Within-host viral evolution in a heterogeneous environment: insights into the HIV co-receptor switch

A virus infecting a host faces a heterogeneous and a spatially structured environment. Using a mathematical model that incorporates two types of target cells and spatial structuring, we investigate conditions for viral within-host diversification. We show that branching occurs for a wide range of parameters but that it always requires some spatial structure. Applying our model to the case of HIV, we show that it captures three main properties of the 'co-receptor switch' observed in many HIV infections: the initial dominance of virus strains that infect CCR5(+) cells, the late switch in some (but, importantly, not all) HIV infections and the associated drop in the number of uninfected T-cells. This suggests that the co-receptor switch could result from gradual adaptation of the virus population to target cell heterogeneity. More generally, we argue that evolutionary ecology can help us better understand the course of some infections.     

Ecological factors driving the long-term evolution of influenza's host range

The evolution of a pathogen''s host range is shaped by the ecology of its hosts and by the physiological traits that determine host specificity. For many pathogen traits, there is a trade-off: a phenotype suitable for infecting one set of hosts poorly infects another. Introducing and analysing a simple evo-epidemiological model, here we study how such a trade-off is expected to affect evolution of the host ranges of influenza viruses. We examine a quantitative trait underlying host specificity, given by an influenza virus''s degree of adaptation to certain conformations of sialic acid receptors, and investigate how this receptor preference evolves in a minimal network of host species, including humans, that differ in life history and receptor physiology. Using adaptive dynamics theory, we establish thresholds in interspecific transmission rates and host population sizes that govern the emergence and persistence of human-adapted viruses. These ecological thresholds turn out to be largely independent of the strength of the evolutionary trade-off, underscoring the importance of ecological conditions in determining a disease''s host range.     

Virulence evolution and the trade‐off hypothesis: history,current state of affairs and the future

It has been more than two decades since the formulation of the so‐called ‘trade‐off’ hypothesis as an alternative to the then commonly accepted idea that parasites should always evolve towards avirulence (the ‘avirulence hypothesis’). The trade‐off hypothesis states that virulence is an unavoidable consequence of parasite transmission; however, since the 1990s, this hypothesis has been increasingly challenged. We discuss the history of the study of virulence evolution and the development of theories towards the trade‐off hypothesis in order to illustrate the context of the debate. We investigate the arguments raised against the trade‐off hypothesis and argue that trade‐offs exist, but may not be of the simple form that is usually assumed, involving other mechanisms (and life‐history traits) than those originally considered. Many processes such as pathogen adaptation to within‐host competition, interactions with the immune system and shifting transmission routes, will all be interrelated making sweeping evolutionary predictions harder to obtain. We argue that this is the heart of the current debate in the field and while species‐specific models may be better predictive tools, the trade‐off hypothesis and its basic extensions are necessary to assess the qualitative impacts of virulence management strategies.     

Idiosyncratic evolution of maternal effects in response to juvenile malnutrition in Drosophila

Maternal effects often affect fitness traits, but there is little experimental evidence pertaining to their contribution to response to selection imposed by novel environments. We studied the evolution of maternal effects in Drosophila populations selected for tolerance to chronic larval malnutrition. To this end, we performed pairwise reciprocal F₁ crosses between six selected (malnutrition tolerant) populations and six unselected control populations and assessed the effect of cross direction on larval growth and developmental rate, adult weight and egg‐to‐adult viability expressed under the malnutrition regime. Each pair of reciprocal crosses revealed large maternal effects (possibly including cytoplasmic genetic effects) on at least one trait, but the magnitude, sign and which traits were affected varied among populations. Thus, maternal effects contributed significantly to the response to selection imposed by the malnutrition regime, but these changes were idiosyncratic, suggesting a rugged adaptive landscape. Furthermore, although the selected populations evolved both faster growth and higher viability, the maternal effects on growth rate and viability were negatively correlated across populations. Thus, genes mediating maternal effects can evolve to partially counteract the response to selection mediated by the effects of alleles on their own carriers’ phenotype, and maternal effects may contribute to evolutionary trade‐offs between components of offspring fitness.     

