Proteome allocation and the evolution of metabolic cross-feeding.

In a common instance of metabolic cross-feeding (MCF), an organism incompletely metabolizes nutrients and releases metabolites that are used by another to produce energy or building blocks. Why would the former waste edible food, and why does this preferentially occur at specific locations in a metabolic pathway have challenged evolutionary theory for decades. To address these questions, we combine adaptive dynamics with an explicit model of cell metabolism, including enzyme-driven catalysis of metabolic reactions and the cellular constraints acting on the proteome that may incur a cost to expressing all enzymes along a pathway. After pointing out that cells should in principle prioritize upstream reactions when metabolites are restrained inside the cell, we show that the occurrence of permeability-driven MCF is rare and requires that an intermediate metabolite be extremely diffusive. Indeed, only at very high levels of membrane permeability (consistent with those of acetate and glycerol, for instance) and under distinctive sets of parameters should the population diversify and MCF evolve. These results help understand the origins of simple microbial communities, such as those that readily evolve in short-term evolutionary experiments, and may later be extended to investigate how evolution has progressively built up today's extremely diverse ecosystems.

Hormonal pleiotropy and the evolution of allocation trade-offs.

Recent empirical evidence suggests that trade-off relationships can evolve, challenging the classical image of their high entrenchment. For energy reliant traits, this relationship should depend on the endocrine system that regulates resource allocation. Here, we model changes in this system by mutating the expression and conformation of its constitutive hormones and receptors. We show that the shape of trade-offs can indeed evolve in this model through the combined action of genetic drift and selection, such that their evolutionarily expected curvature and length depend on context. In particular, the shape of a trade-off should depend on the cost associated with resource storage, itself depending on the traded resource and on the ecological context. Despite this convergence at the phenotypic level, we show that a variety of physiological mechanisms may evolve in similar simulations, suggesting redundancy at the genetic level. This model should provide a useful framework to interpret and unify the overly complex observations of evolutionary endocrinology and evolutionary ecology.

Robust Frankia phylogeny, species delineation and intraspecies diversity based on Multi-Locus Sequence Analysis (MLSA) and Single-Locus Strain Typing (SLST) adapted to a large sample size.

Diazotrophic Actinobacteria of the genus Frankia represent a challenge to classical bacterial taxonomy as they include many unculturable strains. As a consequence, we still have a poor understanding of their diversity, evolution and biogeography. In this study, a Multi-Locus Sequence Analysis (MLSA) using atpD, dnaA, ftsZ, pgk, and rpoB loci was done on a large set of cultured and uncultured strains, compared to 16S rRNA and correlated to Average Nucleotide Identity (ANI) from available Frankia genomes. MLSA provided a robust resolution of Frankia genus phylogeny and clarified the status of unresolved species and complex of species. The robustness of single-gene topologies and their congruence with the MLSA tree were tested. Lateral Gene Transfers (LGT) were few and scattered, suggesting they had no impact on the concatenate topology. The pgk marker - providing the longest sequence, highest mean genetic divergence and least occurrence of LGT - was used to survey an unequalled number of Alnus-infective Frankia - mainly uncultured strains from a broad range of host-species and geographic origins. This marker allowed reliable Single-Locus Strain Typing (SLST) below the species level, revealed an undiscovered taxonomical diversity, and highlighted the effect of cultivation, sporulation phenotype and host plant species on symbiont richness, diversity and phylogeny.

The Biased Evolution of Generation Time.

Many life-history traits are important determinants of the generation time. For instance, semelparous species whose adults reproduce only once have shorter generation times than iteroparous species that reproduce on several occasions, assuming equal development duration. A shorter generation time ensures a higher growth rate in stable environments where resources are in excess and is therefore a positively selected feature in this situation. In a stable and limiting environment, all combinations of traits that produce the same number of viable offspring are selectively equivalent. Here we study the neutral evolution of life-history strategies with different generation times and show that the slowest strategy represents the most likely evolutionary outcome when mutation is considered. Indeed, strategies with longer generation times generate fewer mutants per time unit, which makes them less likely to be replaced within a given time period. This turnover bias favors the evolution of strategies with long generation times. Its real impact, however, depends on both the population size and the nature of selection on life-history strategies. The latter is primarily impacted by the relationships between life-history traits whose estimation will be crucial to understanding the evolution of life-history strategies.

