Strong selective pressure by parasitoids mitigates the costs of consuming chemically defended plants

Co-evolutionary interactions between plants and herbivores have led to a range of plant defenses that minimize insect damage and a suite of counter-adaptations that allow herbivores to feed on defended plants. Consumption of plant secondary compounds results in herbivore growth and developmental costs but can be beneficial if eating these secondary compounds results in deterrence or harm to natural enemies.To test the role of secondary compounds on herbivore fitness in the context of natural enemies, I combined field measurements of the prevalence of a parasitoid wasp (Cotesia congregata) with detailed measurements of the costs of plant secondary compounds on growth, immune, and fitness traits across developmental stages in the herbivore Manduca sexta. When M. sexta larvae consume defended plants, Cotesia congregata are known to have reduced success. However, this anti-enemy benefit to the M. sexta host must be considered in relationship to parasitoid abundance and the type and strength of the fitness costs M. sexta incurs feeding on plant secondary compounds.I found that Cotesia congregata parasitoids exert large negative selective pressures, killing 31-57% of M. sexta larvae in the field. Manduca sexta developed fastest during the instars most at risk for parasitoid oviposition but growth was slowed by consumption of plant secondary compounds (nicotine and rutin). These negative size effects at the larval stage carried over to influence adult traits associated with flight and mating but there were no immune, survival, or fecundity costs of consuming plant defensive compounds as larvae.Synthesis. These results suggest that the developmental costs experienced by M. sexta herbivores consuming defensive compounds may be outweighed by a survival benefit in the face of abundant enemy pressures.

Reproductive context of extremely short sperm in the parasitic wasp Cotesia congregata (Hymenoptera: Braconidae)

Among adaptive traits under sexual selection, the length of spermatozoa shows high interspecific variation. In insects, extremes exist for both short and long sperm. The spermatozoa of the endoparasitic wasp Cotesia congregata (Say) are the shortest flagellated sperm described in animals, 6.6 µm in length. By comparison, the sperm of Drosophila bifurca are almost 6000 times longer. Thus, C. congregata has the potential to shed light on the selection pressures that drive variation in sperm length in relation to their production and use. The reproductive organs, sperm counts, controlled oviposition and sex ratios were investigated. The testes showed stratified differentiation stages of spermatogenesis, and sperm counts revealed continuous spermatogenesis in the late pupal stage. The small female spermatheca stored ~1000 sperm, resulting in an extremely high sperm concentration. The number of progeny per brood decreased over time until depletion of eggs. Females produced up to 370 daughters, corresponding to the effective use of 34% of the average sperm stock. Haploid males made up a greater proportion of broods in later parasitisms. Sperm miniaturization may be an adaptation to transfer increased quantities for the entire reproductive life of females in the absence of sperm competition but in the reduced space offered by the spermatheca.

Cotesia congregata Bracovirus Circles Encoding PTP and Ankyrin Genes Integrate into the DNA of Parasitized Manduca sexta Hemocytes

ABSTRACT Polydnaviruses (PDVs) are essential for the parasitism success of tens of thousands of species of parasitoid wasps. PDVs are present in wasp genomes as proviruses, which serve as the template for the production of double-stranded circular viral DNA carrying virulence genes that are injected into lepidopteran hosts. PDV circles do not contain genes coding for particle production, thereby impeding viral replication in caterpillar hosts during parasitism. Here, we investigated the fate of PDV circles of Cotesia congregata bracovirus during parasitism of the tobacco hornworm, Manduca sexta, by the wasp Cotesia congregata. Sequences sharing similarities with host integration motifs (HIMs) of Microplitis demolitor bracovirus (MdBV) circles involved in integration into DNA could be identified in 12 CcBV circles, which encode PTP and VANK gene families involved in host immune disruption. A PCR approach performed on a subset of these circles indicated that they persisted in parasitized M. sexta hemocytes as linear forms, possibly integrated in host DNA. Furthermore, by using a primer extension capture method based on these HIMs and high-throughput sequencing, we could show that 8 out of 9 circles tested were integrated in M. sexta hemocyte genomic DNA and that integration had occurred specifically using the HIM, indicating that an HIM-mediated specific mechanism was involved in their integration. Investigation of BV circle insertion sites at the genome scale revealed that certain genomic regions appeared to be enriched in BV insertions, but no specific M. sexta target site could be identified. IMPORTANCE The identification of a specific and efficient integration mechanism shared by several bracovirus species opens the question of its role in braconid parasitoid wasp parasitism success. Indeed, results obtained here show massive integration of bracovirus DNA in somatic immune cells at each parasitism event of a caterpillar host. Given that bracoviruses do not replicate in infected cells, integration of viral sequences in host DNA might allow the production of PTP and VANK virulence proteins within newly dividing cells of caterpillar hosts that continue to develop during parasitism. Furthermore, this integration process could serve as a basis to understand how PDVs mediate the recently identified gene flux between parasitoid wasps and Lepidoptera and the frequency of these horizontal transfer events in nature.