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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Assessment of Triatoma dimidiata dispersal in the Yucatan Peninsula of Mexico by morphometry and microsatellite markers.

In the Yucatán Peninsula of Mexico, the main vector of Chagas disease is Triatoma dimidiata. Field studies suggest that natural transmission occurs through transient and seasonal invasion of houses by sylvatic/peridomestic triatomines, rather than through persistent domiciliated bug populations. We investigated the genetic structure of T. dimidiata populations, using morphometry and microsatellite markers, to assess dispersal of individuals in this triatomine species and to understand the dynamics of domestic infestation. We observed low phenotypic and genetic differentiation among populations from different villages, with an FST of only 0.0553, which suggested a weak but significant population structure at this level. Similarly low but significant differences were observed among populations from the same village but different biotopes (sylvatic, peridomestic, and domestic), with FST values ranging from 0.0096 to 0.0455. These data suggested elevated dispersal of bugs between biotopes (Nm = 5-25), which was confirmed by likelihood and Bayesian assignment tests. A proportion of bugs collected within domiciles were significantly assigned to peridomestic and sylvatic areas. This study showed that T. dimidiata has important dispersal capabilities that can explain the seasonal pattern of domicile infestation by peridomestic and sylvatic bugs. Therefore, dispersal should be taken into account in the design of effective vector control strategies.

Bet-Hedging Diapause Strategies in Stochastic Environments.

In many insect species, adult emergence spreads over several years because of the existence of prolonged diapause in certain individuals. From stochastic models, we show that diversified bet-hedging strategies (mixed strategies with emergence after 1 or 2 yr) are more fit than simple diapause strategy (emergence after 1 yr) or fixed prolonged diapause strategy (emergence after 2 yr) in isolated chestnut weevil populations. This conclusion applies to a large range of survival rates in prolonged diapause and is insensitive to initial conditions, magnitude of temporal autocorrelation, distribution of demographic parameters, and quoted values of population size limitation. However, the shape of the fitness distribution as a function of prolonged diapause frequency changes greatly in the absence of population size limitation. Whatever the survival rate during prolonged diapause, we find that there is no genotypic advantage to extending diapause for all chestnut weevil larvae to more than 1 yr. Our models predict selection of bet-hedging strategies over a large range of prolonged diapause frequencies. This result is consistent with the existence of several mixed strategies in a population. Emergences after 3 yr are not crucial for selection or for the dynamics of mixed strategies in the chestnut weevil.

Dynamics of production of sexual forms in aphids: theoretical and experimental evidence for adaptive "coin-flipping" plasticity.

The best strategy for an organism to deal with unpredictable environmental conditions is a stochastic one, but it is not easy to distinguish it from nonadaptive randomness in phenotype production, and its convincing demonstrations are lacking. Here we describe a new method for detection of adaptive stochastic polyphenism and apply it to the following problem. In fall, each female of the bird cherry-oat aphid, Rhopalosiphum padi, faces a decision either to produce sexuals, which mate and lay cold-tolerant eggs, or to continue production of cold-sensitive parthenogenetic females, which potentially yields a higher population growth rate but is risky because a cold winter can kill all of her descendants. Using a simulation model, we show that global investment in sexual reproduction should be proportional to winter severity and that variance in the peak date of production of sexual individuals should depend on climate predictability. Both predictions are validated against standardized trap data on aphid flight accompanied by meteorological data, and the predictions support adaptive phenotypic plasticity.

Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruzi in the Yucatan peninsula of Mexico.

Chagas disease represents a major public health concern in most of Latin America, and its control is currently based on vector control and blood bank screening. We investigated the geographic distribution and seasonal variations in triatomine populations in the Yucatan peninsula of Mexico to obtain entomologic data for the optimization of potential control programs. We collected domiciliated and peri-domiciliated Triatoma dimidiata from 115 houses in 23 villages distributed throughout most of the peninsula. A high abundance of bugs was observed in the northern part of the peninsula, indicating a prioritary area for vector control. Part of this distribution could be attributed to the type of vegetation. We also documented strong seasonal variations in T. dimidiata populations, with a higher abundance during the hot and dry season in April-June. These variations, associated with reduced year-round colonization of houses and the analysis of developmental stage structure, suggest that flying adults seasonally invading houses may play a larger role than domiciliated bugs in transmission of Trypanosoma cruzi to humans. The importance of this transmission dynamics may not be limited to the Yucatan peninsula, but may be a general mechanism contributing to natural transmission that should be taken into account in other regions for the design and optimization of control strategies.

