Integrated pest management relies on the combined use of different practices in time and/or space. The main objectives are to better control pests, not to induce too much selective pressure on resistance mechanisms present in pest populations and to minimize non-targeted effects on the ecosystem [1]. The efficiency of such a strategy requires at least additional or synergistic effects of chosen tools against targeted pest population in a specific environment. Any antagonistic effect on targeted or non-targeted organisms might reduce control effort to nil even worst.

Van Oudenhove et al [2] raised the question of the interaction between botanical pesticides (BPs) and egg parasitoids. Each of these two strategies used for pest management present advantages and are described as eco-friendly. First, the use of parasitoids is a great example of biological control and is massively used in a broad range of crop production in different ecological settings. Second, BPs, especially essential oils (EOs) used for a wide range of activities on pests (repellent, antifeedant, antiovipositant, ovicidal, larvicidal and simply pesticidal) present low-toxicity to non-target vertebrates and do not last too long in the environment. Combining these two strategies might be considered as a great opportunity to better pest control with minimized impact on environment. However, EOs used to target a wide range of pest might directly or indirectly affect parasitoids.

Van Oudenhove et al [2] focused their study on non-target effects of 10 essentials oils with pesticide potential on larval development and egg-seeking behaviour of five strains of the biocontrol agent Trichogramma evanescens. Within two laboratory experiments mimicing EOs fumigation (i.e. contactless EOs exposure), the authors evaluated (1) the toxicity of EOs on parasitoid development and (2) the repellent effect of these EOs on adult wasps. They confirmed that contactless exposure of EOs can (1) induce mortality during pre-imaginal development (more acute at the pupal stage) and (2) induce behavioural avoidance of EOs odour plume. These experiments ran onto five strains of T. evanescens also highlighted the variation of the effects of EOs among parasitoid strains.

The complex and dynamic interaction between pest, plant, parasitoid (a natural enemy) and their environment is disturbed by EOs. EOs plumes are also dynamic and variable upon the environmental conditions. The results of van Oudenhove et al. experimentally illustrate such a complexity by describing opposite effects (repellent and attractive) of the same EO on the behaviour of two T. evanescens strains. These contrasting results led us to question more broadly the non-target effects of pest management programs based on EOs fumigation on natural enemies.

Finally, the limits of this experimental study as discussed in the paper draw research avenues taking into account biotic variables such as plant chemical cues, odour plume dynamics, individual behavioural experiences and abiotic variables such as temperature, light and gravity [3] in laboratory, semi-field and field experiments. Facing such a complexity, modelling studies at fine scale in time and space have the operational objective to help farmers to choose the best IPM strategy regarding their environment (as illustrated for aphid population management in the recent review by Stell et al. [4]). But before such research effort to be undertaken, Van Oudenhove et al study [2] sounds like an alert for a cautious use of EOs in pest control programs that integrate biological control with parasitoids.

References

[1] Fauvergue, X. Biocontrôle Elements Pour Une Protection Agroecologique des Cultures; Éditions Quae: Versailles, France, 2020.

[2] van Oudenhove L, Cazier A, Fillaud M, Lavoir AV, Fatnassi H, Pérez G, Calcagno V. Non-target effects of ten essential oils on the egg parasitoid Trichogramma evanescens. bioRxiv 2022.01.14.476310, ver. 4 peer-reviewed and recommended by PCI Zoology. https://doi.org/10.1101/2022.01.14.476310

[3] Victor Burte, Guy Perez, Faten Ayed, Géraldine Groussier, Ludovic Mailleret, Louise van Oudenhove and Vincent Calcagno (2022) Up and to the light: intra- and interspecific variability of photo- and geo-tactic oviposition preferences in genus Trichogramma, Peer Community Journal, 2: e3. https://doi.org/10.24072/pcjournal.78

[4] Stell E, Meiss H, Lasserre-Joulin F, Therond O. Towards Predictions of Interaction Dynamics between Cereal Aphids and Their Natural Enemies: A Review. Insects 2022, 13, 479. https://doi.org/10.3390/insects13050479

