Odonata (dragonflies and damselflies) as a bridge between ecology and evolutionary genomics

Fossil record

Odonates have one of the most complete and well-preserved fossil records among insects (Fig. 2). The Protodonata represent a fossil crown group to the extant Odonata and first appeared in the Namurian of the Carboniferous around 319,000,000 years ago). Protodonate fossils show evidence of many important traits that are still exhibited by extant odonates, such as an aquatic immature stage, a complex life cycle [34], and the complex mating system that typifies this group (i.e. males use secondary genitalia to transfer sperm, see also section 2E, [35]). The earliest fossils that are recognized as “modern” odonates date to ~268 Mya from the Upper Permian (Saxonagrion minutus, [36]) soon after which several stem group fossils for each of the modern suborders appeared, representing many of the families and even some modern genera. The extensive fossil record for several contemporary odonate groups, in combination with information of their relative ages from genomic data, offers the prospect of a thorough integration between the fossil record and contemporary studies of evolutionary biology that will help to shed significant light on many evolutionary questions. For example, insect flight is particularly intriguing as it likely evolved only once [37], and the anatomical regions from which wings evolved among the early insects are as yet unknown. A combination of genomic resources, fossils and evolutionary development approaches may help to identify the genetic toolkit responsible for insect flight, as well as the loci associated with key innovations during the evolution of wing morphology as different odonate species diversified and colonised new habitats.

Genome size

The so-called “C-value enigma” refers to the observation that the genome size among many eukaryotes can vary widely, and this variation does not have to correlate with the number of genes or the organismal complexity (e.g. some unicellular organisms have genomes much larger than humans). Understanding how and why genomes show such pronounced size variation has become a timely research topic, especially in the current post-genomics era [38].

Much has been discovered about the patterns and consequences of variation in genome size, with most of these discoveries coming from studies on vertebrates and plants (e.g. [39, 40]), and comparatively little from insects. The first comprehensive study of genomic variation in odonates quantified genome variation in 100 North American species, and revealed a nearly ten-fold difference in genome size between species (from 0.41 pg (Miathyria marcella) to 2.36 pg (Somatochlora elongata), [41]). Genome size correlations with voltinism and larval habitat were not found, but a significant relationship between genome size and body size (positive in dragonflies and negative in damselflies), and flight ability was found (with small genomes being associated with percher species, that is those that only fly intermittently in between periods of perching, and large genomes with fliers, that is those that fly continuously). Finally, genome size was also positively correlated with a species’ chromosome number [41]. Future work using a combination of genomic and transcriptomic data could be used to elucidate putative mechanisms responsible for the variation in genome size across odonate species; such as gene duplication, DNA loss, variation in intron size or transposable elements.

Complex life cycle

Most animal species (80 % of the animal kingdom) have a complex life cycle (CLC), whereby the immature and adult stages occupy different ecological niches and often undergo varied degrees of metamorphosis [50–52]. Odonata make an excellent group to explore the evolutionary causes and consequences of CLCs as the larvae are aquatic and the adults are terrestrial, and both life stages are well-studied [52]. Organisms that live in different environments throughout their ontogenies are faced with constraints to optimize responses to the various selection pressures that operate in each environment [53]. Thus, the relevant question concerns how one genome responds to contrasting selection regimes in multiple environments. Moreover, when these environments undergo divergent changes, for example through global warming which will affect aquatic and terrestrial habitats differently [51], one genome must mediate appropriate genetic responses in two different life stages across two different and changing environments. Studies of such genetic (including epigenetic) responses in odonates can be used to understand how other animals with CLCs may respond to climatic changes and in what systems adaptations are likely to occur. A major hurdle to the study of CLC evolution is a lack of knowledge about the extent to which life stages genetically covary and whether selection acts in a complementary (or divergent) way [54, 55]. The few quantitative genetic studies that have addressed this issue found support for genetic associations across life stages, but also showed that traits are capable of independent evolutionary change in response to the divergent conditions encountered during each life stage (ascidians [55], or anurans [56]). It thus seems that both genetic association and independent evolution can help to shape adaptation in some species, however, the paucity of studies to date make it impossible to draw general conclusions.

