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

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.     

Indirect Monitoring of Agonistic Encounters in Larvae of Lestes viridis (Odonata: Lestidae) Using Exuviae Lamellae Status

Differences in interference competition between larvae of the damselfly Lestes viridis (Vander Linden) were examined using caudal lamellae status of exuviae. Exuviae from a small temporary fishless pond near Antwerp (Belgium) where L.viridis was the only odonate present were studied. No lamellae loss during emergence was seen. Therefore, the lamellae status of the exuviae reflects the lamellae status of the final instar larvae. The deviations of the distribution of the number of missing lamellae per individual from a binomial distribution suggested that lamellae are not always lost separately or that some animals are more prone to agonistic encounters. I found no difference in agonistic encounters between sexes. In accordance with the hypothesis of Pierce et al. (1985) interference competition was higher in the lestid species inhabiting small, temporary fishless ponds than in the coenagrionid damselfly Ischnura posita inhabiting large permanent fish containing water bodies that was studied by Robinson et al. (1991).     

What factors shape female phenotypes of a poleward‐moving damselfly at the edge of its range?

Individuals at the expansion front during a climate‐driven range expansion are expected to differ phenotypically from those individuals in core populations. Little information is known about the joint, potentially opposing, effects of stressful conditions at the range edge versus evolutionary changes that take place during range expansion in shaping the phenotypes at the range front. We investigated the effect of range expansion on immune function, body condition and flight‐related morphology (flight muscle ratio, wing loading, and wing aspect ratio) of field‐collected females of the poleward‐moving damselfly Coenagrion scitulum. Individuals at the expansion front had a lower body condition, which indicated more stressful conditions at the range edge. Despite the counteracting effect of the shorter growth season, the higher flight muscle ratios at the expansion front indicated a strong selection for dispersal ability during range expansion. The current study suggests that models need to incorporate the interplay of stressful conditions and evolutionary processes at the expansion front to arrive at robust predictions of future species distributions under global warming. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 556–568.     

Invertebrate predation selects for the loss of a morphological antipredator trait

Antagonistic selection by different predators has been suggested to underlie variation in morphological antipredator traits among and within species. Direct empirical proof is equivocal, however, given the potential interrelationships of morphological and behavioral traits. Here, we tested whether spines in larvae of the dragonfly Leucorrhinia caudalis, which are selected for by fish predators, are selected against by invertebrate aeshnid predators. Using a manipulative approach by cutting spines instead of making comparisons among species or inducing spines, we were able to decouple the presence of spines from other potentially covarying morphological antipredator traits. Results showed survival selection for the loss of spines imposed by invertebrate predation. Moreover, spined and nonspined larval L. caudalis did not differ in the key antipredator behaviors, activity level, and escape burst swimming speed. The observed higher mortality of spined larvae can therefore be directly linked to selection by aeshnid predation against spines.     

Behavioral responses to fish kairomones and autotomy in a damselfly

The threat-sensitivity hypothesis predicts that prey species assess and adjust their behavior in accordance with the magnitude of the threat posed by a predator. A largely overlooked characteristic of a prey that will affect its sensitivity to predators is its history of autotomy. We studied threat-sensitive behavior to fish kairomones in larvae of Ischnura elegans damselflies, which had undergone autotomy, from a fishpond and from a fishless pond. In agreement with their higher perceived risk, larvae from the fishpond showed fewer rigid abdomen bends, foraged less and walked more slowly than larvae from the fishless pond. In line with their higher vulnerability to predators, larvae without lamellae spent less time foraging than larvae with lamellae. There was a decrease in swimming activity in the presence of fish kairomones except for larvae with lamellae from the fishless pond. This may reflect differences in vulnerability of larvae without lamellae between pond types. Such context-dependent responses in activity to kairomones should be kept in mind when evaluating the ability of a prey to recognize kairomones.     

Seasonal time constraints shape life history,physiology and behaviour independently,and decouple a behavioural syndrome in a damselfly

The integration of traits into ‘syndromes' has been suggested as a useful framework to advance insights in trait responses to environmental stressors. Yet, how stressors shape the consistency (‘repeatability') of traits and their covariation at the individual level remains debated. We studied how seasonal time constraints shape trait repeatability and integration of life-history, behavioural and physiological traits along a fast–slow continuum, using the ‘pace-of-life syndrome' as a framework. We manipulated the photoperiod during the larval development of the damselfly Ischnura elegans, generating a time-relaxed early, a control, and a time-constrained late group. The photoperiod treatment did not seem to affect the voltinism of the larvae. As predicted, late-period larvae accelerated development and growth, yet this acceleration was no longer detectable for growth and metabolic rate during the final instar, possibly due to costs of the initial life-history acceleration. This warrants caution when inferring a species' pace-of-life based on a specific developmental stage. The late-period larvae were as predicted more active (only during the later stages of the final instar) and bolder than the control larvae, but not different from the early-period larvae. Most studies on time constraints only compared late and control animals, thereby potentially wrongly concluding adaptive responses to time constraints. Activity, boldness and body mass were repeatable, while growth and metabolic rates were not. Notably, repeatabilities did not change under time constraints. There was no support for an overall trait integration in a pace-of-life syndrome, yet activity and boldness covaried positively as expected. Importantly, this ‘behavioural syndrome' was decoupled in the late-period larvae, which might be adaptive to enhance energy acquisition to fuel the accelerated development rate. Our results suggest that besides the predicted plastic acceleration of life-history, plastic changes in behavioural trait integration may also be an important but overlooked adaptive aspect of responding to time constraints.     