Because of the inability of eggs to move, the fitness of oviparous organisms is particularly dependent on the oviposition site. The choice of oviposition site by mothers is therefore the result of trade-offs between exposure to risk factors or favorable conditions such as the presence/absence of predators, the threat of extreme temperatures, the risk of desiccation, the presence and quality of nutritional resources... In addition to these trade-offs between different biotic and abiotic factors that determine oviposition site selection, the ability of mothers to move their eggs after oviposition is a game-changer in insect strategies to optimize egg development and survival [1]. Oviposition site selection combined with egg transport has been explored in insects in relation to the risk of exposure to egg parasitoids [2] or needs for oxygenation [3] but surprisingly has not been investigated in regards to temperatures. Considering egg transport in the ability of insects to adapt their behavior to environmental conditions and in particular to potential extreme temperatures is yet inherent in providing a complete picture of the diversity of behaviors that shape adaptation to temperature and potential tolerance to climate change. In this sense, the study presented by Tourneur et al. [4], explores whether insects capable of egg-care might use egg transport as an adaptive behavior to protect them from suboptimal or extreme temperatures. The study was conducted in the European earwig, Forficula auricularia Linnaeus, 1758, which is known to practice egg-care in a variety of ways, that presumably includes egg-transportation, for several weeks or months during winter until hatching. The authors characterized different life-history traits related to egg-laying, egg-transport, and egg-development in two device systems with three experimental temperature regimes in two populations of European earwigs from Canada. The inclusion of two populations, which turned out to belong to two clades, allowed the identification of a diversity of behaviors although this did not allow to attribute the differences between the two populations to specific population differences, genetic differences, or to their geographical origins. Interestingly, the study showed that oviposition site selection in the European earwig is driven by temperature and that in winter temperatures, female earwigs may move their eggs to warmer temperatures that are adequate for hatching. These results are original in the sense that they highlight new adaptive strategies in female insects used during the post-oviposition stage to protect their eggs from temperature changes.

In the current context of climate change and potential changes in selective pressures, the study contributes to the understanding of the wide range of strategies deployed by insects to adapt to the temperature. This appears essential to predict and anticipate the consequences of global instability, it also describes from an academic point of view a new and fascinating adaptive strategy in an overlooked biological system. 

References

[1] Machado G, Trumbo ST (2018) Parental care. In: Insect Behavior, pp. 203–218. Oxford University Press, Oxford. https://doi.org/10.1093/oso/9780198797500.003.0014

[2] Carrasco D, Kaitala A (2009) Egg-laying tactic in Phyllomorpha laciniata in the presence of parasitoids. Entomologia Experimentalis et Applicata, 131, 300–307. https://doi.org/10.1111/j.1570-7458.2009.00857.x

[3] Smith RL (1997) Evolution of paternal care in the giant water bugs (Heteroptera: Belostomatidae). In: The Evolution of Social Behaviour in Insects and Arachnids (eds Crespi BJ, Choe JC), pp. 116–149. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511721953.007

[4] Tourneur J-C, Cole C, Vickruck J, Dupont S, Meunier J (2022) Pre- and post-oviposition behavioural strategies to protect eggs against extreme winter cold in an insect with maternal care. bioRxiv, 2021.11.23.469705, ver. 3 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.11.23.469705

I recommend the Van Steenberge et al. study. With over 2000 endemic species, the East African cichlids are a well-established model system in speciation research (Salzburger 2018) and several models have been proposed and tested to explain how these radiations formed (Kocher 2004). Hybridization was shown to be a main driver of the rapid speciation and adaptive radiations of the East African Cichlid fishes (Seehausen 2004). However, it is obvious that unrestrained hybridization also has the potential to reduce taxonomic diversity by erasing species barriers. In the classical model of cichlid evolution, special emphasis was placed on mate preference (Kocher 2004). However, no attention was placed on species recognition, which was implicitly assumed. There is, however, more research needed on what species recognition means, especially in radiating lineages such as cichlids. In a previous study, Nevado et al. 2011 found traces of asymmetrical hybridization between members of the Lake Tanganyika radiation: the genus Ophthalmotilapia. This recommended study by Van Steenberge et al. is based on Nevado et al. (2011), which detected that in one genus of Ophthalmotilapia mitochondrial DNA ‘typical’ for one of the four species (O. nasuta) was also found in three other species (O. ventralis, O. heterodonta, and O. boops). The authors suggested that this could be explained by the fact that females of the three other species accepted O. nasuta males, but that O. nasuta females were more selective and accepted only conspecifc males. This could hence be due to asymmetric mate preferences, or by asymmetric abilities for species recognition. 

