bioRxiv preprint doi: https://doi.org/10.1101/2020.06.24.168112; this version posted June 24, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-NC 4.0 International license. 1 1 Stressful times in a climate crisis: how will aphids respond to more 2 frequent drought? 3 Running title: Aphid-plant interactions under drought stress 4 Daniel J Leybourne 1,2,3Ŧ, Katharine F Preedy 4, Tracy A Valentine 2,, Jorunn IB Bos 1,3 & 5 Alison J Karley 2* 6 1 Division of Plant Science, School of Life Science. Dundee University, Dundee. UK 7 2 Ecological Science, The James Hutton Institute. Invergowrie, Dundee. UK 8 3 Cell and Molecular Science, The James Hutton Institute. Invergowrie, Dundee. UK 9 4 Biomathematics and Statistics Scotland. Invergowrie, Dundee. UK 10 Ŧ Current address: ADAS High Mowthorpe, Duggleby, Malton, North Yorkshire, YO17 8BP, 11 UK 12 * Author for correspondence 13 Funding 14 DJL was funded by the James Hutton Institute and the Universities of Aberdeen and Dundee 15 through a Scottish Food Security Alliance (Crops) PhD studentship. The James Hutton 16 Institute is supported by the Scottish Government Rural and Environment Science and 17 Analytical Services. 18 Author contributions 19 AJK, DJL, and KFP conceived and designed the study. DJL extracted and analysed the 20 data, with input from KFP. All authors contributed to data interpretation. DJL wrote the 21 manuscript with input from all authors. All authors read and approved the final manuscript. 22 Conflict of interest 23 The authors declare no conflict of interest. 24 25 26 27 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.24.168112; this version posted June 24, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-NC 4.0 International license. 2 28 Abstract 29 Aphids are a common and widely distributed group of phloem-feeding insects and are 30 abundant components of insect communities in natural and managed ecosystems. It is 31 anticipated that a changing climate will lead to more frequent periods of drought, which will 32 have consequences for the biology and ecology of these ubiquitous species and the 33 foodwebs they support. To date there has been no comprehensive assessment of the 34 literature to determine the extent to which drought negatively affects aphid fitness. For the 35 first time, we qualitatively and quantitatively assess the literature to determine whether 36 drought stress has an overall negative, positive, or null effect on aphid fitness in terms of 37 development, fecundity, survival and abundance. The underlying causes of changes in 38 aphid fitness are assessed by examining measures of plant growth, nutrition, and defence 39 in relation to the predictions of the plant vigour hypothesis. The meta-analysis indicates that 40 aphid fitness is typically reduced under drought stress, and this is mediated by a reduction 41 in plant vigour and an increase in allocation to defence in drought-stressed plants. We 42 discuss the ecological consequences of increased drought frequency for aphid success, 43 plant resistance against aphids, and aphid-trophic interactions in natural and agricultural 44 systems. 45 46 47 48 49 50 51 52 53 54 55 56 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.24.168112; this version posted June 24, 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-NC 4.0 International license. 3 57 Introduction 58 The changing climate is anticipated to lead to decreased annual levels of precipitation in 59 some regions, resulting in extended periods of drought (Blenkinsop & Fowler 2007; Santos 60 et al., 2016). For areas which do not regularly experience prolonged periods of water 61 deprivation, such as temperate regions, prolonged drought conditions can have severe 62 consequences on plant physiology, often leading to reduced growth and photosynthetic 63 capacity (Osakabe et al., 2014; Zeppel et al., 2014). Changes in plant physiology in 64 response to drought stress can directly influence the population dynamics, fitness, 65 phenology, and biology of herbivorous insects (Huberty & Denno 2004; Mody et al., 2009; 66 Aslam et al., 2013), with consequences that cascade through trophic networks (Johnson et 67 al., 2011; Rodríguez‐Castañeda 2013). 