From Grazing Resistance to Pathogenesis: The Coincidental Evolution of Virulence Factors

To many pathogenic bacteria, human hosts are an evolutionary dead end. This begs the question what evolutionary forces have shaped their virulence traits. Why are these bacteria so virulent? The coincidental evolution hypothesis suggests that such virulence factors result from adaptation to other ecological niches. In particular, virulence traits in bacteria might result from selective pressure exerted by protozoan predator. Thus, grazing resistance may be an evolutionarily exaptation for bacterial pathogenicity. This hypothesis was tested by subjecting a well characterized collection of 31 Escherichia coli strains (human commensal or extra-intestinal pathogenic) to grazing by the social haploid amoeba Dictyostelium discoideum. We then assessed how resistance to grazing correlates with some bacterial traits, such as the presence of virulence genes. Whatever the relative population size (bacteria/amoeba) for a non-pathogenic bacteria strain, D. discoideum was able to phagocytise, digest and grow. In contrast, a pathogenic bacterium strain killed D. discoideum above a certain bacteria/amoeba population size. A plating assay was then carried out using the E. coli collection faced to the grazing of D. discoideum. E. coli strains carrying virulence genes such as iroN, irp2, fyuA involved in iron uptake, belonging to the B2 phylogenetic group and being virulent in a mouse model of septicaemia were resistant to the grazing from D. discoideum. Experimental proof of the key role of the irp gene in the grazing resistance was evidenced with a mutant strain lacking this gene. Such determinant of virulence may well be originally selected and (or) further maintained for their role in natural habitat: resistance to digestion by free-living protozoa, rather than for virulence per se.     

PLEIOTROPY CAUSES LONG-TERM GENETIC CONSTRAINTS ON LIFE-HISTORY EVOLUTION IN BRASSICA RAPA

Fundamental, long-term genetic trade-offs constrain life-history evolution in wild crucifer populations. I studied patterns of genetic constraint in Brassica rapa by estimating genetic correlations among life-history components by quantitative genetic analyses among ten wild populations, and within four populations. Genetic correlations between age and size at first reproduction were always greater than +0.8 within and among all populations studied. Although quantitative genetics might provide insight about genetic constraints if genetic parameters remain approximately constant, little evidence has been available to determine the constancy of genetic correlations. I found strong and consistent estimates of genetic correlations between life-history components, which were very similar within four natural populations. Population differentiation also showed these same trade-offs, resulting from long-term genetic constraint. For some traits, evolutionary changes among populations were incompatible with a model of genetic drift. Historical patterns of natural selection were inferred from population differentiation, suggesting that correlated response to selection has caused some traits to evolve opposite to the direct forces of natural selection. Comparison with Arabidopsis suggests that these life-history trade-offs are caused by genes that regulate patterns of resource allocation to different components of fitness. Ecological and energetic models may correctly predict these trade-offs because there is little additive genetic variation for rates of resource acquisition, but resource allocation is genetically variable.     

Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments

The adaptive potential of pathogens in novel or heterogeneous environments underpins the risk of disease epidemics. Antagonistic pleiotropy or differential resource allocation among life-history traits can constrain pathogen adaptation. However, we lack understanding of how the genetic architecture of individual traits can generate trade-offs. Here, we report a large-scale study based on 145 global strains of the fungal wheat pathogen Zymoseptoria tritici from four continents. We measured 50 life-history traits, including virulence and reproduction on 12 different wheat hosts and growth responses to several abiotic stressors. To elucidate the genetic basis of adaptation, we used genome-wide association mapping coupled with genetic correlation analyses. We show that most traits are governed by polygenic architectures and are highly heritable suggesting that adaptation proceeds mainly through allele frequency shifts at many loci. We identified negative genetic correlations among traits related to host colonization and survival in stressful environments. Such genetic constraints indicate that pleiotropic effects could limit the pathogen’s ability to cause host damage. In contrast, adaptation to abiotic stress factors was likely facilitated by synergistic pleiotropy. Our study illustrates how comprehensive mapping of life-history trait architectures across diverse environments allows to predict evolutionary trajectories of pathogens confronted with environmental perturbations.Subject terms: Population genetics, Plant sciences, Molecular evolution, Fungi     

