Redistribution of domesticated and non domesticated species by humans profoundly affected earth biogeography and in return human activities. This process accelerated exponentially since human expansion out of Africa, leading to the modern global, highly connected and homogenized, agriculture and trade system (Mack et al. 2000, Jaksic and Castro 2021), that threatens biological diversity and genetic resources. To accompany quarantine and control effort, the reconstruction of invasion routes provides valuable information that help identifying critical nodes and edges in the global networks (Estoup and Guillemaud 2010, Cristescu 2015). Historical records and genetic markers are the two major sources of information of this corpus of knowledge on Anthropocene historical phylogeography. With the advances of molecular genetics tools, the genealogy of these introductions events could be revisited and empowered. Due to their idiosyncrasy and intimate association with the contingency of human trades and activities, understanding the invasion and domestication routes require particular statistical tools (Fraimout et al. 2017).

Because it encompasses all these theoretical, ecological and economical implications, I am pleased to recommend the readers of PCI Zoology this article by Mallez et al. (2021) on pine wood nematode invasion route inference from genetic markers using Approximate Bayesian Computation (ABC) methods.

Economically and ecologically, this pest, is responsible for killing millions of pines worldwide each year. The results show these damages and the global genetic patterns are due to few events of successful introductions. The authors consider that this low probability of introductions success reinforces the idea that quarantine measures are efficient. This is illustrated in Europe where the pine-worm has been quarantined successfully in the Iberian Peninsula since 1999. Another relevant conclusion is that hybridization between invasive populations have not been observed and implied in the invasion process. Finally the present study reinforced the role of Asiatic bridgehead populations in invasion process including in Europe.

Methodologically, for the first time, ABC was applied to this species. A total of 310 individual sequences were added to the Mallez et al. (2015) microsatellite dataset. Fraimoult et al. (2017) showed the interest to apply random forest to improve scenario selection in ABC framework. This method, implemented in the DiYABC software (Collin et al. 2020) for invasion route scenario selection allows to handle more complex scenario alternatives and was used in this study. In this article by Mallez et al. (2021), you will also find a clear illustration of the step-by-step approach to select scenario using ABC techniques (Lombaert et al. 2014). The rationale is to reduce number of scenario to be tested by assuming that most recent invasions cannot be the source of the most ancient invasions and to use posterior results on most ancient routes as prior hypothesis to distinguish following invasions. The other simplification is to perform classical population genetic analysis to characterize genetic units and representative populations prior to invasion routes scenarios selection by ABC.

Yet, even when using the most advanced Bayesian inference methods, it is recognized by the authors that the method can be pushed to its statistical power limits. The method is appropriate when population show strong inter-population genetic structure. But the high number of differentiated populations in native area can be problematic since it is generally associated to incomplete sampling scheme. The hypothesis of ghost populations source allowed to bypass this difficulty, but the authors consider simulation studies are needed to assess the joint effect of genetic diversity and number of genetic markers on the inference results in such situation. Also the need to use a stepwise approach to reduce the number of scenario to test has to be considered with caution. Scenarios that are not selected but have non negligible posterior, cannot be ruled out in the constitution of next step scenarios hypotheses.

Due to its interest to understand this major facet of Anthropocene, reconstruction of invasion routes should be more considered as a guide to damper biological homogenization process.

References

Collin, F.-D., Durif, G., Raynal, L., Lombaert, E., Gautier, M., Vitalis, R., Marin, J.-M. and Estoup, A. (2020) Extending Approximate Bayesian Computation with Supervised Machine Learning to infer demographic history from genetic polymorphisms using DIYABC Random Forest. Authorea. doi: https://doi.org/10.22541/au.159480722.26357192

Cristescu, M.E. (2015) Genetic reconstructions of invasion history. Molecular Ecology, 24, 2212–2225. doi: https://doi.org/10.1111/mec.13117

Estoup, A. and Guillemaud, T., (2010) Reconstructing routes of invasion using genetic data: Why, how and so what? Molecular Ecology, 9, 4113-4130. doi: https://doi.org/10.1111/j.1365-294X.2010.04773.x

