A core tenant in the field of ecological immunology is that immune responses trade off with other physiological functions due to resource allocation costs. Caterpillars, for example, tend to exhibit reduced immune responses when reared on more toxic food plants due to a cost from detoxifying or sequestering secondary metabolites, also known as the ‘vulnerable host hypothesis’. However, support for this hypothesis is mixed, and studies have not yet mechanistically isolated the relative contributions of total plant defences, specific metabolites or macro‐nutritional quality. We used the tobacco hornworm Manduca sexta, a specialist herbivore on plants in the nightshade family (Solanaceae), to investigate trade‐offs in immune response. This system is ideal given the availability of solanaceous plant lines varying in general (i.e. jasmonate‐induced) and specific (i.e. nicotine) resistance traits. We also applied a geometric diet stoichiometry approach to examine how phytochemical toxicity and nutritional quality interactively impact insect immunity and performance. We predicted that as plant toxicity increased, immune activity and herbivore performance would decrease. Increasing food plant toxicity reduced insect growth and development, as predicted, but contrary to our hypothesis, plant toxicity did not trade off with immune parameters. Surprisingly, specific plant chemicals, in this case nicotine, appeared immunotherapeutic, stimulating the phenoloxidase (PO) immune response of M. sexta. Available nutrients in artificial diets, mainly protein, also strongly impacted insect growth, but did not affect PO activity, while diets supplemented with nicotine enhanced the PO and melanization response. This work highlights how specific secondary metabolites, and not overall plant toxicity, impact the immune response. Importantly, our data also suggest an alternative mechanism (i.e. immune enhancement) for reduced parasitoid performance when reared from hosts on toxic plants via tritrophic interactions. A free Plain Language Summary can be found within the Supporting Information of this article.
Traditional breeding techniques, applied incrementally over thousands of years, have yielded huge benefits in the characteristics of agricultural animals. This is a result of significant, measurable changes to the genomes of those animal species and breeds. Genome editing techniques may now be applied to achieve targeted DNA sequence alterations, with the potential to affect traits of interest to production of agricultural animals in just one generation. New opportunities arise to improve characteristics difficult to achieve or not amenable to traditional breeding, including disease resistance, and traits that can improve animal welfare, reduce environmental impact, or mitigate impacts of climate change. Countries and supranational institutions are in the process of defining regulatory approaches for genome edited animals and can benefit from sharing approaches and experiences to institute progressive policies in which regulatory oversight is scaled to the particular level of risk involved. To facilitate information sharing and discussion on animal biotechnology, an international community of researchers, developers, breeders, regulators, and communicators recently held a series of seven virtual workshop sessions on applications of biotechnology for animal agriculture, food and environmental safety assessment, regulatory approaches, and market and consumer acceptance. In this report, we summarize the topics presented in the workshop sessions, as well as discussions coming out of the breakout sessions. This is framed within the context of past and recent scientific and regulatory developments. This is a pivotal moment for determination of regulatory approaches and establishment of trust across the innovation through-chain, from researchers, developers, regulators, breeders, farmers through to consumers.
BackgroundMale parasitic wasps attract females with a courtship song produced by rapid wing fanning. Songs have been described for several parasitic wasp species; however, beyond association with wing fanning, the mechanism of sound generation has not been examined. We characterized the male courtship song of Cotesia congregata (Hymenoptera: Braconidae) and investigated the biomechanics of sound production.Methods and Principal FindingsCourtship songs were recorded using high-speed videography (2,000 fps) and audio recordings. The song consists of a long duration amplitude-modulated “buzz” followed by a series of pulsatile higher amplitude “boings,” each decaying into a terminal buzz followed by a short inter-boing pause while wings are stationary. Boings have higher amplitude and lower frequency than buzz components. The lower frequency of the boing sound is due to greater wing displacement. The power spectrum is a harmonic series dominated by wing repetition rate ∼220 Hz, but the sound waveform indicates a higher frequency resonance ∼5 kHz. Sound is not generated by the wings contacting each other, the substrate, or the abdomen. The abdomen is elevated during the first several wing cycles of the boing, but its position is unrelated to sound amplitude. Unlike most sounds generated by volume velocity, the boing is generated at the termination of the wing down stroke when displacement is maximal and wing velocity is zero. Calculation indicates a low Reynolds number of ∼1000.Conclusions and SignificanceAcoustic pressure is proportional to velocity for typical sound sources. Our finding that the boing sound was generated at maximal wing displacement coincident with cessation of wing motion indicates that it is caused by acceleration of the wing tips, consistent with a dipole source. The low Reynolds number requires a high wing flap rate for flight and predisposes wings of small insects for sound production.