Experimental evolution in Drosophila melanogaster: interaction of temperature and food quality selection regimes

Abstract. In Drosophila , both the phenotypic and evolutionary effect of temperature on adult size involves alterations to larval resource processing and affects other life-history traits, that is, development time but most notably, larval survival. Therefore, thermal evolution of adult body size might not be independent of simultaneous adaptation of larval traits to resource availability. Using experimental evolution lines adapted to high and low temperatures at different levels of food, we show that selection pressures interact in shaping larval resource processing. Evolution on poor food invariably leads to lower resource acquisition suggesting a cost to feeding behavior. However, following low temperature selection, lower resource acquisition led to a higher adult body size, probably by more efficient allocation to growth. In contrast, following high temperature selection, low resource acquisition benefited larval survival, possibly by reducing feeding-associated costs. We show that evolved differences to larval resource processing provide a possible proximate mechanism to variation in a suite of correlated life-history traits during adaptation to different climates. The implication for natural populations is that in nature, thermal evolution drives populations to opposite ends of an adult size versus larval survival trade-off by altering resource processing, if resource availability is limited.     

Predation on Multiple Trophic Levels Shapes the Evolution of Pathogen Virulence

The pathogen virulence is traditionally thought to co-evolve as a result of reciprocal selection with its host organism. In natural communities, pathogens and hosts are typically embedded within a web of interactions with other species, which could affect indirectly the pathogen virulence and host immunity through trade-offs. Here we show that selection by predation can affect both pathogen virulence and host immune defence. Exposing opportunistic bacterial pathogen Serratia marcescens to predation by protozoan Tetrahymena thermophila decreased its virulence when measured as host moth Parasemia plantaginis survival. This was probably because the bacterial anti-predatory traits were traded off with bacterial virulence factors, such as motility or resource use efficiency. However, the host survival depended also on its allocation to warning signal that is used against avian predation. When infected with most virulent ancestral bacterial strain, host larvae with a small warning signal survived better than those with an effective large signal. This suggests that larval immune defence could be traded off with effective defence against bird predators. However, the signal size had no effect on larval survival when less virulent control or evolved strains were used for infection suggesting that anti-predatory defence against avian predators, might be less constrained when the invading pathogen is rather low in virulence. Our results demonstrate that predation can be important indirect driver of the evolution of both pathogen virulence and host immunity in communities with multiple species interactions. Thus, the pathogen virulence should be viewed as a result of both past evolutionary history, and current ecological interactions.     

The evolution of virulence and host specialization in malaria parasites of primates

Parasite virulence, i.e. the damage done to the host, may be a by-product of the parasite's effort to maximize its fitness. Accordingly, several life-history trade-offs may explain interspecific differences in virulence, but such constraints remain little tested in an evolutionary context. In this phylogenetic study of primate malarias, I investigated the relationship between virulence and other parasite life-history traits. I used peak parasitaemia as a proxy for virulence, because it reflected parasite reproductive success and parasite-induced mortality. Peak parasitaemia was higher in specialist than in generalist species, even when confounding life-history traits were controlled. While there was a significant phylogenetic relationship between the number of competitors per host and host specialization, peak parasitaemia was unrelated to within-host competition. Therefore, the key evolutionary factor that favours virulence is host specialization, and the evolutionary success of virulent parasites, such as Plasmodium falciparum , may be better understood when the trade-off in virulence between different hosts is considered. Such phylogenetic results may help us design better protection programmes against malaria.     

Genetic Basis and Selection for Life-History Trait Plasticity on Alternative Host Plants for the Cereal Aphid Sitobion avenae

