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Odonata (Dragonflies and Damselflies) As a Bridge Between Ecology and Evolutionary Genomics Seth Bybee1* , Alex Córdoba-Aguilar2, M

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Odonata (Dragonflies and Damselflies) As a Bridge Between Ecology and Evolutionary Genomics Seth Bybee1* , Alex Córdoba-Aguilar2, M Bybee et al. Frontiers in Zoology (2016) 13:46 DOI 10.1186/s12983-016-0176-7 REVIEW Open Access Odonata (dragonflies and damselflies) as a bridge between ecology and evolutionary genomics Seth Bybee1* , Alex Córdoba-Aguilar2, M. Catherine Duryea3, Ryo Futahashi4, Bengt Hansson3, M. Olalla Lorenzo-Carballa5, Ruud Schilder6, Robby Stoks7, Anton Suvorov8, Erik I. Svensson3, Janne Swaegers7, Yuma Takahashi9, Phillip C. Watts10 and Maren Wellenreuther3,11 Abstract Odonata (dragonflies and damselflies) present an unparalleled insect model to integrate evolutionary genomics with ecology for the study of insect evolution. Key features of Odonata include their ancient phylogenetic position, extensive phenotypic and ecological diversity, several unique evolutionary innovations, ease of study in the wild and usefulness as bioindicators for freshwater ecosystems worldwide. In this review, we synthesize studies on the evolution, ecology and physiology of odonates, highlighting those areas where the integration of ecology with genomics would yield significant insights into the evolutionary processes that would not be gained easily by working on other animal groups. We argue that the unique features of this group combined with their complex life cycle, flight behaviour, diversity in ecological niches and their sensitivity to anthropogenic change make odonates a promising and fruitful taxon for genomics focused research. Future areas of research that deserve increased attention are also briefly outlined. Keywords: NGS, Ancient insects, Complex life cycle, Naiad, Climate change, Polymorphism, Flight, Ecological Genomics Background Dragonflies and damselflies (Insecta: Odonata) repre- With more than 1,000,000 species described and an esti- sent a species rich, yet tractable (~6000 described spe- mated 5,000,000 extant species, insects represent the cies, [7]) insect order, which encompasses two main most diverse animal taxon on Earth [1, 2]. They inhabit suborders, Anisoptera (dragonflies) and Zygoptera (dam- key roles as herbivores, pollinators, seed dispersers, selflies). The former are generally larger and alight with predators, detritivores and vectors, thereby contributing their wings held out to the sides, while damselflies have to the core biological foundation of all terrestrial ecosys- slender bodies, and generally hold their wings over the tems [3, 4]. Insects are also of exceptional economic im- abdomen when at rest. Here we will use the term odon- portance as providers of essential ecosystem services ate as the inclusive terms when referring to both subor- (e.g. global economic value of US$153 billion of insect ders. Several characteristics make odonates an attractive pollination in 2005, [5]), pests in agricultural landscapes group to combine ecology with evolutionary genomics. (e.g. annual control of the diamondback moth Plutella First, they are direct descendants of one of the most an- xylostella costs US$4–5 billion, [6]) and as vectors of cient winged insect groups and, along with Ephemerop- diseases affecting humans (e.g. malaria control costs ~ tera (mayflies), are sister to all other neopteran insects US$12 billion annually, Centre for Disease Control). [8]. Second, odonates incorporate rich phenotypic and ecological diversity in one single insect order and there- fore constitute excellent candidates for ecological and * Correspondence: [email protected] evolutionary studies [9]. As such, they have been used Seth Bybee, Phillip Watts and Maren Wellenreuther are Senior authors extensively as model species in many areas of ecology 1Brigham Young University, Provo, UT 84606, USA Full list of author information is available at the end of the article and evolution, such as sexual selection, behaviour, © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Bybee et al. Frontiers in Zoology (2016) 13:46 Page 2 of 20 evolution of flight and life history theory [9]. Third, the evolutionary processes within the group, but also add group shows several evolutionary innovations, particu- fundamental insights across insects. In this review, we larly with regard to flight (e.g. direct flight musculature), outline the central research importance of Odonata vision (e.g. complex colour vision,) sexual behaviour (e.g. by presenting some of the key features that make this secondary genitalia), and life