Eco‐evolutionary feedbacks between private and public goods: evidence from toxic algal blooms

The importance of ‘eco‐evolutionary feedbacks’ in natural systems is currently unclear. Here, we advance a general hypothesis for a particular class of eco‐evolutionary feedbacks with potentially large, long‐lasting impacts in complex ecosystems. These eco‐evolutionary feedbacks involve traits that mediate important interactions with abiotic and biotic features of the environment and a self‐driven reversal of selection as the ecological impact of the trait varies between private (small scale) and public (large scale). Toxic algal blooms may involve such eco‐evolutionary feedbacks due to the emergence of public goods. We review evidence that toxin production by microalgae may yield ‘privatised’ benefits for individual cells or colonies under pre‐ and early‐bloom conditions; however, the large‐scale, ecosystem‐level effects of toxicity associated with bloom states yield benefits that are necessarily ‘public’. Theory predicts that the replacement of private with public goods may reverse selection for toxicity in the absence of higher level selection. Indeed, blooms often harbor significant genetic and functional diversity: bloom populations may undergo genetic differentiation over a scale of days, and even genetically similar lineages may vary widely in toxic potential. Intriguingly, these observations find parallels in terrestrial communities, suggesting that toxic blooms may serve as useful models for eco‐evolutionary dynamics in nature. Eco‐evolutionary feedbacks involving the emergence of a public good may shed new light on the potential for interactions between ecology and evolution to influence the structure and function of entire ecosystems.     

POPULATION DYNAMICS DETERMINE GENETIC ADAPTATION TO TEMPERATURE IN DAPHNIA

Rising temperatures associated with global warming present a challenge to the fate of many aquatic organisms. Although rapid evolutionary response to temperature-mediated selection may allow local persistence of populations under global warming, and therefore is a key aspect of evolutionary biology, solid proof of its occurrence is rare. In this study, we tested for genetic adaptation to an increase in temperature in the water flea Daphnia magna , a keystone species in freshwater systems, by performing a thermal selection experiment under laboratory conditions followed by the quantification of microevolutionary responses to temperature for both life-history traits as well as for intraspecific competitive strength. After three months of selection, we found a microevolutionary response to temperature in performance, but only in one of two culling regimes, highlighting the importance of population dynamics in driving microevolutionary change within populations. Furthermore, there was an evolutionary increase in thermal plasticity in performance. The results of the competition experiment were in agreement with predictions based on performance as quantified in the life table experiment and illustrate that microevolution within a short time frame has the ability to influence the outcome of intraspecific competition.     

Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes

Soil bacteria produce a diverse array of antibiotics, yet our understanding of the specific roles of antibiotics in the ecological and evolutionary dynamics of microbial interactions in natural habitats remains limited. Here, we show a significant role for antibiotics in mediating antagonistic interactions and nutrient competition among locally coexisting Streptomycete populations from soil. We found that antibiotic inhibition is significantly more intense among sympatric than allopatric Streptomycete populations, indicating local selection for inhibitory phenotypes. For sympatric but not allopatric populations, antibiotic inhibition is significantly positively correlated with niche overlap, indicating that inhibition is targeted toward bacteria that pose the greatest competitive threat. Our results support the hypothesis that antibiotics serve as weapons in mediating local microbial interactions in soil and suggest that coevolutionary niche displacement may reduce the likelihood of an antibiotic arms race. Further insight into the diverse roles of antibiotics in microbial ecology and evolution has significant implications for understanding the persistence of antibiotic inhibitory and resistance phenotypes in environmental microbes, optimizing antibiotic drug discovery and developing strategies for managing microbial coevolutionary dynamics to enhance inhibitory phenotypes.     