Sitobion avenae (F.) can survive on various plants in the Poaceae, which may select for highly plastic genotypes. But phenotypic plasticity was often thought to be non-genetic, and of little evolutionary significance historically, and many problems related to adaptive plasticity, its genetic basis and natural selection for plasticity have not been well documented. To address these questions, clones of S. avenae were collected from three plants, and their phenotypic plasticity under alternative environments was evaluated. Our results demonstrated that nearly all tested life-history traits showed significant plastic changes for certain S. avenae clones with the total developmental time of nymphs and fecundity tending to have relatively higher plasticity for most clones. Overall, the level of plasticity for S. avenae clones’ life-history traits was unexpectedly low. The factor ‘clone’ alone explained 27.7–62.3% of the total variance for trait plasticities. The heritability of plasticity was shown to be significant in nearly all the cases. Many significant genetic correlations were found between trait plasticities with a majority of them being positive. Therefore, it is evident that life-history trait plasticity involved was genetically based. There was a high degree of variation in selection coefficients for life-history trait plasticity of different S. avenae clones. Phenotypic plasticity for barley clones, but not for oat or wheat clones, was frequently found to be under significant selection. The directional selection of alternative environments appeared to act to decrease the plasticity of S. avenae clones in most cases. G-matrix comparisons showed significant differences between S. avenae clones, as well as quite a few negative covariances (i.e., trade-offs) between trait plasticities. Genetic basis and evolutionary significance of life-history trait plasticity were discussed.     

Environmental versus Anthropogenic Effects on Population Adaptive Divergence in the Freshwater Snail Lymnaea stagnalis

Repeated pesticide contaminations of lentic freshwater systems located within agricultural landscapes may affect population evolution in non-target organisms, especially in species with a fully aquatic life cycle and low dispersal ability. The issue of evolutionary impact of pollutants is therefore conceptually important for ecotoxicologists. The impact of historical exposure to pesticides on genetic divergence was investigated in the freshwater gastropod Lymnaea stagnalis, using a set of 14 populations from contrasted environments in terms of pesticide and other anthropogenic pressures. The hypothesis of population adaptive divergence was tested on 11 life-history traits, using Q _ST -F _ST comparisons. Despite strong neutral differentiation (mean F _ST = 0.291), five adult traits or parameters were found to be under divergent selection. Conversely, two early expressed traits showed a pattern consistent with uniform selection or trait canalization, and four adult traits appeared to evolve neutrally. Divergent selection patterns were mostly consistent with a habitat effect, opposing pond to ditch and channel populations. Comparatively, pesticide and other human pressures had little correspondence with evolutionary patterns, despite hatching rate impairment associated with global anthropogenic pressure. Globally, analyses revealed high genetic variation both at neutral markers and fitness-related traits in a species used as model in ecotoxicology, providing empirical support for the need to account for genetic and evolutionary components of population response in ecological risk assessment.     

What have two decades of laboratory life-history evolution studies onDrosophila melanogaster taught us?

A series of laboratory selection experiments onDrosophila melanogaster over the past two decades has provided insights into the specifics of life-history tradeoffs in the species and greatly refined our understanding of how ecology and genetics interact in life-history evolution. Much of what has been learnt from these studies about the subtlety of the microevolutionary process also has significant implications for experimental design and inference in organismal biology beyond life-history evolution, as well as for studies of evolution in the wild. Here we review work on the ecology and evolution of life-histories in laboratory populations ofD. melanogaster, emphasizing how environmental effects on life-history-related traits can influence evolutionary change. We discuss life-history tradeoffs—many unexpected—revealed by selection experiments, and also highlight recent work that underscores the importance to life-history evolution of cross-generation and cross-life-stage effects and interactions, sexual antagonism and sexual dimorphism, population dynamics, and the possible role of biological clocks in timing life-history events. Finally, we discuss some of the limitations of typical selection experiments, and how these limitations might be transcended in the future by a combination of more elaborate and realistic selection experiments, developmental evolutionary biology, and the emerging discipline of phenomics.     

A synthesis of the theories and concepts of early human evolution

Current evidence suggests that many of the major events in hominin evolution occurred in East Africa. Hence, over the past two decades, there has been intensive work undertaken to understand African palaeoclimate and tectonics in order to put together a coherent picture of how the environment of Africa has varied over the past 10 Myr. A new consensus is emerging that suggests the unusual geology and climate of East Africa created a complex, environmentally very variable setting. This new understanding of East African climate has led to the pulsed climate variability hypothesis that suggests the long-term drying trend in East Africa was punctuated by episodes of short alternating periods of extreme humidity and aridity which may have driven hominin speciation, encephalization and dispersals out of Africa. This hypothesis is unique as it provides a conceptual framework within which other evolutionary theories can be examined: first, at macro-scale comparing phylogenetic gradualism and punctuated equilibrium; second, at a more focused level of human evolution comparing allopatric speciation, aridity hypothesis, turnover pulse hypothesis, variability selection hypothesis, Red Queen hypothesis and sympatric speciation based on sexual selection. It is proposed that each one of these mechanisms may have been acting on hominins during these short periods of climate variability, which then produce a range of different traits that led to the emergence of new species. In the case of Homo erectus (sensu lato), it is not just brain size that changes but life history (shortened inter-birth intervals, delayed development), body size and dimorphism, shoulder morphology to allow thrown projectiles, adaptation to long-distance running, ecological flexibility and social behaviour. The future of evolutionary research should be to create evidence-based meta-narratives, which encompass multiple mechanisms that select for different traits leading ultimately to speciation.     