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.
Parasitic wasps are highly diverse and play a major role in suppression of herbivorous insect pest populations. Several previously identified species of parasitic wasps have been found to be complexes of cryptic species resulting from adaptations to specific hosts or host foodplants. Cotesia congregata (Say) (Hymenoptera: Braconidae), which has long served as a model system for host-parasitoid interactions, can be used for investigating the process of diversification among sympatric populations that differ in host and host foodplant usage. Two incipient species of C. congregata have been identified in the USA mid-Atlantic region, "MsT wasps" originate from Manduca sexta (L.) (Lepidoptera: Sphingidae) on tobacco and "CcC wasps" originate from Ceratomia catalpae (Boisduval) (Lepidoptera: Sphingidae) on catalpa. Both wasp sources can develop in either host species. Hybrids resulting from MsT♂xCcC♀ crosses are fertile, whereas hybrids from CcC♂xMsT♀ crosses are typically sterile. In this study, we compared relative expression in vivo of seven C. congregata bracovirus (CcBV) genes among MsT and CcC parental and hybrid crosses. Also, we established hybrid crosses between MsT and CcC wasps and four additional host foodplant sources of C. congregata. Patterns of relative expression in vivo of MsT and CcC CcBV genes differed; a few were not expressed in hosts parasitized by CcC wasps. Overall, relative expression of CcBV genes from MsT and CcC wasps did not differ with respect to the host species parasitized. Low or absent expression of CcBV genes was found in hosts parasitized by sterile hybrids. For the most part, the other four host-foodplant wasp sources were reproductively compatible with either MsT or CcC wasps and hybrid crosses with the alternative wasp source were asymmetrically sterile. Crosses involving CcC males or MsT females produced sterile hybrids that lacked mature ovaries. Cumulatively, results indicate that C. congregata is composed of two sympatric incipient species that can utilize multiple host species rather than several host-associated races or cryptic species.
Acoustic signals play an important role in premating isolation based on sexual selection within many taxa. Many male parasitic wasps produce characteristic courtship songs used by females in mate selection. In Cotesia (Hymenoptera: Braconidae: Microgastrinae), courtship songs are generated by wing fanning with repetitive pulses in stereotypical patterns. Our objectives were to sample the diversity of courtship songs within Cotesia and to identify e underlying patterns of differentiation. We compared songs among 12 of ca. 80 Cotesia species in North America, including ten species that have not been recorded previously. For Cotesia congregata, we compared songs of wasps originating from six different host-foodplant sources, two of which are considered incipient species. Songs of emergent males from wild caterpillar hosts in five different families were recorded, and pattern, frequency, and duration of song elements analyzed. Principal component analysis converted the seven elements characterized into four uncorrelated components used in a hierarchical cluster analysis and grouped species by similarity of song structure. Species songs varied significantly in duration of repeating pulse and buzz elements and/or in fundamental frequency. Cluster analysis resolved similar species groups in agreement with the most recent molecular phylogeny for Cotesia spp., indicating the potential for using courtship songs as a predictor of genetic relatedness. Courtship song analysis may aid in identifying closely related cryptic species that overlap spatially, and provide insight into the evolution of this highly diverse and agriculturally important taxon.
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