Tell us how you can be, and we’ll make you better: exploiting genetic variability in personality traits to improve top-down control of agricultural pests
Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case study
Agriculture in the XXI century faces the huge challenge of having to provide food to a rapidly growing human population, which is expected to reach 10.9 billion in 2100 (UUNN 2019), by means of practices and methods that guarantee crop sustainability, human health safety, and respect to the environment (UUNN 2015). Such regulation by the United Nations ultimately entails that agricultural scientists are urged to design strategies and methods that effectively minimize the use of harmful chemical products to control pest populations and to improve soil quality.
One of the most, if not the most, sustainable, safe, and environmentally friendly approach to apply against pests is Biological Pest Control (BPC, hereafter), that is, the use of natural enemies to control the populations of pest organisms. The concept of BPC is by no means new: long back to the 300 AC, Chinese farmers built bamboo bridges between citrus trees to facilitate the foraging of the ant species Oecophylla smaragdina to control lepidopteran citrus pests (Konishi and Ito, 1973); It is also nice to use this recommendation letter to recall and quote the words written in 1752 by the famous Swedish taxonomist, botanist and zoologist, Carl Linnaeus: "Every insect has its predator which follows and destroys it. Such predatory insects should be caught and used for disinfecting crop-plants" (Hörstadius (1974) apud Linnaeus 1752).
Acknowledging the many cases of successes from BPC along our recent history, it is also true that application of BPC strategies during the XX century suffered from wrong-doings, mainly when the introduced biological control agent (BCA, hereafter) was of exotic origin and with a generalist diet-breath; in some cases the release of exotic species resulted on global extinction, reduction in the range of distribution, reduction in the population abundance, and partial displacement, of native and functionally similar species, and interbreeding with them (reviewed in van Lenteren et al. 2006). One of the most famous cases is that of Harmonia axyridis, a coccinellid predator of Asian origin that caused important environmental damage in North America (reviewed in Koch & Galvan, 2008).
Fortunately, after the implementation of the Nagoya protocol (CBD, 2011) importation of exotic species for BPC use was severely restricted and controlled, worldwide. Consequently, companies and agricultural scientist were driven to reinforce their focus and interest on the exploitation of native natural enemies, via the mass-rearing and release of native candidates (augmentative BPC), the conservation of landscapes near the crops to provide resources for natural enemies (i.e. conservation biological pest control), or via the exploitation of the genetic variability of BCAs, to create strains performing better at regulating pest populations under specific biotic or abiotic negative circumstances. Some of these cases are cited in Lartigue et al. (2020). The genetic improvement of BCAs is a strategy still in its infancy, but there is no doubt that the interest for it has significantly increased over the last 5 years (Lommen et al 2017, Bielza 2020, Leung et al 2020).
In my humble opinion, what makes the paper of Lartigue et al. (2020) a remarkable contribution to the field of genetic breeding of BCAs is that it opens a new window of opportunities to the field, by exploring the possibilities for artificial selection of behavioral traits (Réale et al. 2007) to "create" strains of natural enemies displaying behavioral syndromes (Sih et al. 2004) that makes them better at regulating pest populations. The behavioral approach for breeding BCAs can then be extended by crossing it with known abiotic and/or biotic hostile environments (e.g. warm and drought environments, presence of predators/competitors to the BCA, respectively) and engineer strains more prompt to display particular behavioral syndromes to help them to overcome the overall hostility of specific environments. I strongly believe that the approach proposed in Lartigue et al. (2020) will influence the future management of agricultural systems, where strategies including the genetic breeding of BCAs’ behavior will contribute to create better guards and protectors of our crops.
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CBD - Convention on Biological Diversity, 2011. The Nagoya Protocol on Access and Benefit-sharing, https://www.cbd.int/abs/doc/protocol/nagoya-protocol-en.pdf
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Konishi, M. and Ito, Y. (1973). Early entomology in East Asia. In: Smith, R.F., Mittler, T.E., Smith, C.N. (Eds.), History of Entomology, Annual Reviews Inc., Palo Alto, California, pp. 1-20.
Lartigue, S., Yalaoui, M., Belliard, J., Caravel, C., Jeandroz, L., Groussier, G., Calcagno, V., Louâpre, P., Dechaume-Moncharmont, F.-X., Malausa, T. and Moreau, J. (2020). Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case study. bioRxiv, 2020.08.21.257881, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.08.21.257881
Leung et al. (2020). Next-generation biological control: the need for integrating genetics and genomics. Biological Reviews, 95(6), 1838–1854. doi: https://doi.org/10.1111/brv.12641
Lommen, S. T. E., de Jong, P. W. and Pannebakker, B. A. (2017). It is time to bridge the gap between exploring and exploiting: prospects for utilizing intraspecific genetic variation to optimize arthropods for augmentative pest control – a review. Entomologia Experimentalis et Applicata, 162: 108-123. doi: https://doi.org/10.1111/eea.12510
Réale, D., Reader, S. M., Sol, D., McDougall, P. T. and Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological Reviews, 82: 291-318. doi: https://doi.org/10.1111/j.1469-185X.2007.00010.x
Sih, A., Bell, A. and Johnson, J. C. (2004). Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology and Evolution, 19(7), 372–378. doi: https://doi.org/10.1016/j.tree.2004.04.009
UUNN. 2015. Transforming our world: the 2030 Agenda for Sustainable Development. report of the Open Working Group of the General Assembly on Sustainable Development Goals (A/68/970 and Corr.1; see also A/68/970/Add.1–3).
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van Lenteren, J. C., Bale, J., Bigler, F., Hokkanen, H. M. T. and Loomans A. J. M. (2006). Assessing risks of releasing exotic biological control agents of arthropod pests. Annual Review of Entomology, 51: 609-634. doi: https://doi.org/10.1146/annurev.ento.51.110104.151129
Marta Montserrat (2021) Tell us how you can be, and we’ll make you better: exploiting genetic variability in personality traits to improve top-down control of agricultural pests. Peer Community in Ecology, 100069. 10.24072/pci.ecology.100069
Evaluation round #1
DOI or URL of the preprint: 10.1101/2020.08.21.257881
Author's Reply, 10 Dec 2020
Decision by Marta Montserrat, 29 Oct 2020
In the preprint presented by Lartigue et al. the authors introduce a novel perspective for the genetic improvement of Biological Control Agents (BCAs) based on behavioral traits that relate to the performance of individuals as BCAs, and that define the personality of individuals. The authors propose the genetic improvement of personality traits to be used as tool to create highly performant BCAs.
The idea is novel and the manuscript has potential to contribute significantly to agricultural sciences and to the development of new strategies to improve pest control with methodologies that are respectful with the environment and the human health.
Yet, in my opinion, the potential success for using behavioral traits to breed natural enemies is likely to be severely hampered by the extremely low heritability values (<0.1) found in most of the behavioral traits and the two personality scores. This is a severe drawback that the authors need to address, not only by acknowledging the limitations of their strategy (as they do in the last paragraph of the discussion) but by offering real solutions, or convincing ways, to overcome this drawback, if only to convince the reader that introducing the genetic improvement of personalities in the biological pest control programs is realistic and feasible.
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