Genetic structure in insular and mainland populations of house sparrows (Passer domesticus) and their hemosporidian parasites

Small and isolated populations usually exhibit low levels of genetic variability, and thus, they are expected to have a lower capacity to adapt to changes in environmental conditions, such as exposure to pathogens and parasites. Comparing the genetic variability of selectively neutral versus functional loci allows one to assess the evolutionary history of populations and their future evolutionary potential. The genes of the major histocompatibility complex (MHC) control immune recognition of parasites, and their unusually high diversity is genes which is likely driven by parasite‐mediated balancing selection. Here, we examined diversity and differentiation of neutral microsatellite loci and functional MHC class I genes in house sparrows (Passer domesticus), living in six insular and six mainland populations, and we aimed to determine whether their diversity or differentiation correlates with the diversity and the prevalence of infection of hemosporidian parasites. We found that island bird populations tended to have lower neutral genetic variability, whereas MHC variability gene was similar between island and mainland populations. Similarly, island populations tended to show greater genetic differentiation than mainland populations, especially at microsatellite markers. The maintenance of MHC genetic diversity and its less marked structure in the island populations could be attributed to balancing‐selection. The greater MHC differentiation among populations was negatively correlated with similarity in blood parasites (prevalence and diversity of parasite strains) between populations. Even at low prevalence and small geographical scale, haemosporidian parasites might contribute to structure the variability of immune genes among populations of hosts.     

Ecological and evolutionary responses in complex communities: implications for invasions and eco‐evolutionary feedbacks

It is easier to predict the ecological and evolutionary outcomes of interactions in less diverse communities. As species are added to communities, their direct and indirect interactions multiply, their niches may shift, and there may be increased ecological redundancy. Accompanying this complexity in ecological interactions, is also complexity in selection and subsequent evolution, which may feed back to affect the ecology of the system, as species with different traits may play different ecological roles. Drawing from my own work and that of many others, I first discuss what we currently understand about ecology and evolution in light of simple and diverse communities, and suggest the importance of escape from community complexity per se in the success of invaders. Then, I examine how community complexity may influence the nature and magnitude of eco‐evolutionary feedbacks, classifying eco‐evolutionary dynamics into three general types: those generating alternative stable states, cyclic dynamics, and those maintaining ecological stasis and stability. The latter may be important and yet very hard to detect. I suggest future directions, as well as discuss methodological approaches and their potential pitfalls, in assessing the importance and longevity of eco‐evolutionary feedbacks in complex communities. Synthesis The ecology, evolution and eco‐evolutionary dynamics of simple and diverse communities are reviewed. In more diverse communities, direct and indirect interactions multiply, species’ niches often shift, ecological redundancy can increase, and selection may be less directional. Community complexity may influence the magnitude and nature of eco‐evolutionary dynamics, which are classified into three types: those generating alternative stable states, cyclic dynamics, and those maintaining ecological stasis and stability. Strengths and pitfalls of approaches to investigating eco‐evolutionary feedbacks in complex field communities are discussed.     

Convergence to a novel environment: comparative method versus experimental evolution

Abstract Laboratory adaptation allows researchers to contrast temporal studies of experimental evolution with comparative studies. The comparative method is here taken to mean the inference of microevolutionary processes from comparisons among contemporaneous populations of diverse origins, from one or multiple species. The data contrasted here come from Drosophila subobscura populations that were introduced to the laboratory at several different times and from two different locations. Two questions were addressed. First, can we correctly infer evolutionary dynamics from comparative data collected simultaneously from disparate populations? In most cases, we could, except for the character of starvation resistance. Second, are the evolutionary dynamics inferred from the comparative approach similar to those revealed by temporal studies of experimental evolution? For fecundity characters, they were. Overall the results show that both comparative and temporal studies are useful, though the former can be uninformative for characters with complex evolutionary trajectories.     