The molecular mechanisms underlying the coupling of life stages across metamorphosis are not particularly well studied (but see [57] for work on Drosophila). Thus, there is a major gap in understanding gene-by-environment interactions that would occur during major developmental transitions [58]; for example, how do the immune systems of dragonflies and damselflies respond to different larval and adult environments? The recently identified immune genes in the damselfly Coenagrion puella [59] would allow testing more directly whether larval and adult stages evolve independently from one another. Furthermore, transcriptomic studies measuring gene expression patterns during larval and adult stages would elucidate the degree of plasticity in gene expression in different life stages and how environmentally induced changes differentially affect the genetic responses of larval and adult life stages [58]. Such studies would improve our understanding of how differential selection pressures across the life cycle modulate genetic and plastic adaptive processes. A genomic approach would also provide an important complement to understanding the documented carry-over effects of larval stressors to adult fitness. For example, it has been demonstrated that larval food shortage affects adult lifetime reproductive success in the damselfly Lestes viridis [60]. Moreover, transcriptomic studies could address the extent to which epigenetic changes in the larval stage are reprogrammed during metamorphosis [61], which may facilitate novel epigenetic responses at the adult stage.

Movement dynamics: dispersal

Dispersal is a fundamental ecological and evolutionary process that redistributes individuals among areas [62], thereby buffering against the demographic and genetic losses that are expected to occur in otherwise isolated populations. Perhaps the best-studied animal in terms of dispersal ecology and concomitant eco-evolutionary dynamics is the Glanville fritillary butterfly Melitaea cinxia [63]. This was one of the first non-laboratory organisms studied using high-throughput sequencing approaches [64], which demonstrates not only the feasibility but also the usefulness of obtaining genomic data from wild populations. Work on the Glanville fritillary quantified how polymorphisms at a single locus can be associated with population demography [65] and life history traits and fitness in both adults and larvae [63, 66, 67]. Odonates share many of the attractive features of butterflies for integrative research into movement dynamics, including the ease to study larval life history traits, and adults that can be marked and recaptured to quantify dispersal and mortality in the wild. In addition, odonates provide the added dimension of linking terrestrial and aquatic systems.

Dispersal can be quantified using both ecological and genetic methods. Indeed, studies on odonates have provided evidence that such different methodologies provide comparable information about population connectivity [68, 69]. Odonates have provided model systems for studies of how landscape features, such as urban areas [68] or high grounds [70], can limit dispersal and how agricultural development may affect dispersal pathways [71]. These studies also uncovered a loss of genetic diversity in isolated populations [72], but there is little information about the eco-evolutionary consequences of genetic erosion in odonate populations. The application of genomic techniques to quantify, for example, whether, and if so how, small population size limits adaptation in wild populations would be useful for informing conservation management.

Monitoring the consequences of climate change

Several damselfly species have modified their distributions and abundances over the last few decades in response to rising global temperatures [73–75]. Long-term distributional data of adults show that odonates are amongst the taxa showing the strongest poleward range expansions [73, 74], making them excellent study organisms for unravelling the still poorly documented rapid microevolutionary changes associated with range expansions [76]. This research can be embedded in the several well-documented cases of latitudinal adaptation among odonates. For example, common garden studies on larvae of the damselflies Ischnura elegans and Lestes sponsa provided a detailed picture of thermal adaptation along a latitudinal gradient in Europe. A key pattern is the evolution of thermal reaction norms and voltinism in response to differences in temperature [77]. Notably, the evolution of higher thermal optima and faster growth rates in southern latitudes has been associated with changes in digestive physiology [78], cold resistance [79], predator–prey interactions [80] and resistance against contaminants [81]. Other studies in L. sponsa indicated the evolution of larval growth and development rates and their response to photoperiod [82–84]. Genomic studies for these cases of latitude-associated adaptation may not only reveal the pathways underlying the observed phenotypic differentiation but may also identify novel aspects of adaptation along this strong thermal axis. Variation in these candidate genes can then be screened in spatial and temporal contexts as climate change continues.