Response of life‐history traits to artificial and natural selection for virulence and nonvirulence in a Drosophila parastitoid,Asobara tabida

Co‐evolution of host–parasitoid interactions is determined by the costs of host resistance, which received empirical evidence, and the costs of parasitoid virulence, which have been mostly hypothesized. Asobara tabida is a parasitoid, which mainly parasitizes Drosophila melanogaster and D. subobscura, the first species being able to resist to the parasitoid development while the second species is not. To parasitize resistant hosts, including D. melanogaster, A. tabida develops sticky eggs, which prevent encapsulation, but this virulence mechanism may be costly. Interindividual and interpopulation variation in the proportion of sticky eggs respectively allowed us to (i) artificially select and compare life‐history traits of a virulent and a nonvirulent laboratory strain, and (ii) compare a virulent and a nonvirulent field strain, to investigate the hypothetical costs of virulence. We observed strong differences between the 2 laboratory strains. The nonvirulent strain invested fewer resources in reproduction and walked less than the virulent one but lived longer. Concerning the field strains, we observed that the nonvirulent strain had larger wings while the virulent one walked more and faster. All together, our results suggest that virulence may not always be costly, but rather that different life histories associated with different levels of virulence may coexist at both intra‐ and interpopulation levels.     

A UNIFIED MODEL FOR THE COEVOLUTION OF RESISTANCE,TOLERANCE, AND VIRULENCE

We present a general host–parasite model that unifies previous theory by investigating the coevolution of virulence, resistance, and tolerance, with respect to multiple physiological, epidemiological, and environmental parameters. Four sets of new predictions emerge. First, compared to virulence coevolving with resistance or tolerance, three‐trait coevolution promotes more virulence and less tolerance, and broadens conditions under which pure defenses evolve. Second, the cost and efficiency of virulence and the epidemiological rates are the key factors of virulence coevolving with resistance and tolerance. Maximum virulence evolves for intermediate infection rate, at which coevolved levels of resistance and tolerance are both high. The influence of host and parasite background mortalities is strong on the evolution of defenses and weak on the coevolution of virulence. Third, evolutionary correlations between defenses can switch sign along single‐parameter gradients. The evolutionary trade‐off between resistance and tolerance may coevolve with virulence that either increases or decreases monotonically, depending on the underlying parameter gradient. Fourth, despite global attractiveness and stability of coevolutionary equilibria, not‐so‐rare and not‐so‐small mutations can beget large variation in virulence and defenses around equilibrium, in the form of transient “evolutionary spikes.” Implications for evolutionary management of infections are discussed and directions for future research are outlined.     

Environmental determinants of population divergence in life‐history traits for an invasive species: climate,seasonality and natural enemies

Invasive species cope with novel environments through both phenotypic plasticity and evolutionary change. However, the environmental factors that cause evolutionary divergence in invasive species are poorly understood. We developed predictions for how different life‐history traits, and plasticity in those traits, may respond to environmental gradients in seasonal temperatures, season length and natural enemies. We then tested these predictions in four geographic populations of the invasive cabbage white butterfly (Pieris rapae) from North America. We examined the influence of two rearing temperatures (20 and 26.7 °C) on pupal mass, pupal development time, immune function and fecundity. As predicted, development time was shorter and immune function was greater in populations adapted to longer season length. Also, phenotypic plasticity in development time was greater in regions with shorter growing seasons. Populations differed significantly in mean and plasticity of body mass and fecundity, but these differences were not associated with seasonal temperatures or season length. Our study shows that some life‐history traits, such as development time and immune function, can evolve rapidly in response to latitudinal variation in season length and natural enemies, whereas others traits did not. Our results also indicate that phenotypic plasticity in development time can also diverge rapidly in response to environmental conditions for some traits.     

Mobility as an emergent property of biological organization: Insights from experimental evolution

Anthropologists accept that mobility is a critical dimension of human culture, one that links economy, technology, and social relations. Less often acknowledged is that mobility depends on complex and dynamic interactions between multiple levels of our biological organization, including anatomy, physiology, neurobiology, and genetics. Here, we describe a novel experimental approach to examining the biological foundations of mobility, using mice from a long‐term artificial selection experiment for high levels of voluntary exercise on wheels. In this experiment, mice from selectively bred lines have evolved to run roughly three times as far per day as those from nonselected control lines. We consider three insights gleaned from this experiment as foundational principles for the study of mobility from the perspective of biological evolution. First, an evolutionary change in mobility will necessarily be associated with alterations in biological traits both directly and indirectly connected to mobility. Second, changing mobility will result in trade‐offs and constraints among some of the affected traits. Third, multiple solutions exist to altering mobility, so that various combinations of adjustments to traits linked with mobility can achieve the same overall behavioral outcome. We suggest that anthropological knowledge of variation in human mobility might be improved by greater research attention to its biological dimensions.     

