Using entomopathogenic fungi for biological control is an effective method for controlling certain crop pests, with the perspective of reducing the use of chemical pesticides. Yet, the efficiency of pathogenic fungi is dependent upon many factors that need to be evaluated to improve biological control potential in the fields (Lacey, 2001). The article by Chailleux et al. (2024) presents an exciting contribution to the field of biological pest control, specifically focusing on using entomopathogenic fungi to manage the oriental fruit fly, Bactrocera dorsalis. This fly, a member of the Tephritidae family, is a major threat to orchards in Asia, the Pacific and Africa, as it attacks fruit and causes considerable damage, in addition to having a relatively rapid biological invasion dynamic (Clarke et al. 2005). 

The objective of the Chailleux et al. (2024) study was to evaluate the virulence of Metarhizium anisopliae spores (strain Met69) on B. dorsalis adult flies according to various conditions: the inoculation dose and spore load, the formulation (adjuvant) and temperature conditions. The focus on host specificity and on-target applications was conducted to ensure minimal impact on non-target organisms, which is crucial for sustainable agriculture. The main challenge in this system was to achieve high strain virulence to kill wild individuals with a low number of spores—therefore limiting impact on non-target species such as natural enemies—but with a sufficient incubation period to allow transmission from mass-reared insects to wild conspecifics (Leite et al. 2022). A comparison of different inoculation methods is also provided and is interesting from a methodological point of view for future studies or even large-scale applications.

Using a well-designed experimental setup, the authors show that high pathogenicity (measured by LD50) is achievable even at low spore doses and independently of the fly's sex. Lethal action speed was, however, dependent on the dose. Regarding temperature, the authors demonstrated that mycelium growth was affected by the mean temperature but, most importantly, by daily fluctuation regimes; night and day temperature alternation allowed faster growth than constant temperature. These notions of thermal fluctuations are still under-researched in terms of their modulating role in biological control yet seem central to understanding them, as the authors demonstrate here. The correlation between increased virulence and specific abiotic factors, such as temperature, offers valuable additional insights into the bioecology of the insect host and the fungal pathogen. Chailleux et al. finally point out the need for careful selection of adjuvants in formulations and pay attention to interactions with the abiotic environment to avoid compromising the effectiveness of biological control agents. Indeed, the survival rate of inoculated flies increased in the presence of the corn starch adjuvant, but this effect decreased with temperature. As corn starch unexpectedly delayed mortality, the authors suggest a potential for enhancing conspecific transmission

From a broader perspective, the study emphasizes the importance of standardizing virulence evaluation to optimize biological control strategies like auto-dissemination or vectoring with sterile males, particularly in field conditions. The study contributions are timely and essential for advancing sustainable pest management strategies and improving inoculation methods. The findings underscore the need for field trials to refine these strategies, particularly in Africa, where climatic factors may affect pathogen efficacy and fly behavior. I recommend publishing this article in a referenced journal like the Peer Community Journal. 

References

Chailleux, A. Coulibaly, ON, Diouf B, Diop S, Sohel A, Brevault T (2023) Dose, temperature and formulation shape Metarhizium anisopliae virulence against the oriental fruit fly: lessons for improving on-target control strategies. bioRxiv, ver.2 peer-reviewed and recommended by PCI Zoology https://doi.org/10.1101/2023.12.14.571642

Clarke, A. R. et al. (2005). Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annu. Rev. Entomol., 50, 293-319. https://doi.org/10.1146/annurev.ento.50.071803.130428

Lacey, L. A. (2001). Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments. J Invertebr Pathol, 77, 147. https://doi.org/10.1006/jipa.2000.5005

Leite, M. O. et al. (2022). Laboratory risk assessment of three entomopathogenic fungi used for pest control toward social bee pollinators. Microorganisms, 10, 1800. https://doi.org/10.3390/microorganisms10091800

Some of the biodiversity of our planet now exists only in museums, due to continuing habitat destruction and climate change. With more than 380 million entomological specimens already preserved in museums (Johnson and Owens 2023), there is much work left to document what we already have. Fortunately, new advances in DNA sequencing have given us the opportunity to get enormous amounts of information from dried specimens on pins.
 
One such advance is HyRAD-X, which uses RAD-derived probes originally developed using RNA extracted from a selection of specimens with high RNA-integrity (Schmid et al. 2017). These exome-limited probes can then be used to capture low-integrity DNA extracted from a single leg from museum specimens, followed by Illumina sequencing of the enriched libraries.
 
