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Know Your Enemy Genomes of biological control agents Know Your Enemy: Know Your Enemy: Genomes of biological control agents Kim B. Ferguson Kim B. Ferguson 2020 KNOW YOUR ENeMy: GeNOMeS OF BIOLOgICAL CONTROL AgeNTS KIM B. FeRgUSON THESIS COMMIttEE Promotor Prof. Dr B. J. Zwaan Professor of Genetics Wageningen University & Research Co-promotors Dr B. A. Pannebakker Assistant professor, Laboratory of Genetics Wageningen University & Research Dr E. C. Verhulst Assistant professor, Laboratory of Entomology Wageningen University & Research Other Members Prof. Dr M. M. van Oers, Wageningen University & Research Dr Y. H. Chen, University of Vermont, USA Prof. Dr J. Ellers, Vrije Universiteit Amsterdam Prof. Dr B. Wertheim, University of Groningen This research was conducted under the auspices of the C. T. de Wit Graduate School for Production Ecology and Resource Conservation. KNOW YOUR ENeMy: GeNOMeS OF BIOLOgICAL CONTROL AgeNTS KIM B. FeRgUSON THESIS Submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus, Prof. Dr A. P. J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Wednesday 25 March 2020 at 4:00 PM in the Aula. Kim B. Ferguson Know Your Enemy: Genomes of biological control agents 312 pages PhD Thesis, Wageningen University, Wageningen, The Netherlands (2020) With references, with summary in English, Dutch, German, and Spanish ISBN 978-94-6395-281-1 DOI 10.18174/511993 Table of Contents CHAPTeR 1: Introduction 7 CHAPTeR 2: Genetic variation of traits in natural enemies relevant for biological control: a systematic review 29 CHAPTeR 3: Effect of mass rearing on the genetic diversity of the predatory mite Amblyseius swirskii 67 CHAPTeR 4: Braconidae revisited: Bracon brevicornis genome showcases the potential of linked-read sequencing in identifying a putative complementary sex determiner gene 91 CHAPTeR 5: Hybrid genome assembly and annotation of egg parasitoid and biological control agent Trichogramma brassicae 109 CHAPTeR 6: The wasp and the butterfly: opulation genetics and genomics of Trichogramma evanescens hint at role of phoresy in dispersal 129 CHAPTeR 7: Jekyll or Hyde? The genome (and more) of Nesidiocoris tenuis, a zoophytophagous predatory bug that is both a biological control agent and a pest 163 CHAPTeR 8: Synthesis 211 APPeNDICeS 235 References 236 Summary 280 Summary in Dutch, German, and Spanish 285 Acknowledgements 303 About the Author 307 List of Publications 308 PE&RC Training and Education Statement 309 About the Artwork 310 Chapter 1 Introduction Kim B. Ferguson 7 Chapter 1 To whom, dear Muse, do you bring these varied fruits of song, or who was it who wrought this garland of poets?1 ANtHOLOGIES The root of the English word “anthology” is interesting2, as its meaning is two- fold in the original Greek: anthologia (‘a gathering of flowers’) andanthologiai (‘a collection of epigrams’) (Beal, 2008). Meleager of Gadara (in modern- day Jordan) is credited with creating the first anthology in approximately 100 B.C.E., though the original has been lost for many centuries (Gutzwiller, 1997). Meleager collected epigrams– a type of short and pithy Greek prose– from various well-known poets, as well as his own, and put them all into one binding. The goal was to bring attention to the works that, in Meleager’s eyes, were the best and most deserving of praise. Comparing each poet to a flower, he created a “garland” out of these works, and so this work came to be known as Meleager’s Garland. The Garland became the only source for many of these poems, and was itself placed within a larger anthology, the Anthologia Palatina. While earlier modern critics of Greek poetry and literature viewed Meleager as unoriginal and overblown, more recent critics see him as more of a very intentional and creative editor. The structure of the Garland also includes two epigrams that are deliberately set outside the rest of the collection and function as introduction and epilogue. Moving into present day, anthologies are collections of works of one or more authors, often on a specific theme or genre (Beal, 2008). Perhaps the most well-known is the Norton set of anthologies, a perennial occupant of North American university libraries and textbook stores (Donadio, 2006). Modern anthologies serve as an accessible yet intentional collection of works and can extend beyond literature. One such example is the ambitious Environment: An interdisciplinary anthology, a collection of various essays and articles with sources across sciences, life sciences, and humanities on the theme of the 1 from Meleager’s Garland, AP 4.1, sourced from http://www.attalus.org/poetry/meleager.html with number references to the original Anthologia Palatina 2 Also interesting is that while Dutch usage switches between anthologie and bloemlezing, both come from the same root idea, but in different languages: Greek and Latin (florilegium), respec- tively (van der Sijs). 