Role of egg-laying behavior, virulence and local adaptation in a parasitoid's chances of reproducing in a new host.

Understanding the ability of parasitoid insects to succeed in new host populations is a relevant question for biological control and adaptive mechanisms. Cotesia typhae is an African parasitoid specialized on the moth Sesamiae nonagrioides, also called the Mediterranean corn borer. Two Kenyan strains of C. typhae differ in their virulence against a new host population from France. We explored behavioral and physiological hypotheses about this differentiation. Cotesia genus belongs to a group of Hymenoptera in which females inject a domesticated virus in their host to overcome its resistance. Since viral particles are injected along with eggs and since the strain with the higher virulence injects more eggs, we hypothesized that virulence could be explained by the quantity of virus injected. To test this assumption, we measured the injected quantities of eggs and viral particles (estimated by viral DNA segments) of each parasitoid strain along several ovipositions, to vary these quantities. Unexpectedly, results showed that virulence against the French host was not correlated to the injected quantities of eggs or viral segments, indicating that virulence differentiation is explained by other causes. The virulence against the respective natural hosts of the two C. typhae strains was also measured, and results suggest that local adaptation to a more resistant natural host may explain the pre-adaptation of one strain to the new host population. We also identified a differentiation of oviposition strategy and subsequent offspring number between the parasitoid strains, which is important in a biocontrol perspective.

Relationship between oviposition, virulence gene expression and parasitism success in Cotesia typhae nov. sp. parasitoid strains.

Studying mechanisms that drive host adaptation in parasitoids is crucial for the efficient use of parasitoids in biocontrol programs. Cotesia typhae nov. sp. (Fernández-Triana) (Hymenoptera: Braconidae) is a newly described parasitoid of the Mediterranean corn borer Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae). Braconidae are known for their domesticated bracovirus, which is injected with eggs in the host larva to overcome its resistance. In this context, we compared reproductive success traits of four Kenyan strains of C. typhae on a French and a Kenyan populations of its host. Differences were found between the four strains and the two most contrasted ones were studied more thoroughly on the French host population. Parasitoid offspring size was correlated with parasitism success and the expression of bracovirus virulence genes (CrV1 and Cystatin) in the host larva after parasitism. Hybrids between these two parasitoid strains showed phenotype and gene expression profiles similar to the most successful parental strain, suggesting the involvement of dominant alleles in the reproductive traits. Ovary dissections revealed that the most successful strain injected more eggs in a single host larva than the less successful one, despite an equal initial ovocyte number in ovaries. It can be expected that the amount of viral particles increase with the number of eggs injected. The ability to bypass the resistance of the allopatric host may in consequence be related to the oviposition behaviour (eggs allocation). The influence of the number of injected eggs on parasitism success and on virulence gene expression was evaluated by oviposition interruption experiments.

The Cotesia sesamiae story: insight into host-range evolution in a Hymenoptera parasitoid and implication for its use in biological control programs.

This review covers nearly 20 years of studies on the ecology, physiology and genetics of the Hymenoptera Cotesia sesamiae, an African parasitoid of Lepidoptera that reduces populations of common maize borers in East and South Africa. The first part of the review presents studies based on sampling of C. sesamiae from maize crops in Kenya. From this agrosystem including one host plant and three main host borer species, studies revealed two genetically differentiated populations of C. sesamiae species adapted to their local host community, and showed that their differentiation involved the joint evolution of virulence genes and sensory mechanisms of host acceptance, reinforced by reproductive incompatibility due to Wolbachia infection status and natural inbreeding. In the second part, we consider the larger ecosystem of wild Poales plant species hosting many Lepidoptera stem borer species that are potential hosts for C. sesamiae. The hypothesis of other host-adapted C. sesamiae populations was investigated based on a large sampling of stem borer larvae on various Poales across sub-Saharan Africa. The sampling provided information on the respective contribution of local hosts, biogeography and Wolbachia in the genetic structure of C. sesamiae populations. Molecular evolution analyses highlighted that several bracovirus genes were under positive selection, some of them being under different selection pressure in C. sesamiae populations adapted to different hosts. This suggests that C. sesamiae host races result from co-evolution acting at the local scale on different bracovirus genes. The third part considers the mechanisms driving specialization. C. sesamiae host races are more or less host-specialized. This character is crucial for efficient and environmentally-safe use of natural enemies for biological control of pests. One method to get an insight in the evolutionary stability of host-parasite associations is to characterize the phylogenetic relationships between the so-called host-races. Based on the construction of a phylogeny of C. sesamiae samples from various host- and plant species, we revealed three main lineages. Mechanisms of differentiation are discussed with regard to the geography and ecology of the samples. One of the lineage presented all the hallmarks of a distinct species, which has been morphologically described and is now studied in the perspective of being used as biological control agent against Sesamia nonagrioides Lefèbvre (Lepidoptera: Noctuidae), a major maize pest in West Africa and Mediterranean countries (see Benoist et al. 2017). The fourth part reviews past and present use of C. sesamiae in biological control, and points out the interest of such molecular ecology studies to reconcile biodiversity and food security stakes in future biological control.