Understanding extinction debts: spatio–temporal scales,mechanisms and a roadmap for future research

Extinction debt refers to delayed species extinctions expected as a consequence of ecosystem perturbation. Quantifying such extinctions and investigating long‐term consequences of perturbations has proven challenging, because perturbations are not isolated and occur across various spatial and temporal scales, from local habitat losses to global warming. Additionally, the relative importance of eco‐evolutionary processes varies across scales, because levels of ecological organization, i.e. individuals, (meta)populations and (meta)communities, respond hierarchically to perturbations. To summarize our current knowledge of the scales and mechanisms influencing extinction debts, we reviewed recent empirical, theoretical and methodological studies addressing either the spatio–temporal scales of extinction debts or the eco‐evolutionary mechanisms delaying extinctions. Extinction debts were detected across a range of ecosystems and taxonomic groups, with estimates ranging from 9 to 90% of current species richness. The duration over which debts have been sustained varies from 5 to 570 yr, and projections of the total period required to settle a debt can extend to 1000 yr. Reported causes of delayed extinctions are 1) life‐history traits that prolong individual survival, and 2) population and metapopulation dynamics that maintain populations under deteriorated conditions. Other potential factors that may extend survival time such as microevolutionary dynamics, or delayed extinctions of interaction partners, have rarely been analyzed. Therefore, we propose a roadmap for future research with three key avenues: 1) the microevolutionary dynamics of extinction processes, 2) the disjunctive loss of interacting species and 3) the impact of multiple regimes of perturbation on the payment of debts. For their ability to integrate processes occurring at different levels of ecological organization, we highlight mechanistic simulation models as tools to address these knowledge gaps and to deepen our understanding of extinction dynamics.     

Transposable elements and microevolutionary changes in natural populations

Transposable elements (TEs) usually represent the most abundant and dynamic fraction of genomes in almost all living organisms. The overall capacity of such ‘junk DNA’ to induce mutations and foster the reorganization of functional genomes suggests that TE may be of central evolutionary significance. However, to what extent TE dynamics drive and is driven by the evolutionary trajectory of host taxa remains poorly known. Further work addressing the fate of TE insertions in natural populations is necessary to shed light on their impact on microevolutionary processes. Here, we highlight methodological approaches (i.e. transposon displays and high‐throughput sequencing), tracking TE insertions across large numbers of individuals and discuss their pitfalls and benefits for molecular ecology surveys.     

Toward an ecological synthesis: a case for habitat selection

Habitat selection, and its associated density and frequency-dependent evolution, has a profound influence on such vital phenomena as population regulation, species interactions, the assembly of ecological communities, and the origin and maintenance of biodiversity. Different strategies of habitat selection, and their importance in ecology and evolution, can often be revealed simply by plots of density in adjacent habitats. For individual species, the strategies are closely intertwined with mechanisms of population regulation, and with the persistence of populations through time. For interacting species, strategies of habitat selection are not only responsible for species coexistence, but provide one of the most convenient mechanisms for measuring competition, and the various community structures caused by competitive interactions. Other kinds of interactions, such as those between predators and prey, demonstrate that an understanding of the coevolution of habitat-selection strategies among strongly interacting species is essential to properly interpret their spatial and temporal dynamics. At the evolutionary scale, the frequency dependence associated with habitat selection may often allow populations to diverge and diversify into separate species. Habitat selection thereby demonstrates how we can map microevolutionary strategies in behavior onto their population and community consequences, and from there, onto macroevolutionary patterns of speciation and adaptive radiation. We can anticipate that future studies of habitat selection will not only help us complete those maps, but that they will also continue to enrich the panoply of ideas that shape evolutionary ecology.     

