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Variation in Insect Herbivore Communities on Individual Plants Reveals Phylogenetic Signal in 2 Uncertainty of Attack in Brassicaceae

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Variation in Insect Herbivore Communities on Individual Plants Reveals Phylogenetic Signal in 2 Uncertainty of Attack in Brassicaceae bioRxiv preprint doi: https://doi.org/10.1101/2020.12.06.413724; this version posted December 7, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Variation in insect herbivore communities on individual plants reveals phylogenetic signal in 2 uncertainty of attack in Brassicaceae 3 4 Daan Mertens1*, Klaas Bouwmeester2 and Erik H. Poelman1 5 1 Laboratory of Entomology, Wageningen University and Research, P.O. Box 16, 6700 AA, 6 Wageningen, The Netherlands. 7 2 Biosystematics Group, Wageningen University and Research, P.O. Box 16, 6700 AA, 8 Wageningen, The Netherlands. 9 10 11 12 * Correspondence: Daan Mertens 13 Email: [email protected] | [email protected] | [email protected] 14 ORCID ID: DM. 0000-0003-4220-9075; KB. 0000-0002-8141-3880; EHP. 0000-0003-3285- 15 613X 16 17 18 19 20 21 22 23 Keywords 24 Plant defence strategies; predictability; ecological interaction networks; cabbage and mustard 25 family; co-evolution 26 27 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.06.413724; this version posted December 7, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 28 Abstract 29 As a result of co-evolution between plants and herbivores, related plants often interact with 30 similar communities of herbivores. On individual plants, typically only a subset of interactions 31 is realized. The stochasticity of realized interactions leads to uncertainty of attack on individual 32 plants and is likely to determine adaptiveness of plant defence strategies. Here, we show that 33 across 12 plant species in two phylogenetic lineages of the Brassicaceae, variation in realized 34 herbivore communities reveals a phylogenetic signal in the uncertainty of attack on individual 35 plants. Individual plants of Brassicaceae Lineage II were attacked by a larger number of 36 herbivore species from a larger species pool, resulting in a higher uncertainty of realized 37 antagonistic interactions compared to plants in Lineage I. We argue that uncertainty of attack 38 in terms of realized interactions on individual plants is ecologically relevant and must therefore 39 be considered in the evolution of plant defences. 40 41 Introduction 42 Over their lifetime, plants interact with numerous organisms of which many are herbivorous. 43 In addition to a mixture of environmental effects such as host plant community composition 44 and abiotic conditions, the set of antagonistic interaction partners of a plant species is strongly 45 determined by selection pressures and phylogenetic history (Morales-Castilla et al. 2015, 46 Hutchinson et al. 2017). Insect herbivores may exert selection that promotes novel defence 47 strategies in plants and these events often coincide with radiation of herbivore species that have 48 counteradaptations to these novel defences (Edger et al. 2015). Even though the relationship 49 between plant phylogenetic distance and overlap in herbivore communities is variable across 50 plant clades, co-evolutionary processes often result in non-random structuring of plant- 51 associated antagonist communities (Bergamini et al. 2017, Rapo et al. 2019, Cirtwill et al. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.06.413724; this version posted December 7, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 52 2020). 53 However, these macro-evolutionary patterns are generally described for the full potential 54 pool of antagonist species interacting with a plant species, whereas natural selection by these 55 antagonists acts on the level of plant individuals. In many plant species, there is a discrepancy 56 between the full potential of antagonistic interaction partners at the plant species level and the 57 subset of realized interactions for individual plants (Lewinsohn et al. 2005, Kuppler et al. 2016). 58 The subset of antagonists actually colonizing individual plants is determined by intraspecific 59 variation in plant traits (Barbour et al. 2015, Barbour et al. 2018), variation in functional traits 60 across antagonist species or individuals (Zytynska and Preziosi 2013), priority effects in 61 community assembly in which a first colonizer affects the likelihood of attack by other 62 antagonists (Lill and Marquis 2003, Stam et al. 2018), environmental heterogeneity and habitat 63 filtering (Johnson and Agrawal 2005, Agrawal and Fishbein 2006, Violle et al. 2012), as well 64 as stochastic processes (Shoemaker et al. 2020). Moreover, plant species may differ in the 65 relative proportion of realized interactions per individual plant out of the full antagonist species 66 pool and thus differ in the uncertainty of which antagonists attack individual plants. For 67 example, plant species that interact with a larger species pool of herbivores face a larger number 68 of potential herbivore species at the level of individual plants, possibly resulting in a larger 69 uncertainty of realized interactions. At the same time, the uncertainty of interactions 70 experienced by individual plants is determined by both the proportion as well as the absolute 71 number of realized interactions and dominance of interactions by key herbivore species. The 72 uncertainty of attack on individual plants is a major component of theories on plant defence 73 plasticity (Poelman and Kessler 2016, Salazar et al. 2016b, Karban 2019). Plants evolved 74 inducible defences that are activated upon recognition of attack to save metabolic costs 75 associated with production and maintenance of defence when herbivores are absent (Meldau et 76 al. 2012). Plasticity in defence also allows plants to tailor defences to specific antagonists and 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.06.413724; this version posted December 7, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 77 to integrate responses to multiple attackers (Van der Ent et al. 2018). Variation across plant 78 species in the uncertainty of attack may strongly impact the evolution of such plastic defence 79 strategies. It is to be expected that related plant species face more similar levels of uncertainty 80 in their interactions as closely related plant species tend to interact with herbivore communities 81 that are similar in composition (Agosta 2006, Agrawal and Fishbein 2006, Futuyma and 82 Agrawal 2009). However, it is unknown whether phylogenetic signals in uncertainty of 83 community composition or structure on individual plants exist. Understanding how the overall 84 uncertainty of interactions that plants experience varies within and among plant species can 85 provide valuable insights in the evolutionary history of defence strategies (Violle et al. 2012, 86 Ohgushi 2016, Salazar et al. 2016a, Stam et al. 2018). 87 To determine phylogenetic signals in plant-herbivore community composition and explore 88 variation in uncertainty of realized interactions across plant individuals, we compare insect 89 herbivore community characteristics among 12 Brassicaceae species, belonging to two major 90 phylogenetic lineages (Lineage I and Lineage II) within this family. We hypothesize that the 91 composition of the herbivore community with which plants interact correlates with plant 92 phylogeny, and that this phylogenetic signal is retained in the uncertainty of realized 93 interactions on individual plant level. We explicitly test whether plant phylogenetic distance 94 predicts i) the species richness, diversity and the proportion of realized interactions on 95 individual plants out of the full potential herbivore community as a measure of uncertainty of 96 attack on individual plants, and ii) the similarity in the average herbivore community 97 composition and structure on individual plants within a species. We subsequently test whether 98 the phylogenetic signal correlates with similarity in plant growth traits. We then evaluate which 99 evolutionary models best predict phylogenetic signals in herbivore community diversity and 100 uncertainty of attack in Brassicaceae and discuss its consequences for the evolution of plant 101 defences. 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.06.413724; this version posted December 7, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 102 Results 103 Plant phylogeny structures the number and proportion of realized interactions on individual 104 plants 105 By repeatedly monitoring insect herbivore communities during the life span of individual 106 plants of 12 annual Brassicaceae species (Supplementary File 1 Table A, Supplementary Fig. 107 1), we identified that the network of insect herbivores interacting with the 12 plant species was 108 strongly connected (Fig. 1). Overall, both
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