8 Introduction environment (Adelson et al., 2008). 1 In many ways, a doctoral thesis is an anthology. It is specific to a theme (the project of the doctoral candidate), often includes multiple authors (co- authors on each chapter or publication) and contains both an introduction (this chapter) as well as an epilogue (the synthesis), similar to Meleager’s Garland and other contemporary iterations. The goal then, of this introduction, is simple: to convince you, the reader, that this anthology is of immediate interest to you, both in terms of its varied chapters but also as a unified whole. To do so, I will first introduce two fields in biology that thus far have mostly run in parallel: biological control and genetics/genomics. BIOLOGIcaL cONtROL Biological control, also known as biocontrol, is the introduction of one organism to control the population of another organism. The practice of releasing these “natural enemies” has been in practice for nearly as long as agriculture in some form (van Lenteren and Godfray, 2005), but has been commercially formalised for over 120 years, with a sharp increase in commercial and economic presence in the last two decades (van Lenteren, 2012). Both types of pests and biological control agents (BCAs) available to use against them run the gamut: microbes, plants, nematodes, arthropods, mammals, birds, et cetera. Here, I will narrow the focus to arthropod pests and their arthropod BCAs, as these are the focus of my thesis. TYPES OF bIOLOGIcaL cONtROL Biological control is typically divided into three categories: conservation, classical, and augmentative. Conservation biological control is about protecting the habitat necessary for natural enemies to thrive and often extends beyond agricultural fields. It is closely related to ecosystem management, and is often happening at the level of large, outdoor landscapes. One example of conservation biological control would be maintaining hedges on the edge of an outdoor tomato field in order to promote a buffer zone for predators and parasitoids against tomato pests (Balzan et al., 2015). 9 Chapter 1 Classical biological control, the more (in)famous of the three, is typically what the general public and biologists alike think of when they hear “biological control.” This is where a foreign parasitoid or predator is released against a pest (which can be foreign or native, but most often is foreign). The idea here is that if existing natural enemies in the affected environment have not been able to deal with the invasive pest, the natural enemy that keeps the pest in check in the place of origin could be the solution. The first successful account of classical biological control is often cited as the importation of the vedalia beetle, Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae) from Australia to control the cottony cushion scale, Icerya purchasi (Maskell) (Hemiptera: Margodidae) in California, USA in 1899 (Caltagirone and Doutt, 1989; Mason et al., 2017). The success of the vedalia beetle was recognised by Australia in stamp form in 2003 (Figure 1) (“Cardinal Ladybird (Rodalia cardinalis),” 2019). In turn, the infamy of classical biological control comes from ecological catastrophes that have occurred, such as the well-known cane toad, Rhinella (Bufo) marinus (L.) (Amphibia: Anura), situation in Australia. Australia was not the first country where the cane toad was introduced, nor was it the last, but it was certainly the most studied introduction from the first half of the 20th century (Easteal, 1981). It was brought in as predator of the cane beetle, Dermolepida albohirtum (Waterhouse) (Coleoptera: Scarabaeidae), one of the main agricultural pests of Australian sugar cane. Over time, the cane toad extended beyond the expected range, led to the decline of several native predators, and also did not do a good job of controlling the pest (Doody et al., 2009). Problem species, such as the cane toad in Australia, are no longer referred to as “biological control agents” but rather “invasive species,” despite long-term establishment being a goal of classical biological control. The whole world has not turned their back on the cane toad, however, as in Barbados it was honoured with its own stamp in 1989, following a successful introduction sometime in the early half of the 19th century (Easteal, 1981) (Figure 1) (“Cane Toad (Bufo marinus),” 2019). Due to a number of unintended consequences such as the establishment of toxic toads in Australia, the importation of non- native species for classical biological
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