Local adaptation in rotifer populations

The adaptation of organisms to their environment has been a subject of study for a long time. One method to study adaptations in populations involves comparing contemporary populations of the same species under different selective regimes, in what is known as a ??local adaptation?? study. A previous study of the cyclically parthenogenetic rotifer Brachionus plicatilis found high heritabilities for some life-history traits. Some of these life-history traits significantly differed among six populations from Eastern Spain and data suggested some traits to have higher evolutionary rates than neutral genetic markers. Here, by studying the same B. plicatilis populations, we examine the variation and possible local adaptation of their main life-history traits, closely related to fitness, in relation to habitat salinity and temperature. These environmental factors have been shown to play a key role in the ecological differentiation among co-generic species of B. plicatilis. The results obtained in this study show that: (1) the seasonality of rotifer populations from Eastern Spain has profoundly influenced sexual reproduction strategies; (2) salinity is probably a key factor in the ecological specialization of some populations; and (3) rotifer populations harbour high variability in their fitness components.     

Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

How infectious disease agents interact with their host changes during the course of infection and can alter the expression of disease-related traits. Yet by measuring parasite life-history traits at one or few moments during infection, studies have overlooked the impact of variable parasite growth trajectories on disease evolution. Here we show that infection-age-specific estimates of host and parasite fitness components can reveal new insight into the evolution of parasites. We do so by characterizing the within-host dynamics over an entire infection period for five genotypes of the castrating bacterial parasite Pasteuria ramosa infecting the crustacean Daphnia magna. Our results reveal that genetic variation for parasite-induced gigantism, host castration and parasite spore loads increases with the age of infection. Driving these patterns appears to be variation in how well the parasite maintains control of host reproduction late in the infection process. We discuss the evolutionary consequences of this finding with regard to natural selection acting on different ages of infection and the mechanism underlying the maintenance of castration efficiency. Our results highlight how elucidating within-host dynamics can shed light on the selective forces that shape infection strategies and the evolution of virulence.     

Evolutionary rates for multivariate traits: the role of selection and genetic variation

A fundamental question in evolutionary biology is the relative importance of selection and genetic architecture in determining evolutionary rates. Adaptive evolution can be described by the multivariate breeders'' equation (), which predicts evolutionary change for a suite of phenotypic traits () as a product of directional selection acting on them (β) and the genetic variance–covariance matrix for those traits (G). Despite being empirically challenging to estimate, there are enough published estimates of G and β to allow for synthesis of general patterns across species. We use published estimates to test the hypotheses that there are systematic differences in the rate of evolution among trait types, and that these differences are, in part, due to genetic architecture. We find some evidence that sexually selected traits exhibit faster rates of evolution compared with life-history or morphological traits. This difference does not appear to be related to stronger selection on sexually selected traits. Using numerous proposed approaches to quantifying the shape, size and structure of G, we examine how these parameters relate to one another, and how they vary among taxonomic and trait groupings. Despite considerable variation, they do not explain the observed differences in evolutionary rates.     

Niche-driven evolution of metabolic and life-history strategies in natural and domesticated populations of Saccharomyces cerevisiae

Background  

Variation of resource supply is one of the key factors that drive the evolution of life-history strategies, and hence the interactions between individuals. In the yeast Saccharomyces cerevisiae, two life-history strategies related to different resource utilization have been previously described in strains from different industrial origins. In this work, we analyzed metabolic traits and life-history strategies in a broader collection of yeast strains sampled in various ecological niches (forest, human body, fruits, laboratory and industrial environments).     

