Population responses to anthropogenic disturbance: lessons from three‐spined sticklebacks Gasterosteus aculeatus in eutrophic habitats

Human‐induced environmental changes differ from most natural changes in which they happen at a faster rate and require quicker responses from populations. The first response of populations is usually phenotypically plastic alterations of morphology, physiology and behaviour. This plasticity can be favourable and move the population closer to an adaptive peak in the altered environment and, hence, maintain a viable population, or be maladaptive and move the population further from the peak and increase the risk of extinction. The radiation of the three‐spined stickleback Gasterosteus aculeatus from the ocean to different freshwater habitats has provided much information on adaptation to new environmental conditions. Currently, human‐induced eutrophication is changing the breeding areas of these fish, which creates a model system for investigation of responses to rapid environmental disturbance. Results show that a primary reaction is plastic alterations of behaviour, with some adjustments being adaptive while others are not. At the same time, the strength of sexual selection on several traits is relaxed, which could increase the relative importance of survival selection. Whether this will restore population viability depends on the amount of standing genetic variation in the right direction. Human disturbances can be dramatic and resolution of the limit of flexibility and the possibility of genetic adaptation should be important targets of future research.     

Adaptor Protein2 (AP2) Orchestrates CXCR2‐Mediated Cell Migration

The chemokine receptor CXCR2 is vital for inflammation, wound healing, angiogenesis, cancer progression and metastasis. Adaptor protein 2 (AP2), a clathrin binding heterotetrameric protein comprised of α, β2, μ2 and σ2 subunits, facilitates clathrin‐mediated endocytosis. Mutation of the LLKIL motif in the CXCR2 carboxyl‐terminal domain (CTD) results in loss of AP2 binding to the receptor and loss of ligand‐mediated receptor internalization and chemotaxis. AP2 knockdown also results in diminished ligand‐mediated CXCR2 internalization, polarization and chemotaxis. Using knockdown/rescue approaches with AP2‐μ2 mutants, the binding domains were characterized in reference to CXCR2 internalization and chemotaxis. When in an open conformation, μ2 Patch 1 and Patch 2 domains bind tightly to membrane PIP2 phospholipids. When AP2‐μ2, is replaced with μ2 mutated in Patch 1 and/or Patch 2 domains, ligand‐mediated receptor binding and internalization are not lost. However, chemotaxis requires AP2‐μ2 Patch 1, but not Patch 2. AP2‐σ2 has been demonstrated to bind dileucine motifs to facilitate internalization. Expression of AP2‐σ2 V88D and V98S dominant negative mutants resulted in loss of CXCR2 mediated chemotaxis. Thus, AP2 binding to both membrane phosphatidylinositol phospholipids and dileucine motifs is crucial for directional migration or chemotaxis. Moreover, AP2‐mediated receptor internalization can be dissociated from AP2‐mediated chemotaxis.      

Phenology and temperature‐dependent development of Ceutorhynchus assimilis,a potential biological control agent for Lepidium draba

Lepidium draba (Brassicaceae) is a major concern for agriculture and biodiversity in the western United States. As current control methods do not provide long‐term, sustainable solutions, research has been conducted to find biological control agents. Ceutorhynchus assimilis is one of the currently investigated candidates. Known as oligophagous in the literature, a specialist clade of this root‐galling weevil exists in southern Europe. This raised the question of its ability to survive in colder climates in the target range. We investigated the phenology of C. assimilis in the field in southern France (specialist clade) and Romania (generalist clade) and measured various temperature‐dependent parameters in the laboratory. In both ranges, weevils were univoltine. Oviposition in autumn started later in France compared to Romania, while mature larvae exited galls (to pupate in the soil) earlier the following year. On average, 25% and 32% of galls from France and Romania were completely below the soil surface, respectively, and this appeared to depend on soil substrate. Weevils transported from France to Romania were able to develop, but at a much lower rate than Romanian weevils. Mortality of overwintering larvae of both clades increased with decreasing temperature and exposure time. At ?5°C, lethal times Lt₅₀ and Lt₉₅ were 15 and 42 days for the specialist clade and 26 and 72 days for the generalist clade. A higher proportion of third instar larvae compared to first and second instar larvae survived. Pupation time at different temperatures did not differ between weevils from France or Romania. A climate match model (comparing winter temperatures) indicated that the specialist clade of C. assimilis from France has the potential to establish in some parts of the target range (e.g. Washington, Oregon, California). However, temperature extremes and winters without snow cover will likely limit its establishment unless rapid adaptive evolution takes place.     