Fraimout, A., Debat, V., Fellous, S., Hufbauer, R.A., Foucaud, J., Pudlo, P., Marin, J.M., Price, D.K., Cattel, J., Chen, X., Deprá, M., Duyck, P.F., Guedot, C., Kenis, M., Kimura, M.T., Loeb, G., Loiseau, A., Martinez-Sañudo, I., Pascual, M., Richmond, M.P., Shearer, P., Singh, N., Tamura, K., Xuéreb, A., Zhang, J., Estoup, A. and Nielsen, R. (2017) Deciphering the routes of invasion of Drosophila suzukii by Means of ABC Random Forest. Molecular Biology and Evolution, 34, 980-996. doi: https://doi.org/10.1093/molbev/msx050

Jaksic, F.M. and Castro, S.A. (2021). Biological Invasions in the Anthropocene, in: Jaksic, F.M., Castro, S.A. (Eds.), Biological Invasions in the South American Anthropocene: Global Causes and Local Impacts. Springer International Publishing, Cham, pp. 19-47. doi: https://doi.org/10.1007/978-3-030-56379-0_2

Lombaert, E., Guillemaud, T., Lundgren, J., Koch, R., Facon, B., Grez, A., Loomans, A., Malausa, T., Nedved, O., Rhule, E., Staverlokk, A., Steenberg, T. and Estoup, A. (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: The case of the Asian ladybird Harmonia axyridis. Molecular Ecology, 23, 5979-5997. doi: https://doi.org/10.1111/mec.12989

Mack, R.N., Simberloff, D., Lonsdale, M.W., Evans, H., Clout, M., Bazzaz, F.A. (2000) Biotic Invasions : Causes , Epidemiology , Global Consequences , and Control. Ecological Applications, 10, 689-710. doi: https://doi.org/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2

Mallez, S., Castagnone, C., Lombaert, E., Castagnone-Sereno, P. and Guillemaud, T. (2021) Inference of the worldwide invasion routes of the pinewood nematode Bursaphelenchus xylophilus using approximate Bayesian computation analysis. bioRxiv, 452326, ver. 6 peer-reviewed and recommended by Peer community in Zoology. doi: https://doi.org/10.1101/452326

Host-parasitoid interactions have been the focus of extensive ecological research for decades. One the of the major reasons is the importance host-parasitoid interactions play for the biological control of crop pests. Parasitoids are the main natural regulators for a large number of economically important pest insects, and in many cases they could be the only viable crop protection strategy. Parasitoids are also integral part of complex food webs whose structure and diversity display large spatio-temporal variations [1-3]. With the increasing globalization of human activities, the generalized spread and establishment of invasive species is a major cause of disruption in local community and food web spatio-temporal dynamics. In particular, the deliberate introduction of non-native parasitoids as part of biological control programs, aiming the suppression of established, and also highly invasive crop pests, is a common practice with potentially significant, yet poorly understood effects on local food web dynamics (e.g. [4]).
In their study, Muru et al. [5] took advantage of an existing biological control program focusing on the Asian chestnut gall wasp Dryocosmus kuriphilus, an invasive (and highly damaging) pest of chestnut trees. The species is currently a successful invader in many geographic regions, including southern France, where local parasitoid communities failed to provide an adequate control since its widespread establishment in 2010 [6]. In response, the non-native parasitoid species Torymus sinensis, which is highly-specific to the Asian chestnut gall wasp, was massively released in commercial chestnut orchards across several regions in France and the island of Corsica. The pest population outbreak was successfully contained, and thanks to the vast amount of host-parasitoid interaction data collected as part of the program, the authors were able to explore the effects of the large fluctuations in Asian chestnut gall wasp natural abundances on native parasitoid communities, immediately before, and up to five years following the introduction of its natural enemy T. sinensis.
Using co-occurrence and clustering analyses, Muru et al. [5] demonstrate that the invasion and the consecutive (efficient) control of the Asian chestnut gall wasp by the parasitoid T. sinensis have a significant impact on the structure of local parasitoid food webs. In particular, following decline in the Asian chestnut gall wasp’s populations, native parasitoids markedly switched to alternative hosts, most likely due to their respectively higher relative abundances. This pattern seemed to be driven by the degree of generalism in native parasitoid species. Indeed, when its abundances were still relatively high, the Asian chestnut gall wasp was primarily attacked by species capable of exploiting a broad range of hosts, while at low population densities only specialist parasitoids such as Mesolobus sericeus were able to persist and compete with the non-native T. sinensis.
The current study is important for two major reasons. First, it underscores the value of long-term species interaction data in order to understand the dynamic nature of food webs, namely their structural flexibility in response to changes in the environment or, as in this case, large fluctuation in abundances of a major pest species. In this context, biological control programs could be a great source of data for exploring long-term, large-scale dynamics of species interactions, and their use in ecological studies deserves to be further emphasized. Second, the study adds to the increasing empirical evidence that mobile generalist foragers can display adaptive, frequency-dependent switching behaviour ([1], [7]), which has been suggested to act as a key stabilizing mechanism in food webs by buffering fluctuating population dynamics at larger spatial scales ([8- 10]).
However, the timing of such buffering seems important, especially in systems such as commercial chestnut orchards. Despite their capacity to adaptively switch their foraging behaviour, the response of the native parasitoid communities to the new, unfamiliar resource was not fast enough in order to contain the primary outbreak under an appropriate damage threshold, thus requiring the introduction of the more specialized parasitoid T. sinensis. Nevertheless, based on current ecological theory, results presented by Muru et al. [5] suggest that the response of native parasitoid community to fluctuating host dynamics – i.e. shifts in parasitoid foraging behaviour based on their traits – could be predictable. This is encouraging considering the growing impact of biological invasions and insect pest outbreaks, but also the need to implement efficient, yet sustainable strategies for crop protection. Future studies would show at what extent observations by Muru et al. [5] are generalizable over longer time periods or other model systems. Noticeably, better understanding about population dynamics and interactions with the broader community of hosts available across habitats should allow to fine-tune predictions about parasitoids’ response to fluctuating resources.