Oviparity or viviparity? That is the question…

The modes of reproduction undoubtedly represent one of the most critical life-history traits because they profoundly affect fitness and survival. The parent–offspring conflict over the degree of parental investment may be the main selective factor in the evolution of reproduction. Although the modes of sexual reproduction are remarkably diversified in animals, the traditional typology spanning three classes does not seem to be adequate to clarify the level of parental investment. Thus, lecithotrophy does not provide any information on the retention of the zygotes inside the parent's body and matrotrophy only indicates that nutrients are provided by mother but does not make any distinction between various types of maternal care. I here present a scientific typology of the reproductive modes comprising five classes: ovuliparity, oviparity, ovo-viviparity, histotrophic viviparity and hemotrophic viviparity. Based on the development stage of the zygote and on its interrelation with the parent, my classification details the degree of contrivances by which animals provide alternative parental investment in their offspring. Hence, this typology possesses a great heuristic value, both in reproduction and evolutionary biology. These different modes of reproduction do represent a sequence, with ovuliparity being the most primitive and hemotrophic viviparity the most advanced mode. Lastly, the comparative analysis of different reproductive modes in vertebrates suggests that climatic conditions (cold) could be one of the strongest selection pressures for extending egg retention and the establishment of viviparity.     

Phages can constrain protist predation-driven attenuation of Pseudomonas aeruginosa virulence in multienemy communities

The coincidental theory of virulence predicts that bacterial pathogenicity could be a by-product of selection by natural enemies in environmental reservoirs. However, current results are ambiguous and the simultaneous impact of multiple ubiquitous enemies, protists and phages on virulence evolution has not been investigated previously. Here we tested experimentally how Tetrahymena thermophila protist predation and PNM phage parasitism (bacteria-specific virus) alone and together affect the evolution of Pseudomonas aeruginosa PAO1 virulence, measured in wax moth larvae. Protist predation selected for small colony types, both in the absence and presence of phage, which showed decreased edibility to protists, reduced growth in the absence of enemies and attenuated virulence. Although phage selection alone did not affect the bacterial phenotype, it weakened protist-driven antipredatory defence (biofilm formation), its associated pleiotropic growth cost and the correlated reduction in virulence. These results suggest that protist selection can be a strong coincidental driver of attenuated bacterial virulence, and that phages can constrain this effect owing to effects on population dynamics and conflicting selection pressures. Attempting to define causal links such as these might help us to predict the cold and hot spots of coincidental virulence evolution on the basis of microbial community composition of environmental reservoirs.     

Energetics and life-history of bats in comparison to small mammals

Mammals can be aligned along a slow-fast life-history continuum and a low–high metabolic rate continuum based on their traits. Small non-volant mammals occupy the fast/high end in both continua with high reproductive rates and short life spans linked with high mass-specific metabolic rates. Bats occupy the high end of the metabolic continuum, but the slow end of the life-history continuum with low reproductive rates and long life spans. Typically, both continua are linked, and similar life-history traits of species are reflected in more similar metabolic rates. We therefore hypothesized that metabolic rates are similar in species with similar life-history traits. Resting metabolic rates (RMR) were measured for three ecologically and morphologically similar sympatric bat species (Myotis nattereri, M. bechsteinii, and Plecotus auritus; Vespertilionidae) and compared to data from other similar-sized, temperate insectivorous mammals with other life-history strategies. The bat species share similar life-histories and RMRs, both of which differ from the remaining mammals and therefore supporting our hypothesis. To verify that bats are similar in RMR, two energetically contrasting periods were compared. RMRs in post-lactating females did not differ between bat species. It was, however, positively correlated with parasite load in both Myotis species. However, RMRs differed during energy-demanding pregnancy where M. nattereri had the significantly lowest RMR, suggesting metabolic compensation as an energy-saving strategy. We conclude that the energy requirements of bat species with similar life-history traits resemble each other during periods of low energetic demands and are more similar to each other than to other small temperate mammals.     