Recent work aimed to quantify the genetic consequences for odonate species that are expanding their ranges has shown reductions in genetic diversity in edge-of-range populations [85, 86], and evidence for selection at the gene level [87]. Using common garden experiments, rapid evolution of both larval traits (increased growth rate and increased activity levels) and adult traits (increased flight ability and increased immune function) was demonstrated in the rapidly poleward expanding damselfly Coenagrion scitulum [88, 89]. The few studies on genomic signatures of range expansion in both plants and animals did not link genetic changes to phenotypes and did not unravel the evolutionary processes involved [76]. In a first effort to do so, a single-nucleotide polymorphism (SNP) study focused on C. scitulum revealed one SNP associated with increased flight performance to be under consistent selection in the populations at the expanding range edge [87]. This indicates that evolutionary changes among independent edge populations are driven by the range expansion process per se. This study illustrates the added value of integrating genomic, phenotypic and environmental data to identify and disentangle the neutral and adaptive processes that are simultaneously operating during range expansions. An important future step will be to identify other determinants of dispersal ability at the molecular level. For example, some sequence data on candidate ‘dispersal’ genes, such as pgi, hif1alpha or sdhd [90, 91] are available for odonates [27]. Applying genomic studies to the other well-documented range expansions in odonates may therefore considerably add to the limited knowledge on how species evolve during range expansions.

Climate change and hybridisation

In addition to a loss of species diversity, many range expansions are creating de novo sympatric areas between formerly allopatric taxa, and increasing evidence is suggesting that this can modify species interactions [92]. Furthermore, evidence is growing that species interactions in these newly created sympatric zones are leading to the breakdown of species barriers and rapid hybridisation (reviewed in [93]). Thus, species identities in these de novo sympatric zones may be unclear. Molecular methods for species identification could help us to resolve species identities via genetic means and provide clues about the general processes underlying the creation of biodiversity. For example, by studying the genomics of species hybridisation and species introgression in odonates, we would obtain a better knowledge of the processes underlying the creation of novel genetic adaptations. In general, it is thought that adaptive genes have a greater chance to cross species boundaries than key “speciation genes” or genes residing inside “genomics islands of divergence”, which should both be more resistant to introgression [94, 95]. Genomic studies on introgressive hybridisation in damseflies are being initiated and have the potential to uncover if certain genomic regions are repeatedly inherited from the same parental species. These studies may be able to elucidate the size of genomic linkage islands and how the inheritance of genomic regions correlates with morphology and ecology.

The vulnerability of odonates to anthropogenic changes makes informed conservation measures a priority, given the likely impact that these changes may have on the overall species diversity, food web structure and ecosystem stability. A recent comparative study on several damselfly species assessed the potential to use quantitative predictions of reproductive isolation as an indicator to assess species’ hybridisation risk [96]. The study found a positive correlation between the degree of reproductive isolation and genetic distance between species, as has been shown in fruit flies [97] and butterflies [98]. This clear link between species divergence rates and the likelihood to hybridise strongly suggests that genetic divergence between taxa can be used as a proxy to predict hybridisation rates of species that come into contact following climate induced range expansions [96]. This link can be used to inform conservation efforts, particularly for odonate species that are already endangered (e.g. Ischnura gemina, [96]).

Reproductive mode and behaviour

Insects are incredibly diverse in their reproductive behaviour and genetic tools are beginning to shed light on how the different reproductive modes have originated. To date, our knowledge of the genetics of insect reproductive behaviour comes mainly from studies of laboratory model species like Drosophila (e.g. [105]) and eusocial insects (e.g. [106]). Dragonflies and damselflies have a unique mode of reproduction whereby the male grasps the female by the head (dragonflies) or the prothorax (damseflies) and then the female raises the tip of her abdomen forward to receive sperm from the male secondary genitalia; forming a characteristic ‘mating wheel’ (Fig. 3b in [107]). Elucidating the genes involved in courtship and mating among odonates will help to clarify the evolutionary origin of their unique reproductive mode. Additionally, because modern odonates represent some of the most ancient insects, by identifying the genes involved in mating in this group, we can make evolutionary comparisons of the origins of reproductive behaviours in other well-studied insect groups.

Odonates are also a model system for studying sperm precedence. Males engage in various strategies to ensure reproductive success by removing or displacing rivals’ sperm from the female storage organs before transferring their own sperm [108]. Further studies of these behaviours using genomic tools can give us insight on the evolutionary origins of these diverse reproductive mechanisms and the large variation in female and male mating rate that promoted their evolution. In Drosophila, selection for increased mating rate led to major genetic changes (up to a 21 % of the entire genome) which pleiotropically selected for key functions related to neurogenesis, metabolism, development and general cellular processes [109]. In Odonata, genomic studies could address whether such disparate mating behaviours have also selected for other key biological functions, which may explain the extensive variation in ecologies (e.g. adaptation to tropical and non-tropical environments) observed in many closely-related species. To this extent, ischnuran damselflies may give unique insight because they occupy a variety of extreme environments and exhibit also a vast variation in mating strategies, ranging from polyandry to parthenogenesis. The latter is particularly interesting, because in contrast to other known insect groups in which asexual reproduction is frequently found, only one case of obligate parthenogenesis is known within the Odonata (the only-female populations of the American species Ischnura hastata on the Azores islands [110]). Ongoing comparative transcriptomic studies on sexual and parthenogenetic lineages of this species will help to better understand which genes are related to asexual reproduction and why it has evolved in this but not other species of this group.

