Frédéric Menu

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.

Coin-flipping plasticity and prolonged diapause in insects: example of the chestnut weevil Curculio elephas (Coleoptera: Curculionidae)

Spreading of emergence over several years due to prolonged diapause in some larvae was shown in the chestnut weevil. Depending on the year the larvae buried themselves in the ground, 32–56% of live adults emerged after 2 or 3 years of underground life. Variability in the duration of diapause was assumed to correspond to tactics of adaptative “coin-flipping” plasticity. This plasticity must allow the chestnut weevil to respond to the unpredictability of its habitat as measured by the irregularity of chestnut production and summer drought. Indeed, fecundity and adult longevity did not lessen after 2 years of underground life. No drastic decrease in the population size of weevils occurs after bad years; for instance when the number of chestnuts on the study tree is less than 10 000, passers-by can collect all the fruit and about 95% of larvae developing in chestnuts are destroyed. Diapause nature (simple or prolonged) may be related to moisture and gas rates in the ground from October to December. These factors acting in autumn are not known to be involved in the physiological mechanisms that control the production of chestnuts.

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

Abstract. 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.

Unexpected male choosiness for mates in a spider

Sexual selection theory traditionally considers choosiness for mates to be negatively related to intra-sexual competition. Males were classically considered to be the competing, but not the choosy, sex. However, evidence of male choosiness is now accumulating. Male choosiness is expected to increase with an individuals competitive ability, and to decrease as intra-sexual competition increases. However, such predictions have never been tested in field conditions. Here, we explore male mate choice in a spider by studying size-assortative pairing in two natural sites that strongly differ in the level of male–male competition. Unexpectedly, our results demonstrate that mate choice shifts from opportunism to high selectivity as competition between males increases. Males experiencing weak competition did not exhibit size-related mating preferences. By contrast, when competition was intense we found strong size-assortative pairing due to male choice: while larger, more competitive males preferentially paired with larger, more fecund females, smaller males chose smaller females. Thus, we show that mating preferences of males vary with their competitive ability. The distinct preferences exhibited by males of different sizes seem to be an adaptive response to the lower reproductive opportunities arising from increased competition between males.

Re-infestation of houses by Triatoma dimidiata after intra-domicile insecticide application in the Yucatán peninsula, Mexico.

In most countries, Chagas disease transmission control remains based on domestic insecticide application. We thus evaluated the efficacy of intra-domicile cyfluthrin spraying for the control of Triatoma dimidiata, the only Chagas disease vector in the Yucatán peninsula, Mexico, and monitored potential re-infestation every 15 days for up to 9 months. We found that there was a re-infestation of houses by adult bugs starting 4 months after insecticide application, possibly from sylvatic/peridomicile areas. This points out the need to take into account the potential dispersal of sylvatic/peridomestic adult bugs into the domiciles as well as continuity action for an effective vector control.

Strategies of emergence in the chestnut weevil Curculio elephas (Coleoptera: Curculionidae)

In the chestnut weevil Curculio elephas, adult emergences spread over 3 or 4 years due to prolonged larval diapause in some individuals. Weevils with an extended diapause emerge, on the average, 1–10 days before those with simple diapause, but whatever the age of insects, emergences occur always from mid-August to early October. When the summer is dry, some adults cannot emerge because of the hardness of the soil. Emergence sucess of adults is smaller in females than in males. The result is that the sex ratio is female-biased before emergence and male-biased after. Summer drought cannot be predicted by the chestnut weevil, and when the soil is dry 27–78% of females cannot emerge and do not reproduce. The year after a summer drought, many reproducing females may emerge from larvae with prolonged diapause. These results suggest an evolutionary influence on the variability in diapause duration. Computer simulations and observations do not support the hypothesis that the main cause of variation in diapause length is the existence of several distinct genotypes within populations. On the contrary, our data strengthen the hypothesis for coin-flipping plasticity discussed in a previous paper.

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.

A handbook for uncovering the complete energetic budget in insects: the van Handel's method (1985) revisited

Insects comprise relevant biological models for investigating nutrient acquisition and allocation processes in the context of life‐history ecology and evolution. However, empirical investigations are still partly limited by the lack of availability of simple methods for simultaneously estimating the four major energetic components (i.e. lipids, free sugars, glycogen and proteins) in the same individual. In the present work, we validate a fast, reproducible and cheap method for overcoming this problem that uses different solvents successively. First, proteins are solubilized in a phosphate‐lysis buffer and then quantified according to the classical Bradford assay procedure. In a second step, a chloroform–methanol mixture is added to the aqueous phase, which allows assay of the total lipid fraction, as well as the free sugars and glycogen in the same insect homogenate. In addition, a micro‐separation procedure is adapted to partition the total lipids into neutral (mainly stored lipids) and polar (mainly structural lipids) components. Although these assays are conducted sequentially in the same individual, the sensitivity of our method remains high: the estimated amount of each energetic compartment does not differ from that obtained with former, partial methods. Our method should thus largely improve our knowledge about nutrient acquisition and allocation among insects not only in laboratory‐reared individuals, but also in animals caught in the wild. Descriptions and recommendations are given at each step of the protocol to adapt the procedure to various insect species. Finally, to prevent misinterpretation of data generated in accordance with this protocol, the limits of our method are discussed in the light of life‐history studies.

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.

Clutch size manipulations in the chestnut weevil, Curculio elephas: fitness of oviposition strategies

Abstract We test the adaptive value of clutch size observed in a natural population of the chestnut weevil Curculio elephas. Clutch size is defined as the number of immatures per infested chestnut. In natural conditions, clutch size averages 1.7 eggs. By manipulating clutch size in the field, we demonstrate that deviations from the theoretical ”Lack clutch size”, estimated as eight immatures, are mainly due to proximate and delayed effects of clutch size on offspring performance. We show the existence of a trade-off between clutch size and larval weight. The latter, a key life-history trait, is highly correlated with fitness because it is a strong determinant of larval survival and potential fecundity of offspring females. The fitness of different potential oviposition strategies characterized by their clutch sizes, ranging from one to nine immatures, was calculated from field- estimated parameters. Chestnut weevil females obtain an evolutionary advantage by laying their eggs singly, since, for instance, fitness of single-egg clutches exceeds fitness of two-egg clutches and four-egg clutches by 8.0% and 15.1% respectively.