References

[1] Eveleigh ES, McCann KS, McCarthy PC, Pollock SJ, Lucarotti CJ, Morin B, McDougall GA, Strongman DB, Huber JT, Umbanhowar J, Faria LDB (2007). Fluctuations in density of an outbreak species drive diversity cascades in food webs. Proc. Natl. Acad. Sci. USA 104, 16976-16981. doi: 10.1073/pnas.0704301104
[2] Tylianakis JM, Tscharntke T, Lewis OT (2007). Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445, 202-205. doi: 10.1038/nature05429
[3] Murakami M, Hirao T, Kasei A (2008). Effects of habitat configuration on host–parasitoid food web structure. Ecol. Res. 23, 1039-1049. doi: 10.1007/s11284-008-0478-0
[4] Geslin B, Gauzens B, Baude M, Dajoz I, Fontaine C, Henry M, Ropars L, Rollin O, Thébault E, Vereecken NJ (2016). Massively introduced managed species and their consequences for plant–pollinator interactions. Adv. Ecol. Res. 57, 147-199. doi: 10.1016/bs.aecr.2016.10.007
[5] Muru D, Borowiec N, Thaon M, Ris N, Viciriuc M I, Warot S, Vercken E (2020) The open bar is closed: restructuration of a native parasitoid community following successful control of an invasive pest. bioRxiv, 2019.12.20.884908, ver. 6 peer-reviewed and recommended by PCI Zoology. doi: 10.1101/2019.12.20.884908
[6] Borowiec N, Thaon M, Brancaccio L, Warot S, Vercken E, Fauvergue X, Ris N, Malausa J-C (2014). Classical biological control against the chestnut gall wasp 'Dryocosmus kuriphilus' (Hymenoptera, Cynipidae) in France. Plant Prot. Q. 29, 7-10.
[7] Bartley TJ, McCann KS, Bieg C, Cazelles K, Granados M, Guzzo MM, MacDougall AS, Tunney TD, McMeans BC (2019). Food web rewiring in a changing world. Nat. Ecol. Evol. 3, 345–354. doi: 10.1038/s41559-018-0772-3
[8] Kondoh M (2003). Foraging adaptation and the relationship between food-web complexity and stability. Science. 299, 1388-1391. doi: 10.1126/science.1079154
[9] McCann KS, Rooney N (2009). The more food webs change, the more they stay the same. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1789-801. doi: 10.1098/rstb.2008.0273
[10] Valdovinos FS, Ramos-Jiliberto R, garay-Narváez L, Urbani P, Dunne JA (2010). Consequences of adaptive behaviour for the structure and dynamics of food webs. Ecol. Lett. 13, 1546-1559. doi: 10.1111/j.1461-0248.2010.01535.x

