Ongoing ecological speciation in Cotesia sesamiae, a biological control agent of cereal stem borers

Abstract

To develop efficient and safe biological control, we need to reliably identify natural enemy species, determine their host range, and understand the mechanisms that drive host range evolution. We investigated these points in Cotesia sesamiae, an African parasitic wasp of cereal stem borers. Phylogenetic analyses of 74 individual wasps, based on six mitochondrial and nuclear genes, revealed three lineages. We then investigated the ecological status (host plant and host insect ranges in the field, and host insect suitability tests) and the biological status (cross-mating tests) of the three lineages. We found that one highly supported lineage showed all the hallmarks of a cryptic species. It is associated with one host insect, Sesamia nonagrioides, and is reproductively isolated from the other two lineages by pre- and postmating barriers. The other two lineages had a more variable phylogenetic support, depending on the set of genes; they exhibited an overlapping and diversified range of host species and are not reproductively isolated from one another. We discuss the ecological conditions and mechanisms that likely generated this ongoing speciation and the relevance of this new specialist taxon in the genus Cotesia for biological control.

Keywords: Africa; Hymenoptera; adaptation; cryptic species; ecological niche; evolution; geographic distribution; host range; parasitic wasp; phylogeny; reproductive isolation; virulence.

Figure 1

Phylogeny of Cotesia sesamiae individuals and relatives based on concatenated mtDNA of 3 genes (CO1, 16S, and NADH) and nDNA of a nonviral (LWRH) and two viral genes (EP2 and histone) in relation to host insect and host plant species matrix. See Materials and methods for substitution model selection with PartitionFinder and phylogenetic tree inference in Mr Bayes. Posterior probabilities are given at nodes. All samples have a reference code corresponding to the data bank of the Laboratoire Evolution, Génomes, Comportement et Ecologie. Insect family: Cr, Crambidae; No, Noctuidae. Plant family: Po, Poaceae; Ty, Typhaceae; Cy, Cyperaceae.

Figure 2

Geographical distribution of C. sesamiae samples in sub-Saharan East Africa. Lineages 1, 2, and 3 are lineages defined by the phylogenetic analysis (Fig. 1).

Figure 3

Relative abundance of stem borer–plant associations present in the sites where C. sesamiae samples were found. Sites hosting C. sesamiae from the same lineage were pooled for the analysis. Arrows indicate on which association C. sesamiae samples were found, and colors correspond to the lineage.