Sexual selection and the evolutionary dynamics of the major histocompatibility complex

The genes of the major histocompatibility complex (MHC) are a key component of the adaptive immune system and among the most variable loci in the vertebrate genome. Pathogen-mediated natural selection and MHC-based disassortative mating are both thought to structure MHC polymorphism, but their effects have proven difficult to discriminate in natural systems. Using the first model of MHC dynamics incorporating both survival and reproduction, we demonstrate that natural and sexual selection produce distinctive signatures of MHC allelic diversity with critical implications for understanding host–pathogen dynamics. While natural selection produces the Red Queen dynamics characteristic of host–parasite interactions, disassortative mating stabilizes allele frequencies, damping major fluctuations in dominant alleles and protecting functional variants against drift. This subtle difference generates a complex interaction between MHC allelic diversity and population size. In small populations, the stabilizing effects of sexual selection moderate the effects of drift, whereas pathogen-mediated selection accelerates the loss of functionally important genetic diversity. Natural selection enhances MHC allelic variation in larger populations, with the highest levels of diversity generated by the combined action of pathogen-mediated selection and disassortative mating. MHC-based sexual selection may help to explain how functionally important genetic variation can be maintained in populations of conservation concern.     

CHAOS AND UNPREDICTABILITY IN EVOLUTION

The possibility of complicated dynamic behavior driven by nonlinear feedbacks in dynamical systems has revolutionized science in the latter part of the last century. Yet despite examples of complicated frequency dynamics, the possibility of long‐term evolutionary chaos is rarely considered. The concept of “survival of the fittest” is central to much evolutionary thinking and embodies a perspective of evolution as a directional optimization process exhibiting simple, predictable dynamics. This perspective is adequate for simple scenarios, when frequency‐independent selection acts on scalar phenotypes. However, in most organisms many phenotypic properties combine in complicated ways to determine ecological interactions, and hence frequency‐dependent selection. Therefore, it is natural to consider models for evolutionary dynamics generated by frequency‐dependent selection acting simultaneously on many different phenotypes. Here we show that complicated, chaotic dynamics of long‐term evolutionary trajectories in phenotype space is very common in a large class of such models when the dimension of phenotype space is large, and when there are selective interactions between the phenotypic components. Our results suggest that the perspective of evolution as a process with simple, predictable dynamics covers only a small fragment of long‐term evolution.     

Eco‐evolution on the edge during climate change

We urgently need to predict species responses to climate change to minimize future biodiversity loss and ensure we do not waste limited resources on ineffective conservation strategies. Currently, most predictions of species responses to climate change ignore the potential for evolution. However, evolution can alter species ecological responses, and different aspects of evolution and ecology can interact to produce complex eco‐evolutionary dynamics under climate change. Here we review how evolution could alter ecological responses to climate change on species warm and cool range margins, where evolution could be especially important. We discuss different aspects of evolution in isolation, and then synthesize results to consider how multiple evolutionary processes might interact and affect conservation strategies. On species cool range margins, the evolution of dispersal could increase range expansion rates and allow species to adapt to novel conditions in their new range. However, low genetic variation and genetic drift in small range‐front populations could also slow or halt range expansions. Together, these eco‐evolutionary effects could cause a three‐step, stop‐and‐go expansion pattern for many species. On warm range margins, isolation among populations could maintain high genetic variation that facilitates evolution to novel climates and allows species to persist longer than expected without evolution. This ‘evolutionary extinction debt’ could then prevent other species from shifting their ranges. However, as climate change increases isolation among populations, increasing dispersal mortality could select for decreased dispersal and cause rapid range contractions. Some of these eco‐evolutionary dynamics could explain why many species are not responding to climate change as predicted. We conclude by suggesting that resurveying historical studies that measured trait frequencies, the strength of selection, or heritabilities could be an efficient way to increase our eco‐evolutionary knowledge in climate change biology.     

Genomic signatures of local adaptation in the Drosophila immune response

As environments and pathogen landscapes shift, host defenses must evolve to remain effective. Due to this selection pressure, among-species comparisons of genetic sequence data often find immune genes to be among the fastest evolving genes across the genome. The full extent and nature of these immune adaptations, however, remain largely unexplored. In a recent study, we analyzed patterns of selection within distinct components of the Drosophila melanogaster immune pathway. While we found evidence of positive selection within some immune processes, immune genes were not universally characterized by signatures of strong selection. On the contrary, we even found that some immune functions show greater than expected constraint. Overall these results highlight 2 major factors that appear to play an outsize role in determining a gene's evolutionary rate: the type of pathogen the gene targets and the gene's position within the immune network. These results join a growing body of literature that highlight the complexity of immune adaptation. Rather than there being uniformly strong selection across all immune genes, a combination of pathogen-specificity and host genetic constraints appear to play key roles in determining each immune gene's individual evolutionary trajectory.     