With regards to the intra- and interspecies variation in sperm displacement mechanisms, nothing is yet known about the genetic underpinnings. Genomic studies that reveal these underpinnings can provide answers to several questions. Firstly, is sexual selection on genitalic function involved in population divergence and speciation [111]? Candidate genes for addressing this question are available from genetic work on male genitalic structures [112, 113] and female sperm storage organs in Drosophila [109] and eusocial insects. In particular, odonates exhibit extensive intra- [114] and inter-specific [115] variation in the morphology of female sperm storage organs. Secondly, do females gain indirect (genetic) benefits from mating multiple times [116] (e.g., through the production of more genetically variable offspring)? And thirdly, how can sperm remain viable once stored in the female sperm storage organs? For example, Ischnura aurora mate soon after emergence and then disperse, which implies female adaptations to keep sperm viable even when the animal is not sexually mature [117].

Dragonflies and damselflies also exhibit diverse pre-mating behaviours related to male-male competition. For example, distinct behavioural differences exist between territorial and non-territorial males, both within and among species [118]. Although ultimate effectors and fitness trade-offs of male mating tactics are reasonably well-known [119], knowledge of both the underlying genomic basis and hormonal influences are lacking [120]. There is potential for strong pleiotropic effects in some species, as seen in Japanese Mnais damselflies, where male mating tactics are linked to a male-limited colour polymorphism [121]. In this case we know that the expression of territorial behaviour is correlated with levels of juvenile hormone [122, 123], lipid content [124], muscular activity [125], infection level, and flight muscle protein expression [126]. Studies indicate that these pathways are highly conserved likely due to purifying selection [127], signifying that the widespread variation in male odonate sexual behaviour may be driven by mutations in gene expression profiles rather than changes in protein coding sequences.

Odonata has also been an exemplary group for studies on female preference. Several damselfly species appear to exhibit learned mate behaviours and plastic mate preferences [128], and populations commonly show pronounced preferences even across small spatial scales. The extent to which population divergence is related to mating preference is relatively unexplored, but it is likely that the combined action of learning, plasticity and microevolutionary processes are involved in most cases. For example, it is known that naïve female Calopteryx splendens can rapidly learn to distinguish between con- and heterospecific males based on their wing phenotype [129, 130], and it appears that learning of heterospecific phenotypes may also be involved in sexual isolation between the European Calopteryx species [92]. In the latter study, it was shown that C. virgo males have lost part of their mate recognition ability and that this loss increased heterospecific mating attempts [92]. While association learning is probably partly involved in the increased heterospecific mating rates in allopatry, loss of mate discrimination alleles as a result of selection (e.g. reinforcement) or genetic drift in this case also likely have played a role. By combining behavioural field data with genomic data, we could determine to what extent mating preferences and species recognition are fixed at emergence, and to what degree populations with divergent sexual preferences differ in their genomic signatures. A combination of gene expression studies and mating trials would provide yet another way to gain deeper insights into the involvement of microevolutionary processes in sexual divergence in this group.

Sexual dimorphism

Flight

From the moment of emergence from the aquatic environment, odonate individual fitness is critically dependent on an individual’s ability to fly. Species exhibit wide (~100-fold) variations in body mass and thus have evolved different flight behaviours and motor designs to accommodate this morphological diversity [165]. This variation in flight adaptations makes them excellent models to examine the genomic architecture associated with variation in flight capacity. For example, percher and flier dragonfly species differ in diurnal activity pattern and flight thermoregulatory strategy [166]. Moreover, odonates exhibit distinctly different flight system morphology and kinematics (e.g. wing beat frequency and amplitude [167, 168]). Indeed, maximum lift production per unit mass of the damselfly flight motor is significantly higher (~86 N/Kg) than that of dragonflies due to the lift enhancing “clap and fling” mechanism that they employ in flight (~54–60 N/Kg, [169]). Similarly, flight motor investment during sexual maturation varies dramatically among odonates, with males of territorial species showing relatively high flight muscle mass accretion [165], thus enhancing their flight-muscle ratio and aerial manoeuvrability. It is the continuum of odonate life history strategies that rely largely on flight that makes them such an attractive group for examining the mechanisms that operate to optimize flight motor design [126], neural control [170], comparative biomechanics [171] and closely associated features (e.g. vision, thermoregulation), across different ecological niches and in response to environmental variation. Interestingly, odonates have one of the few extant direct synchronous locomotor flight systems in the insect world, making them more similar to vertebrate musculoskeletal systems than many other insect groups.

