Parallel Evolution in Ecological and Reproductive Traits to Produce Cryptic Damselfly Species Across the Holarctic

Abstract

The damselfly genus Enallagma originated in the Nearctic, and two Nearctic lineages recently underwent radiations partly associated with multiple independent habitat shifts from lakes dominated by fish predators into lakes dominated by dragonfly predators. A previous molecular study of four Palearctic morphospecies and all representative Nearctic species identified the presence of two cryptic species sets, with each set having Palearctic and Nearctic representatives. However, the cryptic species within each set are not sibling species. Here, we present quantitative data on ecologically important larval morphologies and behaviors involved in predator avoidance and on adult male morphological structures involved in mate recognition to quantify the phenotypic relationships among these cryptic species sets. For the adult stage, our data indicate strong parallel evolution of the structures involved in specific mate recognition-the male cerci. For the larval stage, morphometric analyses show that the Palearctic species evolved a nearly identical morphology to the sibling-clade members in the Nearctic that live in waters where dragonflies are the top predators. This implicates the importance of dragonfly predation in the history of the Palearctic clade. Behavioral analyses suggest population differentiation in response to the actual predator environment in the Palearctic clade, consistent with the species differentiation seen in the Nearctic. Our results suggest parallel evolution of adult traits that influence specific mate choice and larval traits that influence ecological performance underlie the striking similarity of Enallagma species across continents. This concurrent parallel evolution in both stages of a complex life cycle, especially when both stages do not share the same selective environment, may be a very unusual mechanism generating cryptic species.

Ontogeny of sexual dimorphism and phenotypic integration in heritable morphs

“…Our findings that most of this genetic variation is aligned along the size axis with less variation in shape is consistent with many other quantitative-genetic studies on other organisms (Schluter, 1996). The phenotypic correlations found here also confirm that larval and adult size and shape are related (Table 8), which has previously been shown for size (Harvey & Corbet, 1985;Banks & Thompson, 1987;Cordero, 1992b (Stoks et al, 2003;Stoks et al, 2005).…”

Genetic divergence predicts reproductive isolation in damselflies

“…Despite the solid number of studies investigating this topic, notable taxonomic gaps exist. Odonates make an important contribution to our general understanding of whether the relationship holds across diverse groups, because they represent the most ancient winged insects order and also a group where sexual selection had a large effect on the diversification process (McPeek & Brown, ; Svensson, ), with sometimes little evidence of niche diversification between closely related species (Stoks et al ., ; Wellenreuther et al ., ). Here, we directly test for an isolation–divergence correlation in 30 species pairs of damselflies and report a positive association across a wide range of values.…”

Regional divergence and mosaic spatial distribution of two closely related damselfly species (Enallagma hageniandEnallagma ebrium)

“…Moreover, multiple appearances of the same reproductive structure have already been observed in Enallagma . For example, Palaearctic E. cyathigerum and Neartic E. annexum were previously regarded as one species on the basis of highly similar cerci (Westfall & May, 1996); however, phylogenetic relationships clearly show that they are highly divergent species and that the same cerci morphology very likely evolved twice (Stoks et al. , 2005; Turgeon et al.…”