Allometry of Defense: Predator Shift Alters Ontogenetic Growth Patterns in an Antipredator Trait.

Predation is a major factor driving prey trait diversification and promoting ecological speciation. Consequently, antipredator traits are widely studied among prey species. However, comparative studies that examine how different predators shape the ontogenetic growth of antipredator traits are scarce. In larval dragonflies, abdominal spines are effective traits against predatory fish in fish lakes, which prefer larger prey. However, defensive spines increase mortality in habitats dominated by invertebrate predators (invertebrate lakes), which prefer smaller prey. Thus, species from fish lakes may accelerate spine growth at a later body size compared to species from invertebrate lakes when growing into the preferred prey size range of predatory fish. In this study, we constructed the allometric relationship between spine length and body size and compared the inflexion point of those growth curves in five species of Leucorrhinia dragonfly larvae. We found that fish-lake Leucorrhinia species accelerated spine growth at a larger body size than congenerics from invertebrate lakes. Further, rather than extending spine length constantly through development, fish-lake species rapidly accelerated spine growth at a larger body size. This is likely to be adaptive for avoiding invertebrate predation at an early life stage, which are also present in fish lakes, though in smaller numbers. Our results highlight that comparative studies of ontogenetic patterns in antipredator traits might be essential to develop an integrated understanding of predator-prey interactions.

Genetic variation and population structure of a widely distributed damselfly (Ischnura senegalensis).

Ischnura senegalensis Rambur, 1842 is among the most widespread damselfly species in the world. Unlike dragonflies with strong migration abilities, I. senegalensis have limited dispersing abilities. Gene flow among I. senegalensis populations may be greatly influenced by anthropogenic disturbance, fragmented suitable habitats, sea straits, or even global warming. In this study, to investigate the genetic diversity of I. senegalensis populations, we sequenced and collected 498 cytochrome oxidase I sequences across the Old World. Haplotype network analysis showed 51 haplotypes and I. senegalensis could be grouped into four regions (Afrotropical region, Oriental region, main Islands of Japan, and the Ryukyu Islands), each of which contains different dominant haplotypes. Based on molecular variance analysis, we found that populations from the Afrotropical region have quite a low gene flow with the Asian populations (except Yemen). Furthermore, rice cultivation may aid the dispersion of I. senegalensis in the oriental region. Populations from the Ryukyu Islands show the highest genetic diversity, which may be due to the geological separation among islands. Our results prove that I. senegalensis has great genetic diversity among different populations across the world.

Complete mitochondrial genomes of two damselfly species in coenagrionidae and phylogenetic implications.

Agriocnemis femina (Brauer, 1868) and Ischnura senegalensis (Rambur, 1842) are two damselflies inhabiting paddy lands. As an intermediate predator, they play an important role in controlling certain crop pest and mosquitoes. In this study, we sequenced complete mitogenomes of these two species. The total length of mitogenomes is 15,936 bp in A. femina and 15,762 bp in I. senegalensis. Both of mitogenomes consist of 13 protein-coding genes, 22 tRNA genes, two rRNA genes, and one control region. The close relationship between I. senegalensis and I. elegans was further proved by phylogenetic analysis. Our phylogenetic analysis indicated a clear two lineages in Coenagrionidae (Core and ridge-faced Coenagrionidae). Ridge-faced Coenagrionidae consisted of Megaloprepus caerulatus and Ceriagrion fallax. In core Coenagrionidae, Ischnura and Enallagma are most closely related; they formed one clade with Agriocnemis and then grouped together with Paracerion. Our study provides new genetic information for further study in phylogenetic analysis of Coenagrionidae.

Predator species related adaptive changes in larval growth and digestive physiology.