Ground beetles allow an excellent demonstration of this approach, as their diversity, large size, and charismatic appearance has led to them being well represented in museums. Using a HyRAD-X probe set previously developed for a higher phylogeny within the subfamily Carabinae (Toussaint et al. 2021), the authors have now applied the same probe set to produce a comprehensive phylogeny for Arcifera, a clade of four subgenera and ten species within the genus Carabus (Pauli et al. 2024).
 
Of the 96 specimens that they started out with, 90% were from natural history collections and 40% dropped out immediately due to poor DNA extraction yield. After filtering the resulting sequence reads for minimum coverage and minimum number of samples per locus, they ended up with 35 museum specimens with an average of 793 loci. Phylogenetic analysis of this data supported the current classification of these beetles.
 
Pauli et al’s. (2024) study has effectively shown the power of HyRAD-X methods for applications at the species level. In-house production of probes makes the method accessible, expanding the opportunity to use museum specimens for population genetic research.

References

Johnson KR, Owens, (IFP. 2023) A global approach for natural history museum collections. Science 379,1192-1194(2023). https://doi.org/10.1126/science.adf6434

Pauli MT, Gauthier J, Labédan M, Blanc M, Bilat J, Toussaint EFA (2024) Museomics of Carabus giant ground beetles shows an Oligocene origin and in situ alpine diversification. bioRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2024.03.21.586057

Schmid, S., Genevest, R., Gobet, E., Suchan, T., Sperisen, C., Tinner, W. and Alvarez, N. (2017), HyRAD-X, a versatile method combining exome capture and RAD sequencing to extract genomic information from ancient DNA. Methods Ecol Evol, 8: 1374-1388. https://doi.org/10.1111/2041-210X.12785

Toussaint EFA, Gauthier J, Bilat J, Gillett CPDT, Gough HM, Lundkvist H, Blanc M, Muñoz-Ramírez CP, Alvarez N (2021) HyRAD-X Exome Capture Museomics Unravels Giant Ground Beetle Evolution, Genome Biology and Evolution, Volume 13, Issue 7, evab112, https://doi.org/10.1093/gbe/evab112

Insect species richness and diversity comparisons between samples of the tropics around the world are rare, especially in taxa composed mainly of cryptic species as parasitoid wasps.

The article by Hopkins et al. (2024) compares samples of parasitoid wasps of the subfamily Rhyssinae (Hymenoptera: Ichneumonidae) collected by Malaise traps in tropical rainforests of Perú and Uganda. The samples presented several differences in the time of collecting, covertures, and the sampling number; however, they used the same kind of traps, and the taxonomic process for species delimitation was made for the same team of ichneumonid experts, using equivalent characters.

Publications about this kind of comparative study are difficult to find because cooperative projects on insect richness and diversity from South American and African continents are not frequent. In this sense, this study presented a valuable contrast that shows interesting results about the higher richness and lower abundance of the biota of the American tropics, even with a small sample, in comparison with the biota of the African tropics. The results are supported mainly by the rarefaction curves shown. This pattern of higher species richness and lower specimen abundance, observed in other American tropical taxa such as trees, birds, or butterflies, is observed too in these parasitoid wasps, increasing the body of information that could support the extension of the pattern to the entire biota of the American tropics. The authors recognize the study's limitations, which include strong differences in the size of the forest coverture between places. However, these differences and others are enough described and discussed.

This work is useful because it increases the information about the diversity patterns of the tropics around the world and because study a taxon mainly composed of cryptic species, with a small amount of information in tropical regions.

References

Hopkins T., Tuomisto H., Gómez I.C., Sääksjärvi I. E. 2024. A comparison of the parasitoid wasp species richness of tropical forest sites in Peru and Uganda – subfamily Rhyssinae (Hymenoptera: Ichneumonidae). bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2023.08.23.554460

The intricate relationships between parasites and their hosts often involve a choreography of behavioral changes, with parasites manipulating their hosts in a way that enhances - or seemingly enhances – their transmission (Hughes et al., 2012; Moore, 2002; Poulin, 2010). Host manipulation is increasingly acknowledged as a pervasive adaptive transmission strategy employed by parasites, and as such is one of the most remarkable manifestations of the extended phenotype (Dawkins, 1982).

