Sex in an uncertain world: environmental stochasticity helps restore competitive balance between sexually and asexually reproducing populations.

Like many organisms, individuals of the freshwater ostracod species Eucypris virens exhibit either obligate sexual or asexual reproductive modes. Both types of individual routinely co-occur, including in the same temporary freshwater pond (their natural habitat in which they undergo seasonal diapause). Given the well-known two-fold cost of sex, this begs the question of how sexually reproducing individuals are able to coexist with their asexual counterparts in spite of such overwhelming costs. Environmental stochasticity in the form of 'false dawn' inundations (where the first hydration is ephemeral and causes loss of early hatching individuals) may provide an advantage to the sexual subpopulation, which shows greater variation in hatching times following inundation. We explore the potential role of environmental stochasticity in this system using life-history data analysis, climate data, and matrix projection models. In the absence of environmental stochasticity, the population growth rate is significantly lower in sexual subpopulations. Climate data reveal that 'false dawn' inundations are common. Using matrix projection modelling with and without environmental stochasticity, we demonstrate that this phenomenon can restore appreciable balance to the system, in terms of population growth rates. This provides support for the role of environmental stochasticity in helping to explain the maintenance of sex and the occurrence of geographical parthenogenesis.

Stress dependent infection cost of the human malaria agent Plasmodium falciparum on its natural vector Anopheles coluzzii.

Unraveling selective forces that shape vector-parasite interactions has critical implications for malaria control. However, it remains unclear whether Plasmodium infection induces a fitness cost to their natural mosquito vectors. Moreover, environmental conditions are known to affect infection outcome and may impact the effect of infection on mosquito fitness. We investigated in the laboratory the effects of exposition to and infection by field isolates of Plasmodium falciparum on fecundity and survival of a major vector in the field, Anopheles coluzzii under different conditions of access to sugar resources after blood feeding. The results evidenced fitness costs induced by exposition and infection. When sugar was available after blood meal, infected and exposed mosquitoes had either reduced or equal to survival to unexposed mosquitoes while fecundity was either increased or decreased depending on the blood donor. Under strong nutritional stress, survival was reduced for exposed and infected mosquitoes in all assays. We therefore provide here evidence of an environmental-dependant reduced survival in mosquitoes exposed to infection in a natural and one of the most important parasite-mosquito species associations for human malaria transmission.

The virulence-transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies.

The adaptive hypothesis invoked to explain why parasites harm their hosts is known as the trade-off hypothesis, which states that increased parasite transmission comes at the cost of shorter infection duration. This correlation arises because both transmission and disease-induced mortality (i.e. virulence) are increasing functions of parasite within-host density. There is, however, a glaring lack of empirical data to support this hypothesis. Here, we review empirical investigations reporting to what extent within-host viral accumulation determines the transmission rate and the virulence of vector-borne plant viruses. Studies suggest that the correlation between within-plant viral accumulation and transmission rate of natural isolates is positive. Unfortunately, results on the correlation between viral accumulation and virulence are very scarce. We found only very few appropriate studies testing such a correlation, themselves limited by the fact that they use symptoms as a proxy for virulence and are based on very few viral genotypes. Overall, the available evidence does not allow us to confirm or refute the existence of a transmission-virulence trade-off for vector-borne plant viruses. We discuss the type of data that should be collected and how theoretical models can help us refine testable predictions of virulence evolution.

Parasites and deleterious mutations: interactions influencing the evolutionary maintenance of sex.

The restrictive assumptions associated with purely genetic and purely ecological mechanisms suggest that neither of the two forces, in isolation, can offer a general explanation for the evolutionary maintenance of sex. Consequently, attention has turned to pluralistic models (i.e. models that apply both ecological and genetic mechanisms). Existing research has shown that combining mutation accumulation and parasitism allows restrictive assumptions about genetic and parasite parameter values to be relaxed while still predicting the maintenance of sex. However, several empirical studies have shown that deleterious mutations and parasitism can reduce fitness to a greater extent than would be expected if the two acted independently. We show how interactions between these genetic and ecological forces can completely reverse predictions about the evolution of reproductive modes. Moreover, we demonstrate that synergistic interactions between infection and deleterious mutations can render sex evolutionarily stable even when there is antagonistic epistasis among deleterious mutations, thereby widening the conditions for the evolutionary maintenance of sex.

Parental crowding influences life-history traits in Locusta migratoria females.