Invasion speeds of Triatoma dimidiata, vector of Chagas disease: An application of orthogonal polynomials method.

Demographic processes and spatial dispersal of Triatoma dimidiata, a triatomine species vector of Chagas disease, are modeled by integrodifference equations to estimate invasion capacity of this species under different ecological conditions. The application of the theory of orthogonal polynomials and the steepest descent method applied to these equations, allow a good approximation of the abundance of the adult female population and the invasion speed. We show that: (1) under the same mean conditions of demography and dispersal, periodic spatial dispersal results in an invasion speed 2.5 times larger than the invasion speed when spatial dispersal is continuous; (2) when the invasion speed of periodic spatial dispersal is correlated to adverse demographic conditions, it is 34.7% higher as compared to a periodic dispersal that is correlated to good demographic conditions. From our results we conclude, in terms of triatomine population control, that the invasive success of T. dimidiata may be most sensitive to the probability of transition from juvenile to adult stage. We discuss our main theoretical predictions in the light of observed data in different triatomines species found in the literature.

Life History Traits and Demographic Parameters of Triatoma infestans (Hemiptera: Reduviidae) Fed on Human Blood.

Triatoma infestans (Klug, 1834) (Hemiptera: Reduviidae), the main vector of Chagas disease in South America, feeds primarily on humans, but ethical reasons preclude carrying out demographical studies using people. Thus, most laboratory studies of T. infestans are conducted using bird or mammal live hosts that may result in different demographic parameters from those obtained on human blood. Therefore, it is of interest to determine whether the use of an artificial feeder with human blood would be operational to rear triatomines and estimate population growth rates. We estimated life history traits and demographic parameters using an artificial feeder with human blood and compared them with those obtained on live hens. Both groups of T. infestans were kept under constant conditions [28 ± 1°C, 40 ± 5% relative humidity, a photoperiod of 12:12 (L:D) h] and fed weekly. On the basis of age-specific survival and age-specific fecundity, we calculated the intrinsic rate of natural increase (r), the finite rate of population growth (λ), the net reproductive rate (Ro), and the mean generation time (Tg). Our results show differences in life history traits between blood sources, resulting in smaller population growth rates on human blood than on live hens. Although demographic growth rate was smaller on human blood than on hens, it still remains positive, so the benefit/cost ratio of this feeding method seems relatively attractive. We discuss possibility of using the artificial feeder with human blood for both ecological and behavioral studies.

In-planta sporulation phenotype: a major life history trait to understand the evolution of Alnus-infective Frankia strains.

Two major types of Frankia strains are usually recognized, based on the ability to sporulate in-planta: spore-positive (Sp+) and spore-negative (Sp-). We carried out a study of Sp+ and Sp- Frankia strains based on nodules collected on Alnus glutinosa, Alnus incana and Alnus viridis. The nodules were phenotyped using improved histology methods, and endophytic Frankia strain genotype was determined using a multilocus sequence analysis approach. An additional sampling was done to assess the relation between Sp+ phenotype frequency and genetic diversity of Frankia strains at the alder stand scale. Our results revealed that (i) Sp+ and Sp- Alnus-infective Frankia strains are genetically different even when sampled from the same alder stand and the same host-plant species; (ii) there are at least two distinct phylogenetic lineages of Sp+ Frankia that cluster according to the host-plant species and without regard of geographic distance and (iii) genetic diversity of Sp+ strains is very low at the alder stand scale compared with Sp- strains. Difference in evolutionary history and genetic diversity between Sp+ and Sp- Frankia allows us to discuss the possible ecological role of in-planta sporulation.

The evolution of bet hedging in response to local ecological conditions.