Fast evolutionary response of house mice to anthropogenic disturbance on a Sub‐Antarctic island

Invasions and anthropogenic disturbances challenge species with rapid environmental changes. Understanding how organisms respond to these changes is of major concern for the future of biodiversity. The house mouse on a Sub‐Antarctic island (Guillou Island, Kerguelen Archipelago) had to face such challenges twice: first when invading the island two centuries ago; and nowadays when coping with an in‐depth remodeling of its habitat due to a cohort of anthropogenic changes. Morphometric and biomechanical results show that the initial invasion triggered the evolution of a jaw shape adapted to the local food resources. Contemporary changes are also associated to changes in jaw morphology, but are not directly functionally relevant. Here, a complex response integrating feeding behaviour, investment in feeding structure, and degree of mineralization, may provide the mice with a better tool to benefit of wider resources utilization and/or better cope with intra‐specific competition in a changing habitat. These Sub‐Antarctic mice exemplify that success of invasive species rely on the capacity of facing rapidly varying environments through integrated, multi‐faceted responses involving behaviour to morphology through life‐history traits. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 513–526.     

Improvement of low‐temperature caseinolytic activity of a thermophilic subtilase by directed evolution and site‐directed mutagenesis

By directed evolution and subsequent site‐directed mutagenesis, cold‐adapted variants of WF146 protease, a thermophilic subtilase, have been successfully engineered. A four‐amino acid substitution variant RTN29 displayed a sixfold increase in caseinolytic activity in the temperature range of 15–25°C, a down‐shift of optimum temperature by ～15°C, as well as a decrease in thermostability, indicating it follows the general principle of trade‐off between activity and stability. Nevertheless, to some extent RTN29 remained its thermophilic nature, and no loss of activity was observed after heat‐treatment at 60°C for 2 h. Notably, RTN29 exhibited a lower hydrolytic activity toward suc‐AAPF‐pNA, due to an increase in K_m and a decrease in k_cat, in contrast to other artificially cold‐adapted subtilases with increased low‐temperature activity toward small synthetic substrates. All mutations (S100P, G108S, D114G, M137T, T153A, and S246N) identified in the cold‐adapted variants occurred within or near the substrate‐binding region. None of these mutations, however, match the corresponding sites in naturally psychrophilic and other artificially cold‐adapted subtilases, implying there are multiple routes to cold adaptation. Homology modeling and structural analysis demonstrated that these mutations led to an increase in mobility of substrate‐binding region and a modulation of substrate specificity, which seemed to account for the improvement of the enzyme's catalytic activity toward macromolecular substrates at lower temperatures. Our study may provide valuable information needed to develop enzymes coupling high stability and high low‐temperature activity, which are highly desired for industrial use. Biotechnol. Bioeng. 2009; 104: 862–870. © 2009 Wiley Periodicals, Inc.     

S100A10‐Mediated Translocation of Annexin‐A2 to SNARE Proteins in Adrenergic Chromaffin Cells Undergoing Exocytosis

In neuroendocrine cells, annexin‐A2 is implicated as a promoter of monosialotetrahexosylganglioside (GM1)‐containing lipid microdomains that are required for calcium‐regulated exocytosis. As soluble N‐ethylmaleimide‐sensitive factor attachment protein receptors (SNAREs) require a specific lipid environment to mediate granule docking and fusion, we investigated whether annexin‐A2‐induced lipid microdomains might be linked to the SNAREs present at the plasma membrane. Stimulation of adrenergic chromaffin cells induces the translocation of cytosolic annexin‐A2 to the plasma membrane, where it colocalizes with SNAP‐25 and S100A10. Cross‐linking experiments performed in stimulated chromaffin cells indicate that annexin‐A2 directly interacts with S100A10 to form a tetramer at the plasma membrane. Here, we demonstrate that S100A10 can interact with vesicle‐associated membrane protein 2 (VAMP2) and show that VAMP2 is present at the plasma membrane in resting adrenergic chromaffin cells. Tetanus toxin that cleaves VAMP2 solubilizes S100A10 from the plasma membrane and inhibits the translocation of annexin‐A2 to the plasma membrane. Immunogold labelling of plasma membrane sheets combined with spatial point pattern analysis confirmed that S100A10 is present in VAMP2 microdomains at the plasma membrane and that annexin‐A2 is observed close to S100A10 and to syntaxin in stimulated chromaffin cells. In addition, these results showed that the formation of phosphatidylinositol (4,5)‐bisphosphate (PIP₂) microdomains colocalized with S100A10 in the vicinity of docked granules, suggesting a functional interplay between annexin‐A2‐mediated lipid microdomains and SNAREs during exocytosis.     