Prey species are often non-randomly distributed along predator gradients but according to how they trade off growth against predation risk. The foraging-mediated growth/predation risk trade-off is well established, with increased foraging accelerating growth but also increasing predator induced mortality. While adaptations in digestive physiology may partly modify the relationship between foraging and growth in response to predation risk, studies exploring the impact of digestive physiology on growth in prey subjected to predation risk are still scarce. Larvae of the dragonfly genus Leucorrhinia segregate at the species level between lakes either being dominated by predatory fish (fish-lakes) or predatory invertebrates (dragonfly-lakes). Predators of these two lake types differ dramatically in their hunting style like searching and pursuing mode causing different selection pressure on prey traits including foraging. In a laboratory experiment we estimated growth rate, digestive physiology (ingested food, growth efficiency, assimilation efficiency, conversion efficiency) and metabolic rate (oxygen consumption) in the presence and absence of predator cues. Whereas fish-lake and dragonfly-lake Leucorrhinia species did not differ in growth rate, they evolved different pathways of digestive physiology to achieve similar growth rate. Because fish-lake species expressed a higher metabolic rate than dragonfly-lake species, we assume energy to be differently allocated and used for metabolic demands between species of both predator environments. Further, growth rate, but not digestive physiology was plastic in response to the presence of predator cues. Our results highlight the impact of digestive physiology in shaping the foraging-mediated growth/predation risk trade-off, with digestive physiology contributing to species distribution patterns along predator gradients.

Phylogeography and larval spine length of the dragonfly Leucorhinia dubia in Europe.

Presence or absence of predators selects for different kind of morphologies. Hence, we expect variation in traits that protect against predators to vary over geographical areas where predators vary in past and present abundance. Abdominal larval spines in dragonfly larvae provide protection against fish predators. We studied geographical variation in larval spine length of the dragonfly Leucorrhinia dubia across Western Europe using a phylogenetic approach. Larvae were raised in a common garden laboratory experiment in the absence of fish predators. Results show that larvae from northern Europe (Sweden and Finland) had significantly longer larval spines compared to larvae from western and central Europe. A phylogeny based on SNP data suggests that short larval spines is the ancestral stage in the localities sampled in this study, and that long spines have evolved in the Fenno-Scandian clade. The role of predators in shaping the morphological differences among the sampled localities is discussed.

The interplay of adult and larval time constraints shapes species differences in larval life history.

In animals with a complex life cycle, larval life-history plasticity is likely shaped by the interplay of selective factors in both larval and adult stages. A wide interspecific variation in responses to larval time constraints imposed by seasonality has been documented. Few studies have addressed differences among closely related species in the evolutionary trajectories of age and size at metamorphosis and their link with larval growth rate under time constraints. None have considered how species-specific length of the reproductive season affects larval developmental responses to time constraints. We tested in four Coenagrion damselfly species whether species with a longer reproductive season, facing a smaller threat of missing out on reproduction, react less to larval time constraints and pre-winter food shortage by accelerating development rate and growth rate, and therefore pay less physiological costs. All species increased development and growth rates under larval time constraints. The magnitude of this increase negatively correlated across species with the length of the reproductive season. Under larval time constraints, only the species exhibiting the longest reproductive season suffered a delayed emergence and a reduced investment in energy storage, yet also showed an increased immune function. Under a longer reproductive season, evolution may favor compensation for larval constraints after metamorphosis. Growth rate was accelerated after pre-winter food shortage to the same extent across species; effects on age and mass at emergence also did not differ among species. Time constraints associated with the length of the reproductive season may predictably contribute to species differences in their response to time constraints imposed in the larval stage. Our study adds empirical proof that the interplay of selective factors in the larval and adult stages may determine life-history plasticity with regard to larval time constraints.

Predator-driven trait diversification in a dragonfly genus: covariation in behavioral and morphological antipredator defense.

Proof for predation as an agent shaping evolutionary trait diversification is accumulating, however, our understanding how multiple antipredator traits covary due to phenotypic differentiation is still scarce. Species of the dragonfly genus Leucorrhinia underwent shifts from lakes with fish as top predators to fishless lakes with large dragonfly predators. This move to fishless lakes was accompanied by a partial loss and reduction of larval spines. Here, we show that Leucorrhinia also reduced burst swimming speed and its associated energy fuelling machinery, arginine kinase activity, when invading fishless lakes. This results in patterns of positive phylogenetic trait covariation between behavioral and morphological antipredator defense (trait cospecialization) and between behavioral antipredator defense and physiological machinery (trait codependence). Across species patterns of trait covariation between spine status, burst swimming speed and arginine kinase activity also matched findings within the phenotypically plastic L. dubia. Our results highlight the importance of predation as a factor affecting patterns of multiple trait covariation during phenotypic diversification.