Genotypes that hedge their bets can be favored by selection in an unpredictably varying environment. Bet hedging can be achieved by systematically expressing several phenotypes, such as one that readily attempts to reproduce and one that procrastinates in a dormant stage. But how much of each phenotype should a genotype express? Theory predicts that evolving bet-hedging strategies depend on local environmental variation, on how the population is regulated, and on exchanges with neighboring populations. Empirically, however, it remains unknown whether bet hedging can evolve to cope with the ecological conditions experienced by populations. Here we study the evolution of bet-hedging dormancy frequencies in two neighboring populations of the chestnut weevil, Curculio elephas. We estimate the temporal distribution of demographic parameters together with the form of the relationship between fecundity and population density and use both to parameterize models that predict the bet-hedging dormancy frequency expected to evolve in each population. Strikingly, the observed dormancy frequencies closely match predictions in their respective localities. We also found that dormancy frequencies vary randomly across generations, likely due to environmental perturbations of the underlying physiological mechanism. Using a model that includes these constraints, we predict the whole distribution of dormancy frequencies whose mean and shape agree with our observed data. Overall, our results suggest that dormancy frequencies have evolved according to local ecological conditions and physiological constraints.

Large-scale patterns in morphological diversity and species assemblages in Neotropical Triatominae (Heteroptera: Reduviidae)

We analysed the spatial variation in morphological diversity (MDiv) and species richness (SR) for 91 species of Neotropical Triatominae to determine the ecological relationships between SR and MDiv and to explore the roles that climate, productivity, environmental heterogeneity and the presence of biomes and rivers may play in the structuring of species assemblages. For each 110 km x 110 km-cell on a grid map of America, we determined the number of species (SR) and estimated the mean Gower index (MDiv) based on 12 morphological attributes. We performed bootstrapping analyses of species assemblages to identify whether those assemblages were more similar or dissimilar in their morphology than expected by chance. We applied a multi-model selection procedure and spatial explicit analyses to account for the association of diversity-environment relationships. MDiv and SR both showed a latitudinal gradient, although each peaked at different locations and were thus not strictly spatially congruent. SR decreased with temperature variability and MDiv increased with mean temperature, suggesting a predominant role for ambient energy in determining Triatominae diversity. Species that were more similar than expected by chance co-occurred near the limits of the Triatominae distribution in association with changes in environmental variables. Environmental filtering may underlie the structuring of species assemblages near their distributional limits.

From income to capital breeding: when diversified strategies sustain species coexistence.

There is empirical evidence of many diversified ways for energy to be acquired and allocated to reproduction, notably with strategies ranging from strict income breeding (females fueling their gametes with energy gained concomitantly during reproduction) to strict capital breeding (females storing nutrients prior reproduction). Until now, the question of whether diversification of these strategies might impact the way communities are organized has not been considered. Here, we suggest that diversified resource allocation strategies among competing species may contribute to their coexistence. We examined this hypothesis by focusing on communities composed of four phytophagous insect species that coexist and compete for egg-laying sites. From wild-caught females, we determined precisely the breeding period of each species and we described their resource acquisition and allocation to reproduction dynamics. We quantified in each species the total amount of larval energy stored by newly-emerging females and then monitored the total energy budget of females caught in the field before and throughout their breeding period. We found that the four sibling weevil species are markedly segregated along the income-capital-breeding continuum, which is correlated with clear time partitioning in their laying activity. Our results suggest that diversified resource allocation strategies might contribute to time partitioning of plant resources exploitation and thus indirectly to their coexistence. This work should further encourage studies examining the extent to which competitive coexistence might be affected by diversification of income-capital breeding strategies together with the intensity of interspecific competition, and considering the divergent evolution of these strategies.

Influence of vectors' risk-spreading strategies and environmental stochasticity on the epidemiology and evolution of vector-borne diseases: the example of Chagas' disease.