The evolution of trade-offs under directional and correlational selection

Using quantitative genetic theory, we develop predictions for the evolution of trade-offs in response to directional and correlational selection. We predict that directional selection favoring an increase in one trait in a trade-off will result in change in the intercept but not the slope of the trade-off function, with the mean value of the selected trait increasing and that of the correlated trait decreasing. Natural selection will generally favor an increase in some combination of trait values, which can be represented as directional selection on an index value. Such selection induces both directional and correlational selection on the component traits. Theory predicts that selection on an index value will also change the intercept but not the slope of the trade-off function but because of correlational selection, the direction of change in component traits may be in the same or opposite directions. We test these predictions using artificial selection on the well-established trade-off between fecundity and flight capability in the cricket, Gryllus firmus and compare the empirical results with a priori predictions made using genetic parameters from a separate half-sibling experiment. Our results support the predictions and illustrate the complexity of trade-off evolution when component traits are subject to both directional and correlational selection.     

Experimental evolution reveals differences between phenotypic and evolutionary responses to population density

Group living can select for increased immunity, given the heightened risk of parasite transmission. Yet, it also may select for increased male reproductive investment, given the elevated risk of female multiple mating. Trade‐offs between immunity and reproduction are well documented. Phenotypically, population density mediates both reproductive investment and immune function in the Indian meal moth, Plodia interpunctella. However, the evolutionary response of populations to these traits is unknown. We created two replicated populations of P. interpunctella, reared and mated for 14 generations under high or low population densities. These population densities cause plastic responses in immunity and reproduction: at higher numbers, both sexes invest more in one index of immunity [phenoloxidase (PO) activity] and males invest more in sperm. Interestingly, our data revealed divergence in PO and reproduction in a different direction to previously reported phenotypic responses. Males evolving at low population densities transferred more sperm, and both males and females displayed higher PO than individuals at high population densities. These positively correlated responses to selection suggest no apparent evolutionary trade‐off between immunity and reproduction. We speculate that the reduced PO activity and sperm investment when evolving under high population density may be due to the reduced population fitness predicted under increased sexual conflict and/or to trade‐offs between pre‐ and post‐copulatory traits.     

Propagule interactions and the evolution of virulence

The evolution of parasite virulence is thought to involve a trade‐off between parasite reproductive rate and the effect of increasing the number of propagules on host survivorship. Such a trade‐off should lead to selection for an intermediate level of within‐host reproduction (λ). Here I consider the effects of parasite propagule number on selection affecting λ when (i) the effect of each propagule is independent of propagule number, and (ii) when the effect of each propagule changes as a function of propagule number. Virulence evolves in these models as a correlated response to selection on λ. If each propagule has the same effect (s) as all previous propagules, the survivorship of infected hosts is reduced by more than 60% at equilibrium, independent of the value of s. If, instead, each propagule has a more negative effect on host survivorship than previous propagules, host survivorship at equilibrium is expected to increase as the effect becomes more pronounced. These results are directly parallel to results derived for population mean fitness at mutation‐selection balance; and they suggest that high virulence should be associated with parasites for which the effect of adding propagules either remains constant or diminishes with propagule number.     

The experimental evolution of herbicide resistance in Chlamydomonas reinhardtii results in a positive correlation between fitness in the presence and absence of herbicides

Pleiotropic fitness trade-offs will be key determinants of the evolutionary dynamics of selection for pesticide resistance. However, for herbicide resistance, empirical support for a fitness cost of resistance is mixed, and it is therefore also questionable what further ecological trade-offs can be assumed to apply to herbicide resistance. Here, we test the existence of trade-offs by experimentally evolving herbicide resistance in Chlamydomonas reinhardtii. Although fitness costs are detected for all herbicides, we find that, counterintuitively, the most resistant populations also have the lowest fitness costs as measured by growth rate in the ancestral environment. Furthermore, after controlling for differences in the evolutionary dynamics of resistance to different herbicides, we also detect significant positive correlations between resistance, fitness in the ancestral environment and cross-resistance to other herbicides. We attribute this to the highest levels of nontarget-site resistance being achieved by fixing mutations that more broadly affect cellular physiology, which results in both more cross-resistance and less overall antagonistic pleiotropy on maximum growth rate. Consequently, the lack of classical ecological trade-offs could present a major challenge for herbicide resistance management.     