Predation risk causes oxidative damage in prey

While there is increasing interest in non-consumptive effects of predators on prey, physiological effects are understudied. While physiological stress responses play a crucial role in preparing escape responses, the increased metabolic rates and shunting of energy away from other body functions, including antioxidant defence, may generate costs in terms of increased oxidative stress. Here, we test whether predation risk increases oxidative damage in Enallagma cyathigerum damselfly larvae. Under predation risk, larvae showed higher lipid peroxidation, which was associated with lower levels of superoxide dismutase, a major antioxidant enzyme in insects, and higher superoxide anion concentrations, a potent reactive oxygen species. The mechanisms underlying oxidative damage are likely to be due to the shunting of energy away from antioxidant defence and to an increased metabolic rate, suggesting that the observed increased oxidative damage under predation risk may be widespread. Given the potentially severe fitness consequences of oxidative damage, this largely overlooked non-consumptive effect of predators may be contributing significantly to prey population dynamics.     

Local genetic adaptation generates latitude‐specific effects of warming on predator–prey interactions

Temperature effects on predator–prey interactions are fundamental to better understand the effects of global warming. Previous studies never considered local adaptation of both predators and prey at different latitudes, and ignored the novel population combinations of the same predator–prey species system that may arise because of northward dispersal. We set up a common garden warming experiment to study predator–prey interactions between Ischnura elegans damselfly predators and Daphnia magna zooplankton prey from three source latitudes spanning >1500 km. Damselfly foraging rates showed thermal plasticity and strong latitudinal differences consistent with adaptation to local time constraints. Relative survival was higher at 24 °C than at 20 °C in southern Daphnia and higher at 20 °C than at 24 °C, in northern Daphnia indicating local thermal adaptation of the Daphnia prey. Yet, this thermal advantage disappeared when they were confronted with the damselfly predators of the same latitude, reflecting also a signal of local thermal adaptation in the damselfly predators. Our results further suggest the invasion success of northward moving predators as well as prey to be latitude‐specific. We advocate the novel common garden experimental approach using predators and prey obtained from natural temperature gradients spanning the predicted temperature increase in the northern populations as a powerful approach to gain mechanistic insights into how community modules will be affected by global warming. It can be used as a space‐for‐time substitution to inform how predator–prey interaction may gradually evolve to long‐term warming.     

Collateral damage: rapid exposure-induced evolution of pesticide resistance leads to increased susceptibility to parasites

Although natural populations may evolve resistance to anthropogenic stressors such as pollutants, this evolved resistance may carry costs. Using an experimental evolution approach, we exposed different Daphnia magna populations in outdoor containers to the carbamate pesticide carbaryl and control conditions, and assessed the resulting populations for both their resistance to carbaryl as well as their susceptibility to infection by the widespread bacterial microparasite Pasteuria ramosa. Our results show that carbaryl selection led to rapid evolution of carbaryl resistance with seemingly no cost when assessed in a benign environment. However, carbaryl-resistant populations were more susceptible to parasite infection than control populations. Exposure to both stressors reveals a synergistic effect on sterilization rate by P. ramosa, but this synergism did not evolve under pesticide selection. Assessing costs of rapid adaptive evolution to anthropogenic stress in a semi-natural context may be crucial to avoid too optimistic predictions for the fitness of the evolving populations.     

Seven decades of southern range dynamics of Canada lynx

The range of the Canada lynx (Lynx canadensis) has contracted substantially from its historical range. Using harvest records, we found that the southern range of the lynx in Ontario in the late 1940s collapsed and then, in a short period of time, increased to its largest extent in the mid‐1960s when the lynx range spread south of the boreal forest for a decade. After this expansion, the southern range contracted northwards beginning in the 1970s. Most recently, there has been a slight expansion between 2010 and 2017. We have attributed these dynamics on the southern range periphery to the fluctuation of the boreal lynx population in the core of the species'' range. In addition, connectivity to boreal lynx populations and snow depth seemed to condition whether the lynx expanded into an area. However, we did not find any evidence to suggest that these changes were due to anthropogenic landscape disturbances or competition. The boreal lynx population does not reach the peak abundance it once did, without which we would not expect to see large expansions of the southern lynx range as in the mid‐1960s. Our results suggest that the southern lynx range in Ontario has been driven by the magnitude of the boreal lynx population cycle, connectivity to the boreal forest, and snow conditions. Future persistence of lynx in the southern range periphery will likely depend on dynamics in the range core.