history (e.g. complex life group an unparalleled model system to integrate gen- cycle). Fourth, the large interspecific variation in habitat omics with ecology and evolution. We synthesize the specificity and complex aquatic/terrestrial life cycles work conducted on the evolution, ecology and physi- makes odonates prominent surrogates for evaluating all ology of odonates, as well as the contemporary re- types of freshwater ecosystems worldwide [10]. Lastly, search showing that they are amenable study species dragonflies and damselflies are comparatively large in- to quantify responses to anthropogenic change, to in- sects, both as adults and late-instar larvae, and as such form conservation efforts. We focus specifically on their behaviours can be studied readily in the wild. Thus, those areas where the integration of genomics with the phylogenetic position of odonates, combined with ecology and evolution would yield significant insights their numerous evolutionary innovations make them an into evolutionary dynamics that would not be easily attractive model to bridge ecology with contemporary gained by working on other animal groups. Finally, evolutionary genomics and can provide fundamental in- we outline future areas of research that deserve in- sights into the origin of these traits. Despite the attract- creased attention. iveness of this group for evolutionary genomics studies, efforts have been lagging behind other insect orders (see Taxonomy and phylogenetic position Table 1 for a summary of current genomic resources for Dragonflies and damselflies (Fig. 1a, [8]) are extant rep- Odonata). resentatives of the first ancient winged insects. Their At present, most genomic resources for arthropods are phylogenetic position makes this group of central im- available for dipteran flies [e.g. the many Drosophila spe- portance to comparative studies on the evolution of gen- cies, http://flybase.org/static_pages/species/sequenced_- omic innovations involved in the origins of physiological species.html], lepidopterans (e.g. moths and butterflies, processes (e.g. flight, colour vision, and metabolism) and [11]) and hymenopterans (e.g. wasps and bees, [12]). To life history strategies (e.g. predation, mating, dispersal, some extent, this taxonomic bias is caused by the large and complex life cycles). Thus, a tractable and large- economic and/or medical importance of these groups scale phylogeny would provide a rigorous framework to and in some cases because they serve as key laboratory quantify evolutionary changes in genome architecture models [13]. However, while it is true that model species and provide insight on the origin of evolutionary innova- provide numerous insights into key molecular and evo- tions in odonates and insects in general. lutionary processes, they do not necessarily capture es- Over the past 20 years, much progress towards sential parts of the biology and ecology of their relatives, reconstructing the phylogeny of Odonata has been especially in the case of those species that are more dis- made [8, 19–23]. Noteworthy, efforts to construct a tantly related. By casting a small net for insect genomic detailed classification scheme based on the solid resources, only a partial picture of insect adaptation is phylogenetic support of suborders and families, albeit formed. Moreover, a focus on a few model organisms some branches still show low support and conflict could promote a confirmation bias - a “tendency to see among families [19, 20, 24–26]. A key limitation of what we expect to see” [14]. Conversely, research into these studies is their reliance on a small set of loci diverse taxa will contribute new knowledge to the for phylogenetic reconstruction [25, 27]. More robust current “omics” (e.g. genomics and transcriptomics) era. results are likely to be found with genomic ap- Such an approach offers insights into molecular adaptive proaches for phylogenetic estimation [28, 29], but be- processes that occur at contemporary and phylogenetic fore these tools can be properly designed and utilized timescales and are of relevance to ecosystem functioning to quantify phylogenetic relationships within Odonata, and stability [15–17]. genome-level data are necessary. One goal of the Recent advances in high-throughput sequencing 1KITE project [8] is to produce transcriptomes of 107 technologies make it possible to generate large odonate species (representing roughly half of the amounts of sequence data from virtually any organ- family-level diversity), which will provide the first “big ism, at a rapid rate and at relatively low cost [18]. data” estimates of the phylogeny of the group and ad-
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