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

Abstract

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.

Western European Populations of the Ichneumonid Wasp Hyposoter didymator Belong to a Single Taxon

“…The role of polydnaviruses in parasitoid local adaptation has previously been reported for the braconid Cotesia sesamiae. Although C. sesamiae was initially considered as a generalist species developing on several lepidopteran hosts, two taxa of C. sesamiae were identified in Kenya that vary in their capacity to overcome the resistance of the lepidopteran host, a feature that was linked to allelic variations in viral genes (Branca et al, 2011;Kaiser et al, 2017;Gauthier et al, 2018). Although not differentiated in several genetically differentiated taxa, H. didymator probably does not parasitize all noctuid species indifferently and part of this specialization might be due, like C. sesamiae, to polydnaviruses, explaining a higher level of genetic differentiation at Hdiv loci.…”

The Parasitic Wasp, Cotesia congregata (Say), Consists of Two Incipient Species Isolated by Asymmetric Reproductive Incompatibility and Hybrid Inability to Overcome Host Defenses

“…The role of BVs in reproductive isolation and hostadaptation has been extensively studied in Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae), an important parasitoid and biocontrol agent of noctuid stemborers in Africa (Kaiser et al, 2017). Cotesia sesamiae has at least two allopatric biotypes that differ in host usage and are not reproductively compatible.…”

Genetic footprints of adaptive divergence in the bracovirus of Cotesia sesamiae identified by targeted resequencing

“…The adaptive role of the bracovirus was revealed with the study of two Kenyan populations of C. sesamiae (reviewed in Kaiser, Dupas, et al., ). Both populations vary in their capacity or failure to overcome the resistance of the host, Busseola fusca .…”

“…When the larvae have completed their development, they egress to the outside of the host, where they spin their cocoons, from which metamorphosed adults emerge. During their short life, C. sesamiae produces one to two gregarious broods (Kaiser, Dupas, et al, 2017), which contain both males and females. Synchronized emergence of ready to mate wasps inside the stem tunnel implies that females generally first mate with siblings (Arakaki & Ganaha, 1986;Ullyett, 1935), which may cause inbreeding as observed in another gregarious Cotesia species (Elias, Dorn, & Mazzi, 2010).…”

“…Microsatellite genotyping of over 600 wasps revealed that C. sesamiae exhibits a genetic structure comprising five major populations , which vary in their host range (Branca et al, 2011) and in parasitic success on different hosts (Gitau, Gundersen-Rindal, Pedroni, Mbugi, & Dupas, 2007;Mochiah, Ngi-Song, Overholt, & Botchey, 2002). These five C. sesamiae populations include one population recently described as a new species, C. typhae (Kaiser et al, 2015;Kaiser, Dupas, et al, 2017). All field samples from this lineage (N = 46 in Branca et al, 2017 andN = 35 in Kaiser et al, 2015) were strictly associated with larvae of the host Sesamia nonagrioides (Noctuidae), feeding mainly on the host plant Typha domingensis (Poales, Typhaceae).…”