Insects are known to display strategies that spread the risk of encountering unfavorable conditions, thereby decreasing the extinction probability of genetic lineages in unpredictable environments. To what extent these strategies influence the epidemiology and evolution of vector-borne diseases in stochastic environments is largely unknown. In triatomines, the vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas' disease, juvenile development time varies between individuals and such variation most likely decreases the extinction risk of vector populations in stochastic environments. We developed a simplified multi-stage vector-borne SI epidemiological model to investigate how vector risk-spreading strategies and environmental stochasticity influence the prevalence and evolution of a parasite. This model is based on available knowledge on triatomine biodemography, but its conceptual outcomes apply, to a certain extent, to other vector-borne diseases. Model comparisons between deterministic and stochastic settings led to the conclusion that environmental stochasticity, vector risk-spreading strategies (in particular an increase in the length and variability of development time) and their interaction have drastic consequences on vector population dynamics, disease prevalence, and the relative short-term evolution of parasite virulence. Our work shows that stochastic environments and associated risk-spreading strategies can increase the prevalence of vector-borne diseases and favor the invasion of more virulent parasite strains on relatively short evolutionary timescales. This study raises new questions and challenges in a context of increasingly unpredictable environmental variations as a result of global climate change and human interventions such as habitat destruction or vector control.

Endosymbiont diversity among sibling weevil species competing for the same resource.

BACKGROUND: Whereas the impact of endosymbionts on the ecology of their hosts is well known in some insect species, the question of whether host communities are influenced by endosymbionts remains largely unanswered. Notably, the coexistence of host species competing with each other, which is expected to be stabilized by their ecological differences, could be facilitated by differences in their endosymbionts. Yet, the composition of endosymbiotic communities housed by natural communities of competing host species is still almost unknown. In this study, we started filling this gap by describing and comparing the bacterial endosymbiotic communities of four sibling weevil species (Curculio spp.) that compete with each other to lay eggs into oak acorns (Quercus spp.) and exhibit marked ecological differences. RESULTS: All four species housed the primary endosymbiont Candidatus Curculioniphilus buchneri, yet each of these had a clearly distinct community of secondary endosymbionts, including Rickettsia, Spiroplasma, and two Wolbachia strains. Notably, three weevil species harbored their own predominant facultative endosymbiont and possessed the remaining symbionts at a residual infection level. CONCLUSIONS: The four competing species clearly harbor distinct endosymbiotic communities. We discuss how such endosymbiotic communities could spread and keep distinct in the four insect species, and how these symbionts might affect the organization and species richness of host communities.

Large-scale patterns in morphological diversity and species assemblages in Neotropical Triatominae (Heteroptera: Reduviidae).

We analysed the spatial variation in morphological diversity (MDiv) and species richness (SR) for 91 species of Neotropical Triatominae to determine the ecological relationships between SR and MDiv and to explore the roles that climate, productivity, environmental heterogeneity and the presence of biomes and rivers may play in the structuring of species assemblages. For each 110 km x 110 km-cell on a grid map of America, we determined the number of species (SR) and estimated the mean Gower index (MDiv) based on 12 morphological attributes. We performed bootstrapping analyses of species assemblages to identify whether those assemblages were more similar or dissimilar in their morphology than expected by chance. We applied a multi-model selection procedure and spatial explicit analyses to account for the association of diversity-environment relationships. MDiv and SR both showed a latitudinal gradient, although each peaked at different locations and were thus not strictly spatially congruent. SR decreased with temperature variability and MDiv increased with mean temperature, suggesting a predominant role for ambient energy in determining Triatominae diversity. Species that were more similar than expected by chance co-occurred near the limits of the Triatominae distribution in association with changes in environmental variables. Environmental filtering may underlie the structuring of species assemblages near their distributional limits.

Emergence and prevalence of human vector-borne diseases in sink vector populations.

Vector-borne diseases represent a major public health concern in most tropical and subtropical areas, and an emerging threat for more developed countries. Our understanding of the ecology, evolution and control of these diseases relies predominantly on theory and data on pathogen transmission in large self-sustaining 'source' populations of vectors representative of highly endemic areas. However, there are numerous places where environmental conditions are less favourable to vector populations, but where immigration allows them to persist. We built an epidemiological model to investigate the dynamics of six major human vector borne-diseases in such non self-sustaining 'sink' vector populations. The model was parameterized through a review of the literature, and we performed extensive sensitivity analysis to look at the emergence and prevalence of the pathogen that could be encountered in these populations. Despite the low vector abundance in typical sink populations, all six human diseases were able to spread in 15-55% of cases after accidental introduction. The rate of spread was much more strongly influenced by vector longevity, immigration and feeding rates, than by transmission and virulence of the pathogen. Prevalence in humans remained lower than 5% for dengue, leishmaniasis and Japanese encephalitis, but substantially higher for diseases with longer duration of infection; malaria and the American and African trypanosomiasis. Vector-related parameters were again the key factors, although their influence was lower than on pathogen emergence. Our results emphasize the need for ecology and evolution to be thought in the context of metapopulations made of a mosaic of sink and source habitats, and to design vector control program not only targeting areas of high vector density, but working at a larger spatial scale.