An example of integrative work on molecular mechanisms controlling odonate flight performance is that on quantitative alternative splicing of the gene encoding troponin T, a key flight muscle sarcomere protein, in Libellula pulchella (reviewed in [172]). This gene regulatory mechanism appears to serve as a key controller of energy consumption and flight muscle performance throughout adult life [125]. It is sensitive to nutrition and body weight variation and impaired by an infectious agent from the environment, which causes a metabolic syndrome and impaired locomotion similar to that occurring in mammalian obesity [173]. The potential to uncover mechanisms controlling trade-offs in locomotor muscle tissue and other equally important organ systems using high throughput sequencing technologies is emphasized by the work on just this single gene. Similar molecular (gene regulatory) mechanisms controlling tissue performance plasticity (i.e. for vision, locomotion, digestion, excretion) likely enable the developmental transition from predatory aquatic larvae to flying adults, and thus could reveal evolutionary signatures important to an aquatic origin of insect flight.

Thermoregulation and thermal biology

Strenuous activity such as flight tends to raise insect body temperature over ambient due to the relatively low (i.e. 10–20 %) efficiency of muscle power production [115]. As a likely consequence, many flying insect taxa evolved flight muscles that operate optimally at temperatures higher than ambient [166, 174], which in turn necessitated behavioural and physiological mechanisms to tightly control flight muscle temperature. Odonates exhibit a diversity of such thermoregulation strategies and are considered the earliest animal groups to have evolved them, millions of years prior to vertebrates [166, 175].

The odonate thermoregulatory repertoire has been reviewed in detail previously [115, 166]. Percher species typically control body temperature heliothermically, i.e. gaining heat from the sun, through postural adjustments [166, 176, 177] or through shivering thermogenesis (even some gomphids), while other perchers (i.e. some gomphid species, [176]) show little evidence of thermoregulation [178, 179]. Thermoregulation strategies in flier species can additionally involve flight behavioural adjustments (i.e. increase ratio of gliding/powered flight; but see [166]) and/or breathing-assisted blood circulation [180]. The evolution of thermoregulatory strategies in Odonata has likely selected for modifications at the molecular level that optimize and/or stabilize cellular functions at these temperatures. Such molecular thermal sensitivity has been demonstrated in other insect groups (e.g. for lactate dehydrogenase and phosphoglucose isomerase [117, 181]), but has thus far not been examined in Odonata.

In the realm of climatic thermal adaptation, Lancaster et al. [182] used a combination of laboratory experiments and field collections to investigate the genomic responses to sub-optimal temperatures (high and low) in the damselfly I. elegans. Thermal chambers were used to expose individuals from central populations and marginal populations in the north of the species’ range to different temperatures, and then RNA-seq was used to examine the number and types of differentially expressed gene transcripts [182]. Several functionally important genes were differentially expressed. Most notably, genes involved in cold tolerance showed a higher evolutionary liability compared to genes associated with heat tolerances. These results will form the basis for future work on climatic adaptation in this and related species. Robust odonate genomic resources would allow us to start examining the molecular consequences of thermoregulatory strategies in this ancient lineage (>300 million years of evolution) and facilitate the integration of thermal biology to better understand the success of Odonata in colonizing environments with vastly different ambient temperatures, and would provide a better understanding of the environmental ecology and dynamics of insects in general.