Local parasite pressures and host genotype modulate epigenetic diversity in a mixed‐mating fish

Parasite‐mediated selection is one of the main drivers of genetic variation in natural populations. The persistence of long‐term self‐fertilization, however, challenges the notion that low genetic variation and inbreeding compromise the host's ability to respond to pathogens. DNA methylation represents a potential mechanism for generating additional adaptive variation under low genetic diversity. We compared genetic diversity (microsatellites and AFLPs), variation in DNA methylation (MS‐AFLPs), and parasite loads in three populations of Kryptolebias hermaphroditus, a predomintanly self‐fertilizing fish, to analyze the potential adaptive value of DNA methylation in relation to genetic diversity and parasite loads. We found strong genetic population structuring, as well as differences in parasite loads and methylation levels among sampling sites and selfing lineages. Globally, the interaction between parasites and inbreeding with selfing lineages influenced DNA methylation, but parasites seemed more important in determining methylation levels at the local scale.     

Invasive house mice facing a changing environment on the Sub‐Antarctic Guillou Island (Kerguelen Archipelago)

Adaptation to new environments is a key feature in evolution promoting divergence in morphological structures under selection. The house mouse (Mus musculus domesticus) introduced on the Sub‐Antarctic Guillou Island (Kerguelen Archipelago) had and still has to face environmental conditions that likely shaped the pattern and pace of its insular evolution. Since mouse arrival on the island, probably not more than two centuries ago, ecological conditions dramatically differed from those available to their Western European commensal source populations. In addition, over the last two decades, the plant and animal communities of Guillou Island were considerably modified by the eradication of rabbits, the effects of climate change and the spread of invasive species detrimental to native communities. Under such a changing habitat, the mouse response was investigated using a morphometric quantification of mandible and molar tooth, two morphological structures related to food processing. A marked differentiation of the insular mice compared with their relatives from Western Europe was documented for both mandibles and molar shapes. Moreover, these shapes changed through the 16 years of the record, in agreement with expectations of drift for the molar, but more than expected by chance for the mandible. These results suggest that mice responded to the recent changes in food resources, possibly with a part of plastic variation for the mandible prone to bone remodelling. This pattern exemplifies the intricate interplay of evolution, ecology and plasticity that is a probable key of the success of such an invasive rodent facing pronounced shifts in food resources exploitation under a changing environment.     

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.     

Experimentally induced host‐shift changes life‐history strategy in a seed beetle

Expansion of the host range in phytophagous insects depends on their ability to form an association with a novel plant through changes in host‐related traits. Phenotypic plasticity has important effects on initial survival of individuals faced with a new plant, as well as on the courses of evolutionary change during long‐term adaptation to novel conditions. Using experimental populations of the seed beetle that evolved on ancestral (common bean) or novel (chickpea) host and applying reciprocal transplant at both larval and adult stage on the alternative host plant, we studied the relationship between the initial (plastic) phases of host‐shift and the subsequent stages of evolutionary divergence in life‐history strategies between populations exposed to the host‐shift process. After 48 generations, populations became well adapted to chickpea by evolving the life‐history strategy with prolonged larval development, increased body mass, earlier reproduction, shorter lifespan and decreased plasticity of all traits compared with ancestral conditions. In chickpea‐adapted beetles, negative fitness consequences of low plasticity of pre‐adult development (revealed as severe decrease in egg‐to‐adult viability on beans) exhibited mismatch with positive effects of low plasticity (i.e. low host sensitivity) in oviposition and fecundity. In contrast, beetles adapted to the ancestral host showed high plasticity of developmental process, which enabled high larval survival on chickpea, whereas elevated plasticity in adult behaviour (i.e. high host sensitivity) resulted in delayed reproduction and decreased fecundity on chickpea. The analysis of population growth parameters revealed significant fluctuation during successive phases of the host‐shift process in A. obtectus.     