Escherichia coli populations adapt to complex,unpredictable fluctuations by minimizing trade‐offs across environments

In nature, organisms are simultaneously exposed to multiple stresses (i.e. complex environments) that often fluctuate unpredictably. Although both these factors have been studied in isolation, the interaction of the two remains poorly explored. To address this issue, we selected laboratory populations of Escherichia coli under complex (i.e. stressful combinations of pH, H₂O₂ and NaCl) unpredictably fluctuating environments for ~900 generations. We compared the growth rates and the corresponding trade‐off patterns of these populations to those that were selected under constant values of the component stresses (i.e. pH, H₂O₂ and NaCl) for the same duration. The fluctuation‐selected populations had greater mean growth rate and lower variation for growth rate over all the selection environments experienced. However, whereas the populations selected under constant stresses experienced trade‐offs in the environments other than those in which they were selected, the fluctuation‐selected populations could bypass the across‐environment trade‐offs almost entirely. Interestingly, trade‐offs were found between growth rates and carrying capacities. The results suggest that complexity and fluctuations can strongly affect the underlying trade‐off structure in evolving populations.     

When to store energy in a stochastic environment

The ability to store energy enables organisms to deal with temporarily harsh and uncertain conditions. Empirical studies have demonstrated that organisms adapted to fluctuating energy availability plastically adjust their storage strategies. So far, however, theoretical studies have investigated general storage strategies only in constant or deterministically varying environments. In this study, we analyze how the ability to store energy influences optimal energy allocation to storage, reproduction, and maintenance in environments in which energy availability varies stochastically. We find that allocation to storage is evolutionarily optimal when environmental energy availability is intermediate and energy stores are not yet too full. In environments with low variability and low predictability of energy availability, it is not optimal to store energy. As environments become more variable or more predictable, energy allocation to storage is increasingly favored. By varying environmental variability, environmental predictability, and the cost of survival, we obtain a variety of different optimal life-history strategies, from highly iteroparous to semelparous, which differ significantly in their storage patterns. Our results demonstrate that in a stochastically varying environment simultaneous allocation to reproduction, maintenance, and storage can be optimal, which contrasts with previous findings obtained for deterministic environments.     

Evolution of specialized microbial cooperation in dynamic fluids

Here, we study the evolution of specialization using realistic computer simulations of bacteria that secrete two public goods in a dynamic fluid. Through this first‐principles approach, we find physical factors such as diffusion, flow patterns and decay rates are as influential as fitness economics in governing the evolution of community structure, to the extent that when mechanical factors are taken into account, (a) generalist communities can resist becoming specialists despite the invasion fitness of specialization; (b) generalist and specialists can both resist cheaters despite the invasion fitness of free‐riding; and (c) multiple community structures can coexist despite the opposing force of competitive exclusion. Our results emphasize the role of spatial assortment and physical forces on niche partitioning and the evolution of diverse community structures.     

The effect of brain size evolution on feeding propensity,digestive efficiency,and juvenile growth

One key hypothesis in the study of brain size evolution is the expensive tissue hypothesis; the idea that increased investment into the brain should be compensated by decreased investment into other costly organs, for instance the gut. Although the hypothesis is supported by both comparative and experimental evidence, little is known about the potential changes in energetic requirements or digestive traits following such evolutionary shifts in brain and gut size. Organisms may meet the greater metabolic requirements of larger brains despite smaller guts via increased food intake or better digestion. But increased investment in the brain may also hamper somatic growth. To test these hypotheses we here used guppy (Poecilia reticulata) brain size selection lines with a pronounced negative association between brain and gut size and investigated feeding propensity, digestive efficiency (DE), and juvenile growth rate. We did not find any difference in feeding propensity or DE between large‐ and small‐brained individuals. Instead, we found that large‐brained females had slower growth during the first 10 weeks after birth. Our study provides experimental support that investment into larger brains at the expense of gut tissue carries costs that are not necessarily compensated by a more efficient digestive system.     