Coexistence of insect species competing for a pulsed resource: toward a unified theory of biodiversity in fluctuating environments.

BACKGROUND: One major challenge in understanding how biodiversity is organized is finding out whether communities of competing species are shaped exclusively by species-level differences in ecological traits (niche theory), exclusively by random processes (neutral theory of biodiversity), or by both processes simultaneously. Communities of species competing for a pulsed resource are a suitable system for testing these theories: due to marked fluctuations in resource availability, the theories yield very different predictions about the timing of resource use and the synchronization of the population dynamics between the competing species. Accordingly, we explored mechanisms that might promote the local coexistence of phytophagous insects (four sister species of the genus Curculio) competing for oak acorns, a pulsed resource. METHODOLOGY/PRINCIPAL FINDINGS: We analyzed the time partitioning of the exploitation of oak acorns by the four weevil species in two independent communities, and we assessed the level of synchronization in their population dynamics. In accordance with the niche theory, overall these species exhibited marked time partitioning of resource use, both within a given year and between different years owing to different dormancy strategies between species, as well as distinct demographic patterns. Two of the four weevil species, however, consistently exploited the resource during the same period of the year, exhibited a similar dormancy pattern, and did not show any significant difference in their population dynamics. CONCLUSIONS/SIGNIFICANCE: The marked time partitioning of the resource use appears as a keystone of the coexistence of these competing insect species, except for two of them which are demographically nearly equivalent. Communities of consumers of pulsed resources thus seem to offer a promising avenue for developing a unifying theory of biodiversity in fluctuating environments which might predict the co-occurrence, within the same community, of species that are ecologically either very similar, or very different.

Adaptive developmental delay in Chagas disease vectors: an evolutionary ecology approach.

BACKGROUND: The developmental time of vector insects is important in population dynamics, evolutionary biology, epidemiology and in their responses to global climatic change. In the triatomines (Triatominae, Reduviidae), vectors of Chagas disease, evolutionary ecology concepts, which may allow for a better understanding of their biology, have not been applied. Despite delay in the molting in some individuals observed in triatomines, no effort was made to explain this variability. METHODOLOGY: We applied four methods: (1) an e-mail survey sent to 30 researchers with experience in triatomines, (2) a statistical description of the developmental time of eleven triatomine species, (3) a relationship between development time pattern and climatic inter-annual variability, (4) a mathematical optimization model of evolution of developmental delay (diapause). PRINCIPAL FINDINGS: 85.6% of responses informed on prolonged developmental times in 5(th) instar nymphs, with 20 species identified with remarkable developmental delays. The developmental time analysis showed some degree of bi-modal pattern of the development time of the 5(th) instars in nine out of eleven species but no trend between development time pattern and climatic inter-annual variability was observed. Our optimization model predicts that the developmental delays could be due to an adaptive risk-spreading diapause strategy, only if survival throughout the diapause period and the probability of random occurrence of "bad" environmental conditions are sufficiently high. CONCLUSIONS/SIGNIFICANCE: Developmental delay may not be a simple non-adaptive phenotypic plasticity in development time, and could be a form of adaptive diapause associated to a physiological mechanism related to the postponement of the initiation of reproduction, as an adaptation to environmental stochasticity through a spreading of risk (bet-hedging) strategy. We identify a series of parameters that can be measured in the field and laboratory to test this hypothesis. The importance of these findings is discussed in terms of global climatic change and epidemiological consequences.

Adaptive dynamics of dormancy duration variability: evolutionary trade-off and priority effect lead to suboptimal adaptation.