METABOLIC FLUX IS A DETERMINANT OF THE EVOLUTIONARY RATES OF ENZYME‐ENCODING GENES

Relationships between evolutionary rates and gene properties on a genomic, functional, pathway, or system level are being explored to unravel the principles of the evolutionary process. In particular, functional network properties have been analyzed to recognize the constraints they may impose on the evolutionary fate of genes. Here we took as a case study the core metabolic network in human erythrocytes and we analyzed the relationship between the evolutionary rates of its genes and the metabolic flux distribution throughout it. We found that metabolic flux correlates with the ratio of nonsynonymous to synonymous substitution rates. Genes encoding enzymes that carry high fluxes have been more constrained in their evolution, while purifying selection is more relaxed in genes encoding enzymes carrying low metabolic fluxes. These results demonstrate the importance of considering the dynamical functioning of gene networks when assessing the action of selection on system‐level properties.     

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.     

Social interaction in synthetic and natural microbial communities

Social interaction among cells is essential for multicellular complexity. But how do molecular networks within individual cells confer the ability to interact? And how do those same networks evolve from the evolutionary conflict between individual‐ and population‐level interests? Recent studies have dissected social interaction at the molecular level by analyzing both synthetic and natural microbial populations. These studies shed new light on the role of population structure for the evolution of cooperative interactions and revealed novel molecular mechanisms that stabilize cooperation among cells. New understanding of populations is changing our view of microbial processes, such as pathogenesis and antibiotic resistance, and suggests new ways to fight infection by exploiting social interaction. The study of social interaction is also challenging established paradigms in cancer evolution and immune system dynamics. Finding similar patterns in such diverse systems suggests that the same ‘social interaction motifs’ may be general to many cell populations.     

Opisthobranchia (Mollusca, Gastropoda) – more than just slimy slugs. Shell reduction and its implications on defence and foraging

Genetic studies have typically inferred the effects of human impact by documenting patterns of genetic differentiation and levels of genetic diversity among potentially isolated populations using selective neutral markers such as mitochondrial control region sequences, microsatellites or single nucleotide polymorphism (SNPs). However, evolutionary relevant and adaptive processes within and between populations can only be reflected by coding genes. In vertebrates, growing evidence suggests that genetic diversity is particularly important at the level of the major histocompatibility complex (MHC). MHC variants influence many important biological traits, including immune recognition, susceptibility to infectious and autoimmune diseases, individual odours, mating preferences, kin recognition, cooperation and pregnancy outcome. These diverse functions and characteristics place genes of the MHC among the best candidates for studies of mechanisms and significance of molecular adaptation in vertebrates. MHC variability is believed to be maintained by pathogen-driven selection, mediated either through heterozygote advantage or frequency-dependent selection. Up to now, most of our knowledge has derived from studies in humans or from model organisms under experimental, laboratory conditions. Empirical support for selective mechanisms in free-ranging animal populations in their natural environment is rare. In this review, I first introduce general information about the structure and function of MHC genes, as well as current hypotheses and concepts concerning the role of selection in the maintenance of MHC polymorphism. The evolutionary forces acting on the genetic diversity in coding and non-coding markers are compared. Then, I summarise empirical support for the functional importance of MHC variability in parasite resistance with emphasis on the evidence derived from free-ranging animal populations investigated in their natural habitat. Finally, I discuss the importance of adaptive genetic variability with respect to human impact and conservation, and implications for future studies.     

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.