Bet-hedging for variability in life cycle duration: bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause.

Diversified bet-hedging for life cycle duration is defined as within-generation variability in cycle length expressed by a single genotype maximising mean geometric fitness. Such plasticity is not predictive, i.e. it is not a response to cues from the environment that has a predictive value for the decision at hand. In evolutionary terms, diversified bet-hedging is perceived as an adaptation to environmental stochasticity. However, clear evidence of bet-hedging is scarce and exists only for a few desert plant species and one desert bee. In temperate insects, diversified bet-hedging for life cycle duration has been suspected in the chestnut weevil, but proximate factors responsible for individual variation are still unknown. From field experiments, we show that the frequency of the long cycle depends on larval weight and on the date when a larva abandons the fruit, but not on larval burying depth in the soil. Since the two first factors are known to depend on food and temperature and cannot lead to predictive plasticity, we give evidence of bet hedging in this temperate species. Indeed, despite a cost associated with prolonged diapause (extra mortality and loss of reproductive opportunity), a previous study showed that plasticity for life cycle duration, such as discussed in this paper, maximises mean geometric fitness and persistence probability in the chestnut weevil. We propose the hypothesis that the variation in life cycle duration depends on individual variability of metabolic resources such as lipids.

Effect of temperature and photoperiod on diapause development in a Douglas fir seed chalcid, Megastigmus spermotrophus.

Douglas fir seeds infested by diapausing larvae of a chalcid, Megastigmus spermotrophus, were transferred under different temperature and photoperiod regimes at various dates during autumn and winter. Both winter diapause and prolonged diapause were compared to the diapause patterns observed in control lots kept under natural conditions. The results showed that exposure to low temperatures in autumn and winter is required for the completion of diapause development. Median adult emergence dates and the date of transfer of larvae to 20°C were negatively correlated. The frequency of prolonged diapause of larvae transferred to 20°C decreased significantly after November. When larvae were submitted to different constant temperatures, the longer the daylength, the higher and faster the reactivation. These results suggest that chalcid larvae can perceive daylength through the seed coat. This phenomenon is probably related to the fact that most of the infested seeds falling in autumn are usually covered by a layer of leaf litter during the winter.

Oviposition pattern of phytophagous insects: on the importance of host population heterogeneity.

Frequency distributions of insect immatures per host are often fitted to contagious distributions, such as the negative binomial, to deduce oviposition pattern. However, different mechanisms can be involved for each theoretical distribution and additional biological information is needed to correctly interpret the fits. We chose the chestnut weevil Curculio elephas, a pest of the European chestnut Castanea sativa, as a model to illustrate the difficulties of inferring oviposition pattern from fits to theoretical distributions and from the variance/mean ratio. From field studies over 13-16 years, we show that 20 out of the 31 yearly distributions available fit a negative binomial and 25 a zero-inflated Poisson (ZIP). No distribution fits a Poisson distribution. The ZIP distribution assumes heterogeneity within the fruit population. There are two categories of host: the first comprises chestnuts unsuitable for weevil oviposition or in excess relative to the number of weevil females, and the second comprises suitable fruits in which oviposition behavior is random. Our results confirm this host heterogeneity. According to the ZIP distribution, the first category of hosts includes on average 74% of the chestnuts. A negative binomial distribution may be generated by either true or false contagion. We show that neither interference between weevil females, nor spatial variation in the infestation rate exist. Consequently, the observed distributions of immatures are not the result of false contagion. Nevertheless, we cannot totally exlude true contagion of immatures. In this paper we discuss the difficulty of testing true contagion in natural conditions. These results show that we cannot systematically conclude in favour of contagion when fitting a distribution such as the negative binomial or when a variance/mean ratio is higher than unity.