Constraints on the evolution of tolerance to herbicide in the common morning glory: resistance and tolerance are mutually exclusive

Evolutionary biologists explain the maintenance of intermediate levels of defense in plant populations as being due to trade-offs, or negative genetic covariances among ecologically important traits. Attempts at detecting trade-offs as constraints on the evolution of defense have not always been successful, leading some to conclude that such trade-offs rarely explain current levels of defense in the population. Using the agricultural pest Ipomoea purpurea, we measured correlations between traits involved in defense to glyphosate, the active ingredient in Roundup, a widely used herbicide. We found significant allocation costs of tolerance, as well as trade-offs between resistance and two measures of tolerance to glyphosate. Selection on resistance and tolerance exhibited differing patterns: tolerance to leaf damage was under negative directional selection, whereas resistance was under positive directional selection. The joint pattern of selection on resistance and tolerance to leaf damage indicated the presence of alternate peaks in the fitness landscape such that a combination of either high tolerance and low resistance, or high resistance and low tolerance was favored. The widespread use of this herbicide suggests that it is likely an important selective agent on weed populations. Understanding the evolutionary dynamics of herbicide defense traits is thus of increasing importance in the context of human-mediated evolution.     

Migratory costs and contemporary evolution of reproductive allocation in male chinook salmon

Energetically demanding migrations may impact the resources available for reproductive trait development and activity, and hence favour evolution of new investment strategies for remaining resources. We conducted a large-scale experiment to evaluate the proximate cost of migration on male reproductive investment in chinook salmon (Oncorhynchus tshawytscha) and contemporary evolution of reproductive allocation. Experimentally induced differences in migratory costs (17 km inland and 17 m elevation vs. 100 km and 430 m) influenced dorsal hump size and upper jaw length, two traits influencing male mating success that are developed during migration. Longer migration also reduced tissue energy reserves available for competition and length of breeding life. Corresponding shifts in the balance between natural and sexual selection appear to have been responsible for heritable population divergence in secondary sexual trait investment, in approximately 26 generations, following colonization of spawning sites with different migratory demands.     

The impact of uniform and mixed species blood meals on the fitness of the mosquito vector Anopheles gambiae s.s: does a specialist pay for diversifying its host species diet?

We investigated the fitness consequences of specialization in an organism whose host choice has an immense impact on human health: the African malaria vector Anopheles gambiae s.s. We tested whether this mosquito’s specialism on humans can be attributed to the relative fitness benefits of specialist vs. generalist feeding strategies by contrasting their fecundity and survival on human‐only and mixed host diets consisting of blood meals from humans and animals. When given only one blood meal, An. gambiae s.s. survived significantly longer on human and bovine blood, than on canine or avian blood. However, when blood fed repeatedly, there was no evidence that the fitness of An. gambiae s.s. fed a human‐only diet was greater than those fed generalist diets. This suggests that the adoption of generalist host feeding strategies in An. gambiae s.s. is not constrained by intraspecific variation in the resource quality of blood from other available host species.     

A framework to gauge the epidemic potential of plant pathogens in environmental reservoirs: the example of kiwifruit canker

New economically important diseases on crops and forest trees emerge recurrently. An understanding of where new pathogenic lines come from and how they evolve is fundamental for the deployment of accurate surveillance methods. We used kiwifruit bacterial canker as a model to assess the importance of potential reservoirs of new pathogenic lineages. The current kiwifruit canker epidemic is at least the fourth outbreak of the disease on kiwifruit caused by Pseudomonas syringae in the mere 50 years in which this crop has been cultivated worldwide, with each outbreak being caused by different genetic lines of the bacterium. Here, we ask whether strains in natural (non‐agricultural) environments could cause future epidemics of canker on kiwifruit. To answer this question, we evaluated the pathogenicity, endophytic colonization capacity and competitiveness on kiwifruit of P. syringae strains genetically similar to epidemic strains and originally isolated from aquatic and subalpine habitats. All environmental strains possessing an operon involved in the degradation of aromatic compounds via the catechol pathway grew endophytically and caused symptoms in kiwifruit vascular tissue. Environmental and epidemic strains showed a wide host range, revealing their potential as future pathogens of a variety of hosts. Environmental strains co‐existed endophytically with CFBP 7286, an epidemic strain, and shared about 20 virulence genes, but were missing six virulence genes found in all epidemic strains. By identifying the specific gene content in genetic backgrounds similar to known epidemic strains, we developed criteria to assess the epidemic potential and to survey for such strains as a means of forecasting and managing disease emergence.