Many plants, insects, and crustaceans show within-population variability in dormancy length. The question of whether such variability corresponds to a genetic polymorphism of pure strategies or a mixed bet-hedging strategy, and how the level of phenotypic variability can evolve remain unknown for most species. Using an eco-genetic model rooted in a 25-year ecological field study of a Chestnut weevil, Curculio elephas, we show that its diapause-duration variability is more likely to have evolved by the spread of a bet-hedging strategy than by the establishment of a genetic polymorphism. Investigating further the adaptive dynamics of diapause-duration variability, we find two unanticipated patterns of general interest. First, there is a trade-off between the ability of bet-hedging strategies to persist on an ecological time scale and their ability to invade. The optimal strategy (in terms of persistence) cannot invade, whereas suboptimal bet-hedgers are good invaders. Second, we describe an original evolutionary dynamics where each bet-hedging strategy (defined by its rate of prolonged diapause) resists invasion by all others, so that the first type of bet-hedger to appear persists on an evolutionary time scale. Such "evolutionary priority effect" could drive the evolution of maladapted levels of diapause-duration variability.

An agent-based model for predicting the prevalence of Trypanosoma cruzi I and II in their host and vector populations.

Trypanosoma cruzi is the causative agent of Chagas disease, an endemic human parasitosis in Latin America. This protozoan is transmitted to human and other mammals by blood-feeding bugs belonging to the Triatominae subfamily. There are two strains (T. cruzi I and T. cruzi II) presenting different biological and ecological characteristics. An original agent-based model (ABM) was designed for predicting the prevalence (i.e., proportion of infected individuals in the total population at a given time) of T. cruzi I and II during single and mixed infections. The ABM was calibrated from experimental data retrieved from literature. It was shown that inclusion of reservoir hosts as supplementary type of agent in the model was necessary for obtaining realistic simulation results of the prevalence of the two strains. This is totally in agreement with experimental and field observations on the importance of reservoirs in the parasite transmission cycle. Proposals were made for refining the model. More generally, the advantages and limitations of the ABM in parasitology modeling have been discussed.

Demographic and dispersal constraints for domestic infestation by non-domicilated chagas disease vectors in the Yucatan Peninsula, Mexico.

Chagas disease is one of the most important diseases in Latin America. Insecticides have been sprayed to control domiciliated vectors. However, some triatomine species are not strictly domiciliated, and the transmission risk posed by immigrants is identified as a major challenge. The design of new control strategies requires disentangling the importance of demography and immigration in vector occurrence inside houses. Using a population dynamics model, we confirmed that dispersal can explain satisfactorily the domestic abundance of Triatoma dimidiata in Yucatan, Mexico. A surprisingly low fecundity was also required (no more than one to two female offspring per female per trimester). A wide range of survival probabilities was possible, although the best fit was obtained for a very low immature survival (< or = 0.01/trimester). Our model predicted that domestic populations are not sustainable, and up to 90% of the individuals found in houses are immigrants. We discuss the potential of different strategies to control the transmission of Chagas disease by non-domiciliated vectors.

Prolonged diapause: a trait increasing invasion speed?

Invasive species are considered to be the second cause of biodiversity erosion, and one challenge is to determine the life history traits that cause an increased invasion capacity. Prolonged diapause is a major trait in evolution and insect population dynamics, but its effects on invasion speed remain unknown. From a recently developed mathematical approach (integro-difference equations) applied to the insect dormancy, we show that despite a dispersal cost, bet-hedging diapause strategies with low (0.1-0.2) prolonged diapause frequency (emergence after 1 or 2 years) can have a higher invasion speed than a simple diapause strategy (emergence after 1 year) when the environmental stochasticity is sufficiently high. In such conditions, prolonged diapause is a trait supporting invasion capacity by increasing population stochastic growth rate. This conclusion, which applies to a large range of demographic parameters, is in opposition to the usual view that prolonged dormancy is an alternative strategy to dispersal. However, prolonged diapause does not support invasion if the level of environmental stochasticity is low. Therefore, conclusion about its influence on invasion ability needs a good knowledge of environmental stochasticity in the introduction area of considered species.