Malaria is a vector-borne parasitic disease found in 91 countries with an estimated of 228 million cases occurred worldwide during 2018. The 93% (213 million) of those cases were reported in the African Region (WHO 2019). Six species of Plasmodium parasites can produce the disease but only P. falciparum and P. vivax are the predominant species globally. More than 40 species of Anopheles mosquitoes are important malaria vectors (Asley et al. 2018). Intrinsic (genetic background, parasite susceptibility) and extrinsic (feeding host preference, host diversity and availability, mosquito abundance) factors affect the capacity of mosquitoes to vector the disease (Macdonald 1952). Malaria is prevented by chemoprophylaxis, vaccination, bite-avoidance and vector-control measures. The mainstays of vector control are long-lasting insecticide (pyrethroid) treated nets and indoor residual spraying with insecticides (Asley et al. 2018). The widespread use of pyrethroid insecticides forced the emergence of insecticide resistance in malaria vectors reducing the insecticidal effect. Mosquitoes can modify their behaviour avoiding insecticide contact and so potentially reducing vector control tools efficacy. In this sense, Diop et al. (2020) investigated whether pre-exposure to an Insecticide-Treated Net (ITN) modulates the mosquito ability to take a blood meal in Anopheles gambiae. By means of video recording experiments the authors analyzed how the feeding/bitting behaviour was affected by kdr mutation genotypes (homozygous susceptible – SS-, heterozygotes -RS- and homozygous resistant -RR-) when exposed to two different insecticides (permethrin and deltamethrin). According to the results, the blood-feeding success did not differ between the three genotypes in the absence of insecticide exposure. However, authors observed differences in the feeding duration and blood meal size. In example, RR mosquitoes spent less time taking their blood meal than RS and SS. On the other hand, RS mosquitoes took higher blood volumes than RR females. These differences can affect the mosquito fitness by decreasing/increasing the likelihood to be killed by the host defensive behavior or increase the oogenesis so enhancing fecundity. Regarding the effect of exposition to insecticides authors detected a strong relationship between kdr genotype and Knock Down (KD) phenotype when mosquitoes were exposed to Permethrin. Previously, the authors have evidenced that RR mosquitoes prefer a host protected by a permethrin-treated net rather than an untreated net and that heterozygotes RS mosquitoes have a remarkable ability to find a hole into a bet net (Diop et al. 2015, Porciani et al. 2017). With data here obtained, they demonstrated that kdr homozygous resistant An. gambiae displayed enhanced feeding success when exposed to permethrin ITN. The changes observed in the feeding/biting mosquito behaviour can affect their fitness shaping the evolution of the insecticide resistance in mosquitoes’ natural populations. Moreover, this may also alter parasite transmission dynamics by modifying vector/host interactions and so vector capacity.

References

World Health Organization (2019). World malaria report 2019. Geneva: World Health Organization; 2019. ISBN 978-92-4-156572-1
Ashley EA, Pyae Phyo A, Woodrow CJ (2018). Malaria. Lancet. 391(10130):1608‐1621. doi: 10.1016/S0140-6736(18)30324-6
Macdonald G (1952). The analysis of equilibrium in malaria. Trop Dis Bull 49: 813-828.
Diop MM, Chandre F, Rossignol M, Porciani A, Château M, Moiroux N and Pennetier, C. (2020). Sub-lethal insecticide exposure affects host biting efficiency of Kdr-resistant Anopheles gambiae. bioRxiv 653980, ver. 4 peer-reviewed and recommended by PCI Zoology. doi: 10.1101/653980
Diop MM, Moiroux N, Chandre F, Martin-Herrou H, Milesi P, Boussari O, et al. (2015) Behavioral cost and overdominance in Anopheles gambiae. PLoS ONE. 10(4):e0121755. doi: 10.1371/journal.pone.0121755
Porciani A, Diop M, Moiroux N, Kadoke-Lambi T, Cohuet A, Chandre F, et al. (2017) Influence of pyrethroïd-treated bed net on host seeking behavior of Anopheles gambiae s.s. carrying the kdr allele. PLOS ONE. 12(7):e0164518. doi: 10.1371/journal.pone.0164518