Influence of plant silicon in Busseola fusca (Lepidoptera: Noctuidae) larvae - Poaceae interactions.

The noctuid stem borer Busseola fusca is an important pest of maize and sorghum in Sub-Saharan Africa. The presence of this species occurred mostly on cultivated than on wild habitats. Busseola fusca is oligophagous having a narrow range of a wild grass species. This might be due, in part, to differences in silicon (Si) content in plant tissues between cultivated and wild grasses. In the present study, we have tested this hypothesis by studying the survival and the relative growth rate (RGR) expressed as daily weight gains of B. fusca larvae on maize and six wild host plants, mostly present in the natural habitat where B. fusca occurred, and correlated with their Si contents. Survival and RGR of B. fusca larvae were considerably higher on maize and wild sorghum than on the other grass species, and they were negatively related to plant Si content. This was corroborated with results on RGR from artificial diets amended with increasing levels of Si. In addition, if Si was added to maize growing substrate B. fusca larval growth was significantly reduced confirming the involvement of Si in B. fusca larvae - Poaceae interactions. The results provide insight into the possible mechanisms of oligophagy of B. fusca and provide a correlative support for a physical role of plant endogenous Si in impeding feeding of B. fusca larvae.

Phylogeography in continuous space: coupling species distribution models and circuit theory to assess the effect of contiguous migration at different climatic periods on genetic differentiation in Busseola fusca (Lepidoptera: Noctuidae).

Current population genetic models fail to cope with genetic differentiation for species with large, contiguous and heterogeneous distribution. We show that in such a case, genetic differentiation can be predicted at equilibrium by circuit theory, where conductance corresponds to abundance in species distribution models (SDMs). Circuit-SDM approach was used for the phylogeographic study of the lepidopteran cereal stemborer Busseola fuscaFüller (Noctuidae) across sub-Saharan Africa. Species abundance was surveyed across its distribution range. SDMs were optimized and selected by cross-validation. Relationship between observed matrices of genetic differentiation between individuals, and between matrices of resistance distance was assessed through Mantel tests and redundancy discriminant analyses (RDAs). A total of 628 individuals from 130 localities in 17 countries were genotyped at seven microsatellite loci. Six population clusters were found based on a Bayesian analysis. The eastern margin of Dahomey gap between East and West Africa was the main factor of genetic differentiation. The SDM projections at present, last interglacial and last glacial maximum periods were used for the estimation of circuit resistance between locations of genotyped individuals. For all periods of time, when using either all individuals or only East African individuals, partial Mantel r and RDA conditioning on geographic distance were found significant. Under future projections (year 2080), partial r and RDA significance were different. From this study, it is concluded that analytical solutions provided by circuit theory are useful for the evolutionary management of populations and for phylogeographic analysis when coalescence times are not accessible by approximate Bayesian simulations.

Two sugar isomers influence host plant acceptance by a cereal caterpillar pest.

Plant sugars are often considered as primary feeding stimuli, conditioning host plant acceptance by herbivorous insects. Of the nine sugars identified from methanolic extracts of seven grass species, only turanose, a sucrose isomer, was negatively correlated with the survival and growth of the noctuid larva of cereal stemborer, Busseola fusca. Sucrose was the most abundant sugar, although it did not vary significantly in concentration among the plant species studied. Using Styrofoam™ cylinders impregnated with increasing concentrations of turanose or sucrose, the two sugars had opposing effects: turanose appeared phagodeterrent while sucrose was phagostimulatory. Electrophysiological studies indicated that B. fusca larvae were able to detect both sugars via their styloconic sensilla located on the mouthparts. The findings indicate that, whereas sucrose is a feeding stimulant and positively influences food choice by B. fusca larvae, turanose negatively contributes to larval food choice. The balance in concentrations of both sugars, however, somehow influences the overall host plant choice made by the larvae. This can partly explain host plant suitability and choice by this caterpillar pest in the field.

Variability in pheromone communication among different haplotype populations of Busseola fusca.