Parental environments could play an important role in controlling insect outbreaks, provided they influence changes in physiological, developmental or behavioural life-history traits related to fluctuations in population density. However, the potential implication of parental influence in density-related changes in life-history traits remains unclear in many insects that exhibit fluctuating population dynamics, particularly locusts. In this study, we report a laboratory experiment, which enabled us to characterize the life-history trait modifications induced by parental crowding of female individuals from a frequently outbreaking population of Locusta migratoria (Linnaeus) (Orthoptera: Acrididae). We found that a rearing history of crowding led to reduced female oviposition times and increased offspring size but did not affect the developmental time, survival, fecundity, and the sex-ratio and the number of offspring. Because all studied females were raised in a common environment (isolation conditions), these observed reproductive differences are due to trans-generational effects induced by density. We discuss the ecological and evolutionary implications of the observed density-dependent parental effects on the life-history of L. migratoria.

Rapid evolution of Wolbachia density in insecticide resistant Culex pipiens.

The maternally inherited symbiotic Wolbachia have been previously shown to have much greater densities in insecticide-resistant Culex pipiens mosquitoes than in insecticide-susceptible individuals. These high densities were shown to be at least partially responsible for the costs related to insecticide resistance in this species. We report here the rapid evolution, on the order of 50 generations, of bacterial densities both in laboratory and field populations. Along with other recently published studies, this report shows that Wolbachia-host interactions are very dynamic.

Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles.

An understanding of the role of factors intrinsic to a species' life history in structuring contemporary genetic variation is a fundamental, but understudied, aspect of evolutionary biology. Here, we assessed the influence of the propensity to outbreak in shaping worldwide genetic variation in Locusta migratoria, a cosmopolitan pest well known for its expression of density-dependent phase polyphenism. We scored 14 microsatellites in nine subspecies from 25 populations distributed over most of the species' range in regions that vary in the historical frequency and extent of their outbreaks. We rejected the hypothesis that L. migratoria consists of two genetically distinct clusters adapted to habitats either rarely (nonoutbreaking) or cyclically (outbreaking) favourable to increases in population density. We also invalidated the current subspecific taxonomic classification based on morphometrics. Bayesian inferences indicated evidence of a homogenizing effect of outbreaks on L. migratoria population structure. Geographical and ecological barriers to gene flow in conjunction with historical events can also explain the observed patterns. By systematically assessing the effects of null alleles using computer simulations, we also provide a template for the analysis of microsatellite data sets characterized by a high prevalence of null alleles.

Resource depletion in Aedes aegypti mosquitoes infected by the microsporidia Vavraia culicis.

SUMMARYParasitic infection is often associated with changes in host life-history traits, such as host development. Many of these life-history changes are ultimately thought to be the result of a depletion or reallocation of the host's resources driven either by the host (to minimize the effects of infection) or by the parasite (to maximize its growth rate). In this paper we investigate the energetic budget of Aedes aegypti mosquito larvae infected by Vavraia culicis, a microsporidian parasite that transmits horizontally between larvae, and which has been previously shown to reduce the probability of pupation of its host. Our results show that infected larvae have significantly less lipids, sugars and glycogen than uninfected larvae. These differences in resources were not due to differences in larval energy intake (feeding rate) or expenditure (metabolic rate). We conclude that the lower energetic resources of infected mosquitoes are the result of the high metabolic demands that microsporidian parasites impose on their hosts. Given the fitness advantages for the parasite of maintaining the host in a larval stage, we discuss whether resource depletion may also be a parasite mechanism to prevent the pupation of the larvae and thus maximize its own transmission.

Proteome of Aedes aegypti larvae in response to infection by the intracellular parasite Vavraia culicis.

We report on the modification of the Aedes aegypti larval proteome following infection by the microsporidian parasite Vavraia culicis. Mosquito larvae were sampled at 5 and 15 days of age to compare the effects of infection when the parasite was in two different developmental stages. Modifications of the host proteome due to the stress of infection were distinguished from those of a more general nature by treatments involving hypoxia. We found that the major reaction to stress was the suppression of particular protein spots. Older (15 days) larvae reacted more strongly to infection by V. culicis (46% of the total number of spots affected; 17% for 5 days larvae), while the strongest reaction of younger (5 days) larvae was to hypoxia for pH range 5-8 and to combined effects of infection and hypoxia for pH range 3-6. MALDI-TOF results indicate that proteins induced or suppressed by infection are involved directly or indirectly in defense against microorganisms. Finally, our MALDI-TOF results suggest that A. aegypti larvae try to control or clear V. culicis infection and also that V. culicis probably impairs the immune defense of this host via arginases-NOS competition.