Predicting evolutionary responses to selection on polyandry in the wild: additive genetic covariances with female extra-pair reproduction

The evolutionary forces that underlie polyandry, including extra-pair reproduction (EPR) by socially monogamous females, remain unclear. Selection on EPR and resulting evolution have rarely been explicitly estimated or predicted in wild populations, and evolutionary predictions are vulnerable to bias due to environmental covariances and correlated selection through unmeasured traits. However, evolutionary responses to (correlated) selection on any trait can be directly predicted as additive genetic covariances (cov_A) with appropriate components of relative fitness. I used comprehensive life-history, paternity and pedigree data from song sparrows (Melospiza melodia) to estimate cov_A between a female''s liability to produce extra-pair offspring and two specific fitness components: relative annual reproductive success (ARS) and survival to recruitment. All three traits showed non-zero additive genetic variance. Estimates of cov_A were positive, predicting evolution towards increased EPR, but 95% credible intervals overlapped zero. There was therefore no conclusive prediction of evolutionary change in EPR due to (correlated) selection through female ARS or recruitment. Negative environmental covariance between EPR and ARS would have impeded evolutionary prediction from phenotypic selection differentials. These analyses demonstrate an explicit quantitative genetic approach to predicting evolutionary responses to components of (correlated) selection on EPR that should be unbiased by environmental covariances and unmeasured traits.     

Evolution in stressful environments. I. Phenotypic variability, phenotypic selection, and response to selection in five distinct environmental stresses

Considerable debate has accompanied efforts to integrate the selective impacts of environmental stresses into models of life-history evolution. This study was designed to determine if different environmental stresses have consistent phenotypic effects on life-history characters and whether selection under different stresses leads to consistent evolutionary responses. We created lineages of a wild mustard (Sinapis arvensis) that were selected for three generations under five stress regimes (high boron, high salt, low light, low water, or low nutrients) or under near-optimal conditions (control). Full-sibling families from the six selection histories were divided among the same six experimental treatments. In that test generation, lifetime plant fecundity and six phenotypic traits were measured for each plant. Throughout this greenhouse study, plants were grown individually and stresses were applied from the early seedling stage through senescence. Although all stresses consistently reduced lifetime fecundity and most size- and growth-related traits, different stresses had contrasting effects on flowering time. On average, stress delayed flowering compared to favorable conditions, although plants experiencing low nutrient stress flowered earliest and those experiencing low light flowered latest. Contrary to expectations of Grime's triangle model of life-history evolution, this ruderal species does not respond phenotypically to poor environments by flowering earlier. Most stresses enhanced the evolutionary potential of the study population. Compared with near-optimal conditions, stresses tended to increase the opportunity for selection as well as phenotypic variance, although both of these quantities were reduced in some stresses. Rather than favoring traits characteristic of stress tolerance, such as slow growth and delayed reproduction, phenotypic selection favored stress-avoidance traits: earlier flowering in all five stress regimes and faster seedling height growth in three stresses. Phenotypic correlations reinforced direct selection on these traits under stress, leading to predicted phenotypic change under stress, but no significant selection in the control environment. As a result of these factors, selection under stress resulted in an evolutionary shift toward earlier flowering. Environmental stresses may drive populations of ruderal plant species like S. arvensis toward a stress-avoidance strategy, rather than toward stress tolerance. Further studies will be needed to determine when selection in stressful environments leads to these alternative life-history strategies.     

Predicting the response to simultaneous selection: genetic architecture and physiological constraints

A great deal is known about the evolutionary significance of body size and development time. They are determined by the nonlinear interaction of three physiological traits: two hormonal events and growth rate (GR). In this study we investigate how the genetic architecture of the underlying three physiological traits affects the simultaneous response to selection on the two life-history traits in the hawkmoth Manduca sexta. The genetic architecture suggests that when the two life-history traits are both selected in the same direction (to increase or decrease) the response to selection is primarily determined by the hormonal mechanism. When the life-history traits are selected in opposite directions (one to increase and one to decrease) the response to selection is primarily determined by factors that affect the GR. To determine how the physiological traits affect the response to selection of the life-history traits, we simulated the predicted response to 10 generations of selection. A total of 83% of our predictions were supported by the simulation. The main components of this physiological framework also exist in unicellular organisms, vertebrates, and plants and can thus provide a robust framework for understanding how underlying physiology can determine the simultaneous evolution of life-history traits.