Interplay between insects and plants: dynamic and complex interactions that have coevolved over millions of years but act in milliseconds

Journal of Experimental Botany, Vol. 66, No. 2 pp. 455–465, 2015 doi:10.1093/jxb/eru391 Advance Access publication 30 September, 2014 Review Paper Interplay between insects and plants: dynamic and complex interactions that have coevolved over millions of years but act in milliseconds Toby J. A. Bruce* Rothamsted Research, Harpenden, Herts AL5 2JQ, UK Received 19 May 2014; Revised 26 August 2014; Accepted 28 August 2014 Abstract In an environment with changing availability and quality of host plants, phytophagous insects are under selection pressure to find quality hosts. They need to maximize their fitness by locating suitable plants and avoiding unsuitable ones. Thus, they have evolved a finely tuned sensory system, for detection of host cues, and a nervous system, capable of integrating inputs from sensory neurons with a high level of spatio-temporal resolution. Insect responses to cues are not fixed but depend on the context in which they are perceived, the physiological state of the insect, and prior learning experiences. However, there are examples of insects making ‘mistakes’ and being attracted to poor quality hosts. While insects have evolved ways of finding hosts, plants have been under selection pressure to do precisely the opposite and evade detection or defend themselves when attacked. Once on the plant, insect-associated molecules may trigger or suppress defence depending on whether the plant or the insect is ahead in evolutionary terms. Plant volatile emission is influenced by defence responses induced by insect feeding or oviposition which can attract natural enemies but repel herbivores. Conversely, plant reproductive fitness is increased by attraction of pollinators. Interactions can be altered by other organisms associated with the plant such as other insects, plant pathogens, or mycorrhizal fungi. Plant phenotype is plastic and can be changed by epigenetic factors in adaptation to periods of biotic stress. Space and time play crucial roles in influencing the outcome of interactions between insects and plants. Key words: Chemical ecology, coevolution, herbivores, insect–plant interactions, pollinators, spatio-temporal dynamics. Introduction The purpose of this review is to consider the important role played by time and space in insect–plant interactions. Great advances are being made in understanding the mechanistic basis by which insects interact with their host plants (reviewed by Hogenhout and Bos, 2011; Mithoefer and Boland 2012; Smith and Clement, 2012). The ecological and evolutionary context of these interactions requires consideration because they are dynamic and what occurs at one point in time may not occur at another. Insects are programmed to recognize and rapidly respond to patterns of host cues. Particularly specialist insect species have to find specific plant species on which they can feed and reproduce (host plants) among plant species that do not support feeding and/or reproduction of the insects (non-host plants). Thus, in an environment with changing availability and quality of host plants, phytophagous insects are under selection pressure to find quality hosts (Bruce et al., 2005). To maximize their fitness they need to locate suitable plants and avoid unsuitable hosts (Bruce and Pickett, 2011). Thus, they have evolved a finely tuned sensory system for detection of host cues and a nervous system capable of integrating inputs from sensory neurons with a high level of spatio-temporal resolution (Martin et al., 2011). Time and space also influence plant responses to insects; for example, a history of pre-exposure can prime plant defence responses so that plants respond more quickly and strongly when they are attacked again (Ton et al., 2007, Jinwon et al., 2011). © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: * To whom correspondence should be addressed. E-mail: 456 | Bruce Coevolution The huge number species of flowering plants on our planet (approximately 275 000) is thought to be the result of adaptive radiation driven by the coevolution between plants and 4. induced defence hours 3. settlement/colonisation minutes 2. host plant decisions made in flight (land or not?) 1. coevolution of plants and insects milliseconds 400 million years Fig. 1. The different timescales associated with insect–plant interactions. The timescale over which mechanisms have evolved is very long whereas the actual mechanisms themselves operate over much shorter periods. their beneficial animal pollinators (Yuan et al., 2013). The fossil record shows that pollination originated 250 million years ago (Labandeira, 2013). Some plants have evolved with their pollinators and produce olfactory messages which make them unique for their specific pollinators (Grajales-Conesa et al., 2011). For example, certain orchid flowers mimic aphid alarm pheromones to attract hoverflies for pollination (Stoekl et al., 2011). Furthermore, insect herbivores can drive real-time ecological and evolutionary change in plant populations. Recent studies provide evidence for rapid evolution of plant traits that confer resistance to herbivores when herbivores are present but for the evolution of traits that confer increased competitive ability when herbivores are absent (Agrawal et al., 2012; Hare, 2012; Züst et al., 2012). While phytophagous insects have been adapting to exploit their hosts, the plants have simultaneously been evolving defensive systems to counteract herbivore attack (Anderson and Mitchell-Olds, 2011; Johnson, 2011). Studies of fossil plant–insect associations suggest that insects have been feeding on plants for 400 million years (Labandeira, 2013). Coevolution between insects and plants was drawn attention to in the classic review by Erhlich and Raven (1964). Thus, the phenotypic traits and interactions we see today are the legacy of a long history of association between the organisms and reciprocal adaptations that provide fitness advantages (Gomez et al., 2010). There is a trend for phytophagous insects to become more specialized in host plant use over time, although some important agricultural pest species are polyphagous. Ecological specialization involves subtle and complex interplay between species and is not limited to the plant and the herbivore but can also be influenced by multitrophic interactions (Forister et al., 2012). There can also be bidirectionality in transitions between generalist and specialist lineages and Janz and Nylin (2008) have proposed an oscillation hypothesis in which periods of host range expansion are followed by periods of specialization, as seen in the leaf-mining fly genus Phytomyza. Divergent selection exerted on ecological traits may result in adaptive population differentiation and reproductive isolation, and affect differentially the level of genetic divergence along the genome (Jaquiery et al., 20 (...truncated)