaptive canalization hypothesis and condition dependence hypothesis). We found a decreased sexual size dimorphism in higher temperature and that females responded more plastically than males, supporting the condition dependence hypothesis. However, selection in a fluctuating environment altered sex-specific patterns of genetic and environmental variation, indicating support for the adaptive canalization hypothesis. Genetic correlations between sexes (r(MF) ) were affected by fluctuating selection, suggesting facilitated independent evolution of the sexes. Thus, the selective past of a population is highly important for the understanding of the evolutionary dynamics of sexual dimorphism.     

Ionome and elemental transport kinetics shaped by parallel evolution in threespine stickleback

Evidence that organisms evolve rapidly enough to alter ecological dynamics necessitates investigation of the reciprocal links between ecology and evolution. Data that link genotype to phenotype to ecology are needed to understand both the process and ecological consequences of rapid evolution. Here, we quantified the suite of elements in individuals (i.e., ionome) and differences in the fluxes of key nutrients across populations of threespine stickleback. We find that allelic variation associated with freshwater adaptation that controls bony plating is associated with changes in the ionome and nutrient recycling. More broadly, we find that adaptation of marine stickleback to freshwater conditions shifts the ionomes of natural populations and populations raised in common gardens. In both cases ionomic divergence between populations was primarily driven by differences in trace elements rather than elements typically associated with bone. These findings demonstrate the utility of ecological stoichiometry and the importance of ionome‐wide data in understanding eco‐evolutionary dynamics.     

Prudent males,group adaptation,and the tragedy of the commons

For almost five decades three threads have coexisted in the evolutionary and ecological literature, with their links only recently becoming visible and some of them still not properly addressed. These are the levels of selection debate, the metaphor of the tragedy of the commons, and the evolutionary study of sexual conflict. We analyze the eco‐evolutionary dynamics of a curious system where an asexual all‐female fish species (the Amazon molly Poecilia formosa) requires sperm from other species as a developmental trigger, without utilizing the genes from sperm. The dynamics of such a system bear strong resemblance to host–parasite dynamics, and populations of the sexual ‘host’ species persist much better if males avoid mating with Amazons. However, such avoidance may compromise their current mating success, and if this is the case, prudent mating becomes an altruistic trait that helps to keep an accumulating problem of a competing species at bay, and Amazon‐free space can be seen to form a common good that a population should maintain for future generations. A model shows that the evolution of altruistic mating restraint is possible but selection for short‐term gains means that it will remain less than perfect. This helps to explain why the anomalous gynogenetic system can persist, but it also raises questions about what kinds of traits can be classified as adaptations when optimization is not perfect and traits evolve to achieve short‐term goals better than long‐term performance. Contributing to the levels of selection debate, we encourage researchers to study the implications of the different timescales involved in the eco‐evolutionary process.     

Variation in the rate of convergent evolution: adaptation to a laboratory environment in Drosophila subobscura

Adaptation to novel environments is a central issue in evolutionary biology. One important question is the prevalence of convergence when different populations adapt to the same or similar environments. We investigated this by comparing two studies, 6 years apart, of laboratory adaptation of populations of Drosophila subobscura founded from the same natural location. In both studies several life‐history traits were periodically assayed for the first 14 generations of laboratory adaptation, as well as later generations, and compared with established, laboratory, control populations. The results indicated: (1) a process of convergence for all traits; (2) differences between the two studies in the pattern and rate of convergence; (3) dependence of the evolutionary rates on initial differentiation. The differences between studies might be the result of the differences in the founder populations and/or changes in the lab environment. In either case, the results suggest that microevolution is highly sensitive to genetic and environmental conditions.     

Rapid evolution of thermal plasticity in mountain lake Daphnia populations

Populations at risk of extinction due to climate change may be rescued by adaptive evolution or plasticity. Selective agents, such as introduced predators, may enhance or constrain plastic or adaptive responses to temperature. We tested responses of Daphnia to temperature by collecting populations from lakes across an elevational gradient in the presence and absence of fish predators (long‐term selection). We subsequently grew these populations at two elevations in field mesocosms over two years (short‐term selection), followed by a common‐garden experiment at two temperatures in the lab to measure life‐history traits. Both long‐term and short‐term selection affected traits, suggesting that genetic variation of plasticity within populations enabled individuals to rapidly evolve plasticity in response to high temperature. We found that short‐term selection by high temperature increased plasticity for growth rate in all populations. Fecundity was higher in populations from fishless lakes and body size showed greater plasticity in populations from warm lakes (long‐term selection). Neither body size nor fecundity were affected by short‐term thermal selection. These results demonstrate that plasticity is an important component of the life‐history response of Daphnia, and that genetic variation within populations enabled rapid evolution of plasticity in response to selection by temperature.     

The implications of rapid eco‐evolutionary processes for biological control ‐ a review

Novel environmental conditions experienced by introduced species can drive rapid evolution of diverse traits. In turn, rapid evolution, both adaptive and non‐adaptive, can influence population size, growth rate, and other important ecological characteristics of populations. In addition, spatial evolutionary processes that arise from a combination of assortative mating between highly dispersive individuals at the expanding edge of populations and altered reproductive rates of those individuals can accelerate expansion speed. Growing experimental evidence shows that the effects of rapid evolution on ecological dynamics can be quite large, and thus it can affect establishment, persistence, and the distribution of populations. We review the experimental and theoretical literature on such eco‐evolutionary feedbacks and evaluate the implications of these processes for biological control. Experiments show that evolving populations can establish at higher rates and grow larger than non‐evolving populations. However, non‐adaptive processes, such as genetic drift and inbreeding depression can also lead to reduced fitness and declines in population size. Spatial evolutionary processes can increase spread rates and change the fitness of individuals at the expansion front. These examples demonstrate the power of eco‐evolutionary dynamics and indicate that evolution is likely more important in biocontrol programs than previously realized. We discuss how this knowledge can be used to enhance efficacy of biological control.