Sex-specific reaction norms to intraspecific larval competition in the mosquito Aedes aegypti.

As the relationship between a given life-history trait and fitness is not necessarily the same for the two sexes, an 'intersexual ontogenetic conflict' may arise. We analysed the phenotypic reaction to intraspecific larval competition of the mosquito, Aedes aegypti, asking: (i) Do both sexes pay the cost of competition with the same life-history traits and are they equal competitors? (ii) Is there a specific cost of competition beyond sharing food resources? We found that competition incurs a specific cost that was expressed differently by the two sexes. Indeed, each sex maintained the more important life-history trait(s) for their fitness (developmental time for males and body weight and size for females) at the expense of other traits, thus minimizing the effects of competition on their fitness. The competition exerted by females was estimated as being more intense, probably linked with the greater importance of body size for their fitness.

Spatial genetic structure of the ectoparasite Ixodes uriae within breeding cliffs of its colonial seabird host.

To examine the potential importance of the spatial subdivision of hosts for the functioning of parasite populations, we analysed patterns of local genetic structure within natural populations of the seabird ectoparasite, Ixodes uriae, at the scale of the host breeding cliff. The seabird hosts of this parasite nest in dense colonies with a hierarchical spatial organisation (individual nests-breeding cliffs-colony). Using eight microsatellite markers and samples from three breeding cliffs of the Black-legged kittiwake (Rissa tridactyla), we found that tick populations were indeed genetically structured at this spatial scale. However, the nature of this structuring depended on the characteristics of the cliffs considered. Both the host nest and cliff topography seemed to be important factors in the isolation of tick groups, but their relative roles may depend on the size of the local parasite population. We found no evidence of isolation by distance within a cliff suggesting that independent tick dispersal may not be a significant force influencing population structure in highly infested cliffs. However, genetic structure seemed to decrease with tick life stage, nymphal ticks being more strongly structured than adult ticks. These results may be related to the clustering of tick progeny combined with differential mortality and dispersal probabilities of each life stage. Overall, results indicate that the spatial organisation of hosts can indeed have important consequences for the population genetic structure of their parasites and, thus, may modify parasite dynamics and the scale at which local coevolutionary processes occur.

Significant linkage disequilibrium and high genetic diversity in a population of Plasmodium falciparum from an area (Republic of the Congo) highly endemic for malaria.

A study based on 28 microsatellite loci was performed on 32 isolates of Plasmodium falciparum from Pointe Noire (Republic of the Congo) and compared with a cosmopolitan sample of 21 isolates collected from different countries in Africa, Latin America, and Asia. The Pointe Noire population exhibited very high genetic diversity (A = 7.8 +/- 2.6, He = 0.79 +/- 0.11). Significant linkage disequilibria were observed in 28 of 378 pairs of microsatellite loci. This result could be explained by two non-exclusive hypotheses: 1) uniparental propagation (i.e., selfing), leading to non-panmictic associations, and/or 2) a Wahlund effect (i.e., spatial population genetic heterogeneity). These observations are in agreement with data previously obtained from isozyme loci of the same isolates, but contrast with other population genetic analyses conducted in other hyperendemic zones.

In vitro growth of Leishmania amazonensis promastigotes resistant to pentamidine is dependent on interactions among strains.

The in vitro growth of promastigote cells of Leishmania amazonensis was found to strongly depend on interactions among strains that differed in their pentamidine resistance. In particular, the growth of resistant strains was reduced when they shared the same environment with a less-resistant strain.

Are there pros as well as cons to being parasitized?

The diversity of ways in which parasites reduce the fitness of their hosts has been documented during the past decades, and clearly indicates that parasites can often be considered as direct agents of selection. In natural systems, however, the outcome of a host-parasite interaction might be strongly determined by other ecological factors. Parasites can be detrimental to host fitness in one environment, whereas they can be beneficial to it in another. From an evolutionary perspective, this phenomenon is of considerable importance for understanding the dynamics of coevolution among geographically structured populations evolving under different ecological pressures. Here, Frédéric Thomas and colleagues review several ecological situations in which parasitized individuals enjoy a selective advantage over unparasitized conspecifics.

Effects of density and larval competition on selected life history traits of Culex pipiens quinquefasciatus (Diptera: Culicidae).