Sensory systems

Adult dragonflies and damselflies rely heavily on one sensory system – vision. Although the relative unimportance of smell may have been underemphasized, as recent research has found morphological and electrophysiological data showing that I. elegans is capable of detecting the odour of both prey and mates ([183]). Odonata offers an ideal system for studying the evolution of genes involved in vision because visual communication is paramount among Odonata; they have complex colour vision [184], and many behaviours that rely on distinguishing colour [185]. Adults have notably large compound eyes that consist of thousands of ommatidia. The number of ommatidia varies among species from about 7000 in damselflies (e.g. Coenagrionidae) to over 28,000 in large dragonfly species (e.g. Aeshnidae), which are the largest number of ommatidia in any insect eye [186]. Odonates can recognize a wide range of spectra from ultraviolet to red [140, 186, 187], with the light sensitivity differing markedly between the dorsal and ventral portion of compound eyes [139, 188]. Odonates, particularly dragonflies, possess a strikingly large number of opsin genes (light sensitive proteins in the eye that function as the first step in phototransduction) [141], and may have the most complex suite of opsins for any terrestrial animal (e.g. Anax parthenope has as many as 30 visual opsin gene copies [141]). These opsin genes are differentially expressed between larvae and adults, and between the dorsal and ventral regions of adult compound eyes [140], which may coincide with the use of different environments between the life stages and sexes. Larvae have smaller eyes that express fewer types of opsins but larger antenna, suggesting that they utilize other cues in addition to vision (e.g. pheromones, vibration or pressure). Indeed, it has been shown that larvae of the damselfly Enallagma antennatum rely mainly on chemical cues to detect predators [189].

Accompanying the colour visual system are equally exceptional visual acuity and visual neurons, which make odonates among the most supreme hunters in the animal world, successfully capturing their prey ~95 % of the time [171, 190]. Dragonflies use internal models to regulate sensorimotor control while hunting [170], a trait that was thought to be unique among only vertebrates. Because odonates appear to use mostly one sensory system to carry out relatively complex activities at the adult life stage (e.g. hunting, mate finding), they make an attractive system for the study of vision since these activities are modulated to a large degree by vision alone, i.e. without the contributions and thus the complications of other sensory systems. Furthermore, we know comparatively little concerning the visual system of the larval stage [191–193]. Genomic resources for Odonata will be central for elucidating the diverse potentially co-evolutionary patterns between visual capability, hunting strategy, colour discrimination, colour and colour patterns that occur in the adult and larvae of this group.

Stress physiology in larvae and integrative physiology

Work on damselfly larvae has been instrumental in exploring physiological stress responses, and has contributed to advancing our understanding of how physiological stress is affected by predation risk, environmental contaminants and responses to combinations of stressors. There is increasing concern that interactions among stressors may negatively affect biodiversity [194]. Specific attention should be paid to understanding how the effects of contaminants may be magnified in the presence of other stressors such as predation risk [195] and higher temperatures [196]. This may explain why contaminant levels assumed to be safe by legislation still cause considerable loss of aquatic biodiversity [197, 198]. To understand and predict synergistic interactions between stressors we need to know how individual and combined stressors affect organismal performance at the physiological level. Yet, even for common natural stressors, such as predation risk, this is poorly known, especially in invertebrates [199]. With regard to physiological effects of predation risk, damselfly larvae are among the best studied invertebrates, which led to novel insights in how predation risk affects prey physiology [200, 201] and thereby can magnify the effects of pesticides [202]. Stress physiology can also help to mechanistically explain how effects of stressors encountered during the larval stage may bridge metamorphosis and shape adult fitness components. For example, it was recently shown that larval exposure to UV stress in the damselfly C. puella impairs adult immune function through increased allocation of melanin to the cuticle [203], thereby identifying a novel pathway by which effects of larval stressors can be carried over to the adult stage in animals with a CLC.

Physiological studies are complicated by the often complex interactions between traits that are typically studied in isolation. The development of genomic resources for odonates would allow more rigorous testing of interactions between a changing environment (e.g. temperature, chemical composition) and the abilities of different species to handle environmental stressors. For example, genomic studies could delineate mechanistically the trade-offs between immunity and energetics (e.g. [126]), or more definitively link environmental stressors to impairments in colour development, flight (e.g. thermoregulation ability, flight motor design) and fitness (e.g. [204–206]). The contrast of their quite homogeneous larval life history and ecological relevance (i.e. one of the apex invertebrate carnivores), and highly variable adult form (size, colour, behaviours, physiology, longevity and distribution), combined with broadly based scientific community and rapidly increasing genomics community, identifies Odonata as an model taxon with high potential to achieve such evolutionary and ecologically relevant integration.

Summary points

Future prospects