This is exactly what the current study by Van Steenberge et al. did. They tested the latter hypothesis by presenting females of two different Ophthalmotilapia species with con- and heterospecific males. This was tested through experiments, making use of wild specimens of two species: O. nasuta and O. ventralis. The authors assumed that if they performed classical “choice-experiments”, they would not notice the recognition effects, given that females would just select preferred, most likely conspecific, males. Instead, specimens were only briefly presented to other fishes since the authors wanted to compare differences in the ability for ‘species recognition’. In this, the authors followed Mendelson and Shaw (2012) who used “a measurable difference in behavioural response towards conspecifics as compared to heterospecifics’’ as a definition for recognition. Instead of the focus on selection/preference, they investigated if females of different species behaved differently, and hence detected the difference between conspecific and heterospecific males. This was tested by a short (15 minutes) exposure to another fish in an isolated part of the aquarium. Recognition was defined as the ‘difference in a particular behaviour between the two conditions’. What was monitored was the swimming behaviour and trajectory (1 image per second) together with known social behaviours of this genus. The selection of these behaviours was further facilitated based on experimental set-ups of reproductive behaviour or the same species previously described by the same research team (Kéver et al. 2018).

The result was that O. nasuta females, for which it was expected that they would not hybridize, showed a different behaviour towards a con- or a heterospecific male. They interacted less with males of the other species. What was unexpected is that there was no difference in behaviour of the females whether they recognized a male or (control) female of their own species. This suggests that they did not detect differences in reproductive behaviour, but rather in the interactions between conspecifics. For females of O. ventralis, for which there are indications for hybridization in the wild, they did not find a difference in behaviour. Females of this species behaved identically with respect to the right and wrong males as well as towards the control females. Interestingly is thus that a complex pattern between species in the wild could be (partially) explained by the behaviour/interaction at first impression of the individuals of these species. 

References

Kéver L, Parmentier E, Derycke S, Verheyen E, Snoeks J, Van Steenberge M, Poncin P (2018) Limited possibilities for prezygotic barriers in the reproductive behaviour of sympatric Ophthalmotilapia species (Teleostei, Cichlidae). Zoology, 126, 71–81. https://doi.org/10.1016/j.zool.2017.12.001

Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics, 5, 288–298. https://doi.org/10.1038/nrg1316

Mendelson TC, Shaw KL (2012) The (mis)concept of species recognition. Trends in Ecology & Evolution, 27, 421–427. https://doi.org/10.1016/j.tree.2012.04.001

Nevado B, Fazalova V, Backeljau T, Hanssens M, Verheyen E (2011) Repeated Unidirectional Introgression of Nuclear and Mitochondrial DNA Between Four Congeneric Tanganyikan Cichlids. Molecular Biology and Evolution, 28, 2253–2267. https://doi.org/10.1093/molbev/msr043

Salzburger W (2018) Understanding explosive diversification through cichlid fish genomics. Nature Reviews Genetics, 19, 705–717. https://doi.org/10.1038/s41576-018-0043-9

Seehausen O (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198–207. https://doi.org/10.1016/j.tree.2004.01.003

Steenberge MV, Jublier N, Kéver L, Gresham S, Derycke S, Snoeks J, Parmentier E, Poncin P, Verheyen E (2022) The initial response of females towards congeneric males matches the propensity to hybridise in Ophthalmotilapia. bioRxiv, 2021.08.07.455508, ver. 3 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.1101/2021.08.07.455508