Trade‐offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans

Temperature is one of the most important environmental parameters with crucial impacts on nearly all biological processes. Due to anthropogenic activity, average air temperatures are expected to increase by a few degrees in coming decades, accompanied by an increased occurrence of extreme temperature events. Such global trends are likely to have various major impacts on human society through their influence on natural ecosystems, food production and biotic interactions, including diseases. In this study, we used a combination of statistical genetics, experimental evolution and common garden experiments to investigate the evolutionary potential for thermal adaptation in the potato late blight pathogen, Phytophthora infestans, and infer its likely response to changing temperatures. We found a trade‐off associated with thermal adaptation to heterogeneous environments in P. infestans, with the degree of the trade‐off peaking approximately at the pathogen's optimum growth temperature. A genetic trade‐off in thermal adaptation was also evidenced by the negative association between a strain's growth rate and its thermal range for growth, and warm climates selecting for a low pathogen growth rate. We also found a mirror effect of phenotypic plasticity and genetic adaptation on growth rate. At below the optimum, phenotypic plasticity enhances pathogen's growth rate but nature selects for slower growing genotypes when temperature increases. At above the optimum, phenotypic plasticity reduces pathogen's growth rate but natural selection favours for faster growing genotypes when temperature increases further. We conclude from these findings that the growth rate of P. infestans will only be marginally affected by global warming.     

Unique evolutionary trajectories in repeated adaptation to hydrogen sulphide‐toxic habitats of a neotropical fish (Poecilia mexicana)

Replicated ecological gradients are prime systems to study processes of molecular evolution underlying ecological divergence. Here, we investigated the repeated adaptation of the neotropical fish Poecilia mexicana to habitats containing toxic hydrogen sulphide (H₂S) and compared two population pairs of sulphide‐adapted and ancestral fish by sequencing population pools of >200 individuals (Pool‐Seq). We inferred the evolutionary processes shaping divergence and tested the hypothesis of increase of parallelism from SNPs to molecular pathways. Coalescence analyses showed that the divergence occurred in the face of substantial bidirectional gene flow. Population divergence involved many short, widely dispersed regions across the genome. Analyses of allele frequency spectra suggest that differentiation at most loci was driven by divergent selection, followed by a selection‐mediated reduction of gene flow. Reconstructing allelic state changes suggested that selection acted mainly upon de novo mutations in the sulphide‐adapted populations. Using a corrected Jaccard index to quantify parallel evolution, we found a negligible proportion of statistically significant parallel evolution of J_corr = 0.0032 at the level of SNPs, divergent genome regions (J_corr = 0.0061) and genes therein (J_corr = 0.0091). At the level of metabolic pathways, the overlap was J_corr = 0.2545, indicating increasing parallelism with increasing level of biological integration. The majority of pathways contained positively selected genes in both sulphide populations. Hence, adaptation to sulphidic habitats necessitated adjustments throughout the genome. The largely unique evolutionary trajectories may be explained by a high proportion of de novo mutations driving the divergence. Our findings favour Gould's view that evolution is often the unrepeatable result of stochastic events with highly contingent effects.     

Environmental variation,hybridization, and phenotypic diversification in Cuatro Ciénegas pupfishes

Hybridization can generate novel phenotypes, and in combination with divergent selection along environmental gradients, can play a driving role in phenotypic diversification. This study examined the influence of introgressive hybridization and environmental variation on the phenotypic diversity of two pupfish species (Cyprinodon atrorus and Cyprinodon bifasciatus) endemic to the Cuatro Ciénegas basin, Mexico. These species occupy opposite environmental extremes and are comprised of multiple, intraspecifically isolated populations. However, interspecific hybridization occurs to various degrees within connecting, intermediate environments. Using geometric morphometric analysis, extensive variation of body shape was observed between and within species, and phenotypic variation was strongly correlated with environmental conditions. Furthermore, some introgressed populations exhibited unique phenotypes not found in either of the parents, and overall morphospace occupation was significantly higher in introgressed populations when compared to the parentals. Overall, we find environmental variation and transgressive segregation both appear to have been important in shaping phenotypic variation in this system.     