The relationship between pheromone composition and mitochondrial haplotype clades was investigated by coupling DNA analyses with pheromone identification and male mate searching behavior among different geographic populations of Busseola fusca. The within-population variations in pheromone blend were as great as those observed between geographic populations, suggesting that the female sex pheromone blend was not the basis of reproductive isolation between the geographic clades. Furthermore, while data from wind tunnel experiments demonstrated that most of the tested males were sensitive to small variations in pheromone mixture, there was considerable within-population variability in the observed response. The study identified a new pheromone component, (Z)-11-hexadecen-1-yl acetate, which when added to the currently used three-component synthetic blend resulted in significantly higher traps catches. The new recommended blend for monitoring flight phenology and for timing control measures for optimal efficacy of B. fusca is (Z)-11-tetradecen-1-yl acetate (62%), (E)-11-tetradecen-1-yl acetate (15%), (Z)-9-tetradecen-1-yl acetate (13%), and (Z)-11-hexadecen-1-yl acetate (10%).

Phylogeography and population genetics of the maize stalk borer Busseola fusca (Lepidoptera, Noctuidae) in sub-Saharan Africa.

The population genetics and phylogeography of African phytophagous insects have received little attention. Some, such as the maize stalk borer Busseola fusca, display significant geographic differences in ecological preferences that may be congruent with patterns of molecular variation. To test this, we collected 307 individuals of this species from maize and cultivated sorghum at 52 localities in West, Central and East Africa during the growing season. For all collected individuals, we sequenced a fragment of the mitochondrial cytochrome b. We tested hypotheses concerning the history and demographic structure of this species. Phylogenetic analyses and nested clade phylogeographic analyses (NCPA) separated the populations into three mitochondrial clades, one from West Africa, and two--Kenya I and Kenya II--from East and Central Africa. The similar nucleotide divergence between clades and nucleotide diversity within clades suggest that they became isolated at about the same time in three different refuges in sub-Saharan Africa and have similar demographic histories. The results of mismatch distribution analyses were consistent with the demographic expansion of these clades. Analysis of molecular variance (amova) indicated a high level of geographic differentiation at different hierarchical levels. NCPA suggested that the observed distribution of haplotypes at several hierarchical levels within the three major clades is best accounted for by restricted gene flow with isolation by distance. The domestication of sorghum and the introduction of maize in Africa had no visible effect on the geographic patterns observed in the B. fusca mitochondrial genome.

Diversity of lepidopteran stem borers on monocotyledonous plants in eastern Africa and the islands of Madagascar and Zanzibar revisited.

Surveys were completed in Eritrea, Ethiopia, Kenya, Madagascar, Mozambique, Tanzania, Uganda and Zanzibar to assess the lepidopteran stem borer species diversity on wild host plants. A total of 24,674 larvae belonging to 135 species were collected from 75 species of wild host plants belonging to the Poaceae, Cyperaceae and Typhaceae. Amongst them were 44 noctuid species belonging to at least nine genera, 33 crambids, 15 pyralids, 16 Pyraloidea species not yet identified, 25 tortricids and three cossids. The noctuid larvae represented 73.6% of the total number of larvae collected, with 66.3, 3.5 and 3.8% found on Poaceae, Cyperaceae and Typhaceae, respectively. The Crambidae, Pyralidae, Tortricidae and Cossidae represented 19.8, 1.9, 2.5 and 0.1% of the total larvae collected, respectively, with 90.4% of the Crambidae and Pyralidae collected from Poaceae, and 99.7% of the Tortricidae collected from Cyperaceae. The lepidopteran stem borer species diversity in the wild host plants was far more diverse than previously reported.

Wild manihot species do not possess C4 photosynthesis.

Cultivated cassava (Manihot esculenta) has a higher rate of photosynthesis than is usual for C3 plants and photosynthesis is not light saturated. For these reasons it has been suggested that cultivated cassava could be derived from wild species possessing C4 photosynthesis. The natural abundance of 13C and activities of phosphoenolpyruvate carboxylase and phosphoglycolate phosphatase were measured in leaves of 20 wild cassava species to test this hypothesis. All the species studied, including M. flabellifolia the potential wild progenitor of cultivated cassava, clearly exhibited C3 not C4 characteristics.

Identification and synthesis of a kairomone mediating host location by two parasitoid species of the cassava mealybug Phenacoccus herreni.

Two encyrtid species, Acerophagus coccois and Aenasius vexans, parasitoids of the cassava mealybug Phenacoccus herreni use a contact kairomone from the body surface of their host as a host-location stimulant. The kairomone was synthesized and identified as O-caffeoylserine based on a combination of chromatographic methods. The synthetic compound was determined to be active.