68 Previous meta-analyses have examined drought effects by comparing responses of 69 herbivorous insect species with different feeding strategies (Huberty & Denno 2004). To 70 date, however, there has been no comprehensive assessment of drought effects on a 71 specific herbivore group and the underpinning causes due to physiological changes in the 72 host plant. Aphids are phloem-feeding insects of global ecological importance due to their 73 near-worldwide distribution, ability to colonise most habitat types, and capacity to vector 74 plant viruses (Van Emden & Harrington 2017). There are over 4400 known species of aphid 75 (Blackman & Eastop 2000) and many of these are major agricultural and horticultural pests, 76 making them an economically important group of herbivorous insects. Aphids are abundant 77 components of insect communities in diverse ecosystems across the globe (Messelink et 78 al., 2012; Roubinet et al., 2018). In many ecosystems, aphids sustain several higher trophic 79 groups, including the primary consumers of aphids, such as parasitoid wasps, spiders, 80 ladybirds, and carabid beetles (Staudacher et al., 2016), the higher-level consumers of these 81 aphid natural enemies, such as hyperparasitoids (Traugott et al., 2008; Lefort et al., 2017), 82 small mammals and birds, and a range of entomological pathogens and parasites (Hagen 83 & van den Bosch 1968). Examining how climate change, including drought, might influence 84 aphid fitness is a major avenue of current research, specifically with regards to examining 85 how this might affect the productivity and functioning of agricultural, horticultural, and natural 86 vegetation systems (Romo & Tylianakis 2013; Teixeira et al., 2020) 87 The effect of drought stress on aphid fitness has been investigated experimentally across 88 many aphid-plant systems (Pons & Tatchell 1995; Agele et al., 2006; Mody et al., 2009; 89 Aslam et al., 2013; Grettenberger & Tooker 2016; Foote et al., 2017), with numerous studies 90 indicating that aphids are negatively affected by drought stress. To date, there has been no bioRxiv preprint doi: https://doi.org/10.1101/2020.06.24.168112; this version posted June 24, 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-NC 4.0 International license. 4 91 comprehensive analysis of the causes of decreased aphid fitness under drought stress, 92 although several studies suggest that it is mediated through reduced plant fitness (Hale et 93 al., 2003; Banfield-Zanin & Leather, 2015; Dai et al., 2015). Two meta-analyses conducted 94 in recent decades provide context for constructing a hypothesis to explain variation in aphid 95 fitness under water stress in relation to plant fitness. First, Huberty & Denno (2004) assessed 96 the responses of herbivorous insects from different feeding guilds to drought stress 97 conditions and found limited evidence for the plant stress hypothesis (i.e. enhanced insect 98 performance on water-stressed host plants due to increased tissue nitrogen availability: 99 White, 1969) amongst sap-feeding insects (phloem and mesophyll feeders); conversely, 100 their analysis showed that drought stress typically has negative effects on herbivorous insect 101 fitness and abundance. Second, Cornelissen et al., (2008) examined insect fitness in 102 relation to plant vigour and demonstrated that sap-feeding insects are more abundant and 103 show increased fitness when feeding on more vigorously growing plants or plant tissues. 104 These findings lead us to hypothesise that the effects of drought stress on aphid fitness and 105 abundance are driven by decreased plant vigour rather than stress-related changes in plant 106 nutritional quality. 107 Although the majority of studies have reported reduced aphid fitness when exposed to 108 drought stressed host plants (Banfield-Zanin & Leather, 2015; Dai et al., 2015; Foote et al., 109 2017), several studies have reported null (Mewis et al., 2012) and positive (Oswald & 110 Brewer, 1997) effects. Multiple factors could explain these contrasting observations, 111 including differences in aphid or plant biology. Indeed, in the study by Oswald & Brewer 112 (1997) a positive effect of drought stress on aphid fitness was detected in the Russian wheat 113 aphid, Diuraphis noxia, and a negative effect was reported for the corn leaf aphid, 114 Rhopalosiphum maidis. Although both of these species are cereal-feeding aphids, D. noxia 115 and R. maidis belong to two distinct aphid tribes, the Macrosiphini and the Aphidini, 116 respectively (Kim & Lee, 2008; Choi et al., 2018). The findings of Oswald and Brewer (1997) 117 suggest that differences in aphid biology and/or life history could underlie contrasting 118 responses to drought stress. Additionally, the specific aphid-plant combination could further 119 influence the effects of drought stress on aphid fitness. For example, multiple aphid species 120 exhibit contrasting responses to drought stress on a common plant host (Mewis et al., 2012) 121 and a single aphid species can display contrasting responses to drought stress on several 122 related host plant species (Hale et al., 2003). These findings suggest that the specific aphid- 123 plant combination could be a key factor in mediating aphid responses to drought stress, with 124 differences likely to be driven by plant species-specific responses to drought (i.e.