The effects of larval densities of one to four individuals in standard Drosophila-vials (diameter 25 by 95 mm) on the age at pupation, starved dry weight, and wing length of Culex pipiens quinquefasciatus Say were studied. This approach required relatively few larvae per replicate and included a control treatment, where individual larvae developed in the absence of competition. This design also tested for competitive interactions between male and female larvae. Mosquitoes pupated later, and emerged with lighter starved dry adult weight and shorter wings as larval density increased. The size of adult female mosquitoes, particularly their starved dry weight, was sensitive to larval density and also was influenced by the presence or absence of competition with another female larva. In contrast, the life history traits of males did not vary as a function of competition with female larva. Female larvae were also more likely to die in the highest density treatment. This design confirmed previous results and offered a potentially useful experimental approach to investigate the effects of density-dependent competition among mosquito larvae.

Host life history responses to parasitism.

Parasites and their infections can adversely effect a host's growth, reproduction and survival. These effects are often not immediate, but increase with time since infection. A general prediction from evolutionary biology is that hosts suffering from this type of infection should preferentially allocate resources towards reproduction, even if this is at the expense of their growth and survival. This review illustrates this argument with several empirical studies showing hosts behaving in this manner. These studies indicate that one way for hosts to reduce the costs of parasitism is by altering their life history traits to bring forward their schedule of reproduction.

Evolution of parasite virulence against qualitative or quantitative host resistance.

We analysed the effects of two different modes of host resistance on the evolution of parasite virulence. Hosts can either adopt an all-or-nothing qualitative response (i.e. resistant hosts cannot be infected) or a quantitative form of resistance (i.e. which reduces the within-host growth rate of the parasite). We show that the mode of host resistance greatly affects the evolutionary outcome. Specifically, a qualitative form of resistance reduces parasite virulence, while a quantitative form of resistance generally selects for higher virulence.

Parasites and host life-history traits: implications for community ecology and species co-existence.

Most of the evidence for a key role of parasites in structuring communities is based on the idea of a differential susceptibility of host species to infection and its consequences. Recent advances in community ecology suggest that life-history traits of free-living species can be an important determinant of their co-existence within communities. On the other hand, parasites have the potential to indirectly alter the life-history traits of their hosts, such as developmental time or dispersal. We discuss the idea that these indirect effects could influence the structure of free-living and parasite communities. We explore this idea in relation to related concepts including 'parasitic arbitration' and engineering processes.

Evolutionarily stable dispersal rate in a metapopulation with extinctions and kin competition

We derive an analytic expression for the evolutionarily stable dispersal rate that formalizes the balance between the effects of four factors: the cost of dispersal, the extinction rate, the coefficient of relatedness and the mode of dispersal (i.e. the probability of common origin of immigrants). This result allows us to study the effects of each factor and, more interestingly, the interactions between them. In particular, we show that the evolutionarily stable dispersal rate is not always a decreasing function of the cost of dispersal and an increasing function of relatedness. These counter-intuitive results are discussed in the light of kin selection theory. We also present the results of numerical simulations in which relatedness is not a fixed parameter but depends on different parameters including dispersal itself. We discuss these results and show how the evolutionarily stable dispersal rate is affected by the environment and the life history traits of the species. More generally, this paper presents a simple formalism allowing the study of the effects of kin selection in unstable environments (i.e. with extinctions and recolonizations). The implications of this formalism for the understanding of the evolution of other life history traits is briefly discussed. Copyright 1999 Academic Press.

Dispersal and distribution of the tick Ixodes uriae within and among seabird host populations: the need for a population genetic approach.

The aim of this study was to characterize the spatial distribution of the tick Ixodes uriae within and among populations of its seabird hosts and to consider the potential insight that could be gained by a population genetic approach to the issue of dispersal of this tick. Analyses of data collected around the Avalon Peninsula, Newfoundland, indicated that both the prevalence and mean abundance of ticks varied significantly among sample locations. Whereas ticks were found on all 4 host species examined (Rissa tridactyla, Uria aalge, Alca torda, Fratercula arctica), infestation prevalence and mean abundance differed among the species. On R. tridactyla, ticks were significantly aggregated at the among-nest scale and nestling infestation was spatially autocorrelated. Conversely, ticks were not aggregated among chicks within nests. These results enabled us to make a priori predictions regarding tick dispersal and host specificity and suggest there may be spatial structure of Ixodes uriae populations at both macro- and microgeographic scales. Investigating the population genetic structure of ticks within and among populations of hosts with different breeding biologies should provide direct insight into the metapopulation dynamics of such a spatially structured system.