Protistan predation interferes with bacterial long‐term adaptation to substrate restriction by selecting for defence morphotypes

Bacteria that are introduced into aquatic habitats face a low substrate environment interspersed with rare productive ‘hotspots’, as well as high protistan grazing. Whereas the former condition should select for growth performance, the latter should favour traits that reduce predation mortality, such as the formation of large cell aggregates. However, protected morphotypes often convey a growth disadvantage, and bacteria thus face a trade‐off between investing in growth or defence traits. We set up an evolutionary experiment with the freshwater isolate Sphingobium sp. strain Z007 that conditionally increases aggregate formation in supernatants from a predator–prey coculture. We hypothesized that low substrate levels would favour growth performance and reduce the aggregated subpopulation, but that the concomitant presence of a flagellate predator might conserve the defence trait. After 26 (1‐week) growth cycles either with (P+) or without (P?) predators, bacteria had evolved into strikingly different phenotypes. Strains from P? had low numbers of aggregates and increased growth yield, both at the original rich growth conditions and on various single carbon sources. By contrast, isolates from the P+ treatment formed elevated proportions of defence morphotypes, but exhibited lower growth yield and metabolic versatility. Moreover, the evolved strains from both treatments had lost phenotypic plasticity of aggregate formation. In summary, the (transient) residence of bacteria at oligotrophic conditions may promote a facultative oligotrophic life style, which is advantageous for survival in aquatic habitats. However, the investment in defence against predation mortality may constrain microbial adaptation to the abiotic environment.     

The genomic basis of eco‐evolutionary dynamics

Recent recognition that ecological and evolutionary processes can operate on similar timescales has led to a rapid increase in theoretical and empirical studies on eco‐evolutionary dynamics. Progress in the fields of evolutionary biology, genomics and ecology is greatly enhancing our understanding of rapid adaptive processes, the predictability of adaptation and the genetics of ecologically important traits. However, progress in these fields has proceeded largely independently of one another. In an attempt to better integrate these fields, the centre for ‘Adaptation to a Changing Environment’ organized a conference entitled ‘The genomic basis of eco‐evolutionary change’ and brought together experts in ecological genomics and eco‐evolutionary dynamics. In this review, we use the work of the invited speakers to summarize eco‐evolutionary dynamics and discuss how they are relevant for understanding and predicting responses to contemporary environmental change. Then, we show how recent advances in genomics are contributing to our understanding of eco‐evolutionary dynamics. Finally, we highlight the gaps in our understanding of eco‐evolutionary dynamics and recommend future avenues of research in eco‐evolutionary dynamics.     

Plasticity results in delayed breeding in a long‐distant migrant seabird

A major question for conservationists and evolutionary biologists is whether natural populations can adapt to rapid environmental change through micro‐evolution or phenotypic plasticity. Making use of 17 years of data from a colony of a long‐distant migratory seabird, the common tern (Sterna hirundo), we examined phenotypic plasticity and the evolutionary potential of breeding phenology, a key reproductive trait. We found that laying date was strongly heritable (0.27 ± 0.09) and under significant fecundity selection for earlier laying. Paradoxically, and in contrast to patterns observed in most songbird populations, laying date became delayed over the study period, by about 5 days. The discrepancy between the observed changes and those predicted from selection on laying date was explained by substantial phenotypic plasticity. The plastic response in laying date did not vary significantly among individuals. Exploration of climatic factors showed individual responses to the mean sea surface temperature in Senegal in December prior to breeding: Common terns laid later following warmer winters in Senegal. For each 1°C of warming of the sea surface in Senegal, common terns delayed their laying date in northern Germany by 6.7 days. This suggests that warmer waters provide poorer wintering resources. We therefore found that substantial plastic response to wintering conditions can oppose natural selection, perhaps constraining adaptation.