In this laboratory study, Rigaud et al. (2023) delved into the time course of antipredator behavioral modifications induced by the acanthocephalan Pomphorhynchus laevis in its amphipod intermediate host Gammarus pulex. This system has a good foundation of prior knowledge (Bakker et al., 2017; Fayard et al., 2020; Perrot-Minnot et al., 2023), nicely drawn upon for the present work. This parasite orchestrates a switch from predation suppression, during the noninfective phase, to predation enhancement upon maturation. Specifically, G. pulex infected with the non-infective acanthella stage of the parasite can exhibit increased refuge use and reduced activity compared to uninfected individuals (Dianne et al., 2011, 2014), leading to decreased predation by trout (Dianne et al., 2011). In contrast, upon reaching the infective cystacanth stage, the parasite can enhance the susceptibility of its host to trout predation (Dianne et al., 2011).

The present work aimed to understand the temporal sequence of these behavioral changes across the entire ontogeny of the parasite. The results confirmed the protective role of P. laevis during the acanthella stage, wherein infected amphipods exhibited heightened refuge use. This protective manipulation, however, became significant only later in the parasite's ontogeny, suggesting a delayed investment strategy, possibly influenced by the extended developmental time of P. laevis. The protective component wanes upon reaching the cystacanth stage, transitioning into an exposure strategy, aligning with theoretical predictions and previous empirical work (Dianne et al., 2011; Parker et al., 2009). The switch was behavior-specific. Unlike the protective behavior, a decline in the amphipod activity rate manifested early in the acanthella stage and persisted throughout development, suggesting potential benefits of reduced activity for the parasite across multiple stages. Furthermore, the findings challenge previous assumptions regarding the condition-dependency of manipulation, revealing that the parasite-induced behavioral changes predominantly occurred in the presence of cues signaling potential predators. Finally, while amphipods infected with acanthella stages displayed survival rates comparable to their uninfected counterparts, increased mortality was observed in those infected with cystacanth stages.

Understanding the temporal sequence of host behavioral changes is crucial for deciphering whether it is adaptive to the parasite or not. This study stands out for its meticulous examination of multiple behaviors over the entire ontogeny of the parasite highlighting the complexity and condition-dependent nature of manipulation. The protective-then-expose strategy emerges as a dynamic process, finely tuned to the developmental stages of the parasite and the ecological challenges faced by the host. The delayed emergence of protective behaviors suggests a strategic investment by the parasite, with implications for the host's survival and the parasite's transmission success. The differential impact of infection on refuge use and activity rate further emphasizes the need for a multidimensional approach in studying parasitic manipulation (Fayard et al., 2020). This complexity demands further exploration, particularly in deciphering how trophically-transmitted parasites shape the behavioral landscape of their intermediate hosts and its temporal dynamic (Herbison, 2017; Perrot-Minnot & Cézilly, 2013).  As we discover the many subtleties of these parasitic manipulations, new avenues of research are unfolding, promising a deeper understanding of the ecology and evolution of host-parasite interactions.

References

Bakker, T. C. M., Frommen, J. G., & Thünken, T. (2017). Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology, 123(11), 779–784. https://doi.org/10.1111/eth.12660

Dawkins, R. (1982). The extended phenotype: The long reach of the gene (Reprinted). Oxford University Press.

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Gaillard, M., Léger, E., & Rigaud, T. (2011). Protection first then facilitation: A manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution, 65(9), 2692–2698. https://doi.org/10.1111/j.1558-5646.2011.01330.x

Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Guvenatam, A., & Rigaud, T. (2014). Parasite-induced alteration of plastic response to predation threat: Increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. International Journal for Parasitology, 44(3–4), 211–216. https://doi.org/10.1016/j.ijpara.2013.11.001

Fayard, M., Dechaume‐Moncharmont, F., Wattier, R., & Perrot‐Minnot, M. (2020). Magnitude and direction of parasite‐induced phenotypic alterations: A meta‐analysis in acanthocephalans. Biological Reviews, 95(5), 1233–1251. https://doi.org/10.1111/brv.12606

Herbison, R. E. H. (2017). Lessons in Mind Control: Trends in Research on the Molecular Mechanisms behind Parasite-Host Behavioral Manipulation. Frontiers in Ecology and Evolution, 5, 102. https://doi.org/10.3389/fevo.2017.00102

Hughes, D. P., Brodeur, J., & Thomas, F. (2012). Host manipulation by parasites. Oxford university press.

Moore, J. (2002). Parasites and the behavior of animals. Oxford University Press.

Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K., & Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution, 63(2), 448–458. https://doi.org/10.1111/j.1558-5646.2008.00565.x

Perrot-Minnot, M.-J., & Cézilly, F. (2013). Investigating candidate neuromodulatory systems underlying parasitic manipulation: Concepts, limitations and prospects. Journal of Experimental Biology, 216(1), 134–141. https://doi.org/10.1242/jeb.074146

Perrot-Minnot, M.-J., Cozzarolo, C.-S., Amin, O., Barčák, D., Bauer, A., Filipović Marijić, V., García-Varela, M., Servando Hernández-Orts, J., Yen Le, T. T., Nachev, M., Orosová, M., Rigaud, T., Šariri, S., Wattier, R., Reyda, F., & Sures, B. (2023). Hooking the scientific community on thorny-headed worms: Interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite, 30, 23. https://doi.org/10.1051/parasite/2023026

Poulin, R. (2010). Parasite Manipulation of Host Behavior. In Advances in the Study of Behavior (Vol. 41, pp. 151–186). Elsevier. https://doi.org/10.1016/S0065-3454(10)41005-0

Rigaud, T., Balourdet, A., & Bauer, A. (2023). Time-course of antipredator behavioral changes induced by the helminth Pomphorhynchus laevis in its intermediate host Gammarus pulex: The switch in manipulation according to parasite developmental stage differs between behaviors. bioRxiv, ver. 6 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2023.04.25.538244

Biotic interactions are often shaped by abiotic factors (Liu and Gaines 2022). Although this notion is not new in ecology and evolutionary biology, we are still far from a thorough understanding of how biotic interactions change along abiotic gradients in space and time. This is particularly challenging because abiotic factors can affect organisms and their interactions in multiple – direct or indirect – ways. For example, because abiotic conditions strongly determine how energy enters biological systems via producers, their effects can propagate through entire food webs, from the bottom to the top (O’Connor 2009, Gilbert et al 2019). Understanding how biological diversity - both within and across species - is shaped by the indirect effects of environmental conditions is a timely question as climate change and anthropogenic activities have been altering temperature and water availability across different ecosystems.

Motivated by the current water crisis and severe droughts predicted for the near future worldwide (du Plessis 2019), Migeon et al. (2023) investigated how water limitation on producers scales up to affect life-history patterns of a widespread crop pest, the spider mite Tetranychus urticae. The authors sampled spider mite populations (n = 12) along a striking gradient of climatic conditions (>16 degrees of latitude) in Europe. After letting mites acclimate to lab conditions for several generations, the authors performed a common garden experiment to quantify how the life-history traits of mite populations from different locations respond to drought stress in their host plants.

Curiously, the authors found that, when reared on drought-stressed plants, mites tended to develop faster, had higher fecundity and lower dispersion rates. This response was in line with some results obtained previously with Tetranychus species (e.g. Ximénez-Embun et al 2016). Importantly, despite some experimental caveats in the experimental design, which makes it difficult to completely disentangle the specific effects of location vs. environmental noise, results suggest the climate that populations originally experienced was also an important determinant of the plastic response in these herbivores. In fact, populations from wetter and colder regions showed a steeper change in drought response, while populations from arid climates showed a shallower response. This interesting result suggests the importance of intraspecific (between-populations) variation in the response to drought, which might be explained by the climatic heterogeneity in space throughout the evolutionary history of different populations. These results become even more important in our rapidly changing world, highlighting the importance of considering genetic variation (and conditions that generate it) when predicting plastic and evolutionary responses to stressful conditions.
 
REFERENCES

du Plessis, A. (2019). Current and Future Water Scarcity and Stress. In: Water as an Inescapable Risk. Springer Water. Springer, Cham. https://doi.org/10.1007/978-3-030-03186-2
 
Gibert, J.P. Temperature directly and indirectly influences food web structure. Sci Rep 9, 5312 (2019). https://doi.org/10.1038/s41598-019-41783-0
 
Liu, O. R., & Gaines, S. D. (2022). Environmental context dependency in species interactions. Proceedings of the National Academy of Sciences, 119(36), e2118539119. https://doi.org/10.1073/pnas.2118539119
 
Migeon A., Auger P., Fossati-Gaschignard O., Hufbauer R.A, Miranda M., Zriki G., Navajas M. (2023) The response to drought-stressed host plants varies among herbivorous mite populations from a climate gradient. bioRxiv, 2021.10.21.465244, ver. 4 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.10.21.465244
 
O'Connor, M.I. (2009), Warming strengthens an herbivore-plant interaction. Ecology, 90: 388-398. https://doi.org/10.1890/08-0034.1
 
Ximénez-Embún, M. G., Ortego, F., & Castañera, P. (2016). Drought-stressed tomato plants trigger bottom-up effects on the invasive Tetranychus evansi. PloS one, 11(1), e0145275. https://doi.org/10.1371/journal.pone.0145275