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

The sorting of organisms along a fast-slow continuum through correlations between life history traits is a long-standing framework (Stearns 1983) and corresponds to the pace-of-life axis. This axis represents the variation in a continuum of life-history strategies, from fast-reproducing short-lived species to slow-reproducing long-lived species. The pace-of-life axis has been the focus of much research largely in mammals, birds, reptiles and plants but less so in invertebrates (Salguero-Gómez et al. 2016; Araya-Ajoy et al. 2018; Healy et al. 2019; Bakewell et al. 2020). Outcomes from this research have highlighted variation across taxa on this axis and mixed support for, and against, patterns expected of the pace-of-life continuum. Given this, a greater understanding of the variation of the pace-of-life across-, and within, taxa are needed. Indeed, Guicharnard et al. (2023) highlight several points regarding our broader understanding of pace-of-life. In general, invertebrates are poorly represented, the variation of pace-of-life across taxonomic scales is less well understood and the relationship between pace-of-life and dispersal, a key life history, requires more attention. Here, Guicharnard et al. (2023) provide a first attempt at addressing the relationship between dispersal and pace-of-life at different scales.

The authors, under controlled conditions, investigated how life-history traits and effective dispersal covary for 28 lines from five species of endoparasitoid wasps from the genus Trichogramma. At the species level negative correlations were found between development time and fecundity, matching pace-of-life axis predictions. Although this correlation was not found to be significant among lines, within species, a similar pattern of a negative correlation was observed. This outcome matches previous findings that consistent pace-of-life axes become more difficult to find at lower taxonomic levels. Unlike the other life-history traits measured, effective dispersal showed no evidence of differences between species or between lines. The authors also found no correlation between effective dispersal and other-life history traits which suggests no dispersal/life-history syndromes in the species investigated. One aspect that was not assessed was the impact of density dependence on pace-of-life and effective dispersal, largely as this was a first step in assessing relationship of dispersal with pace-of-life at different scales. However, the authors do acknowledge the importance of future studies incorporating density dependence and that such studies could potentially lead to more generalizable understanding of pace-of-life and dispersal within Trichogramma.

A pleasant addition was the link to potential implications for biocontrol. This addition showed an awareness by the authors of how insights into pace-of-life can have an applied component. The results of the study highlighted that selecting for specific lines of a species, to maximise a trait of interest at the cost of another, may not be as effective as selecting different species when implementing biocontrol. This is especially important as often single, established species used in biocontrol are favoured without consideration of the potential of other species which can lead to more efficient biocontrol.    

REFERENCES

Araya-Ajoy, Y.G., Bolstad, G.H., Brommer, J., Careau, V., Dingemanse, N.J. & Wright, J. (2018). Demographic measures of an individual's "pace of life": fecundity rate, lifespan, generation time, or a composite variable? Behavioral Ecology and Sociobiology, 72, 75.
https://doi.org/10.1007/s00265-018-2477-7
 
Bakewell, A.T., Davis, K.E., Freckleton, R.P., Isaac, N.J.B. & Mayhew, P.J. (2020). Comparing Life Histories across Taxonomic Groups in Multiple Dimensions: How Mammal-Like Are Insects? The American Naturalist, 195, 70-81.
https://doi.org/10.1086/706195
 
Guicharnaud, C., Groussier, G., Beranger, E., Lamy, L., Vercken, E. & Dahirel, M. (2023). Life-history traits, pace of life and dispersal among and within five species of Trichogramma wasps: a comparative analysis. bioRxiv, 2023.01.24.525360, ver. 3 peer-reviewed and recommended by Peer Community in Zoology.
https://doi.org/10.1101/2023.01.24.525360
 
Healy, K., Ezard, T.H.G., Jones, O.R., Salguero-Gómez, R. & Buckley, Y.M. (2019). Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction. Nature Ecology & Evolution, 3, 1217-1224.
https://doi.org/10.1038/s41559-019-0938-7
 
Salguero-Gómez, R., Jones, O.R., Jongejans, E., Blomberg, S.P., Hodgson, D.J., Mbeau-Ache, C., et al. (2016). Fast-slow continuum and reproductive strategies structure plant life-history variation worldwide. Proceedings of the National Academy of Sciences, 113, 230-235.
https://doi.org/10.1073/pnas.1506215112
 
Stearns, S.C. (1983). The Influence of Size and Phylogeny on Patterns of Covariation among Life-History Traits in the Mammals. Oikos, 41, 173-187.
https://doi.org/10.2307/3544261