David Outomuro

The Evolution of Wing Shape in Ornamented-Winged Damselflies (Calopterygidae, Odonata)

Flight has conferred an extraordinary advantage to some groups of animals. Wing shape is directly related to flight performance and evolves in response to multiple selective pressures. In some species, wings have ornaments such as pigmented patches that are sexually selected. Since organisms with pigmented wings need to display the ornament while flying in an optimal way, we might expect a correlative evolution between the wing ornament and wing shape. We examined males from 36 taxa of calopterygid damselflies that differ in wing pigmentation, which is used in sexual displays. We used geometric morphometrics and phylogenetic comparative approaches to analyse whether wing shape and wing pigmentation show correlated evolution. We found that wing pigmentation is associated with certain wing shapes that probably increase the quality of the signal: wings being broader where the pigmentation is located. Our results also showed correlated evolution between wing pigmentation and wing shape in hind wings, but not in front wings, probably because hind wings are more involved in signalling than front wings. The results imply that the evolution of diversity in wing pigmentations and behavioural sexual displays might be an important driver of speciation due to important pre-copulatory selective pressures.

Hind Wing Shape Evolves Faster than Front Wing Shape in Calopteryx Damselflies

Wing shape has been shown in a variety of species to be influenced by natural and sexual selection. In damselflies, front- and hind wings can beat independently, and functional differentiation may occur. Males of Calopteryx damselflies show species-specific nuptial flights that differ in colour signalling with the hind wings. Therefore, hind wing shape and colour may evolve in concert to improve colour display, independent of the front wings. We predicted that male hind wing shape evolves faster than front wing shape, due to sexual selection. Females do not engage in sexual displays, so we predicted that females do not show differences in divergence between front- and hind wing shape. We analysed the non-allometric component of wing shape of five European Calopteryx taxa using geometric morphometrics. We found a higher evolutionary divergence of hind wing shape in both sexes. Indeed, we found no significant differences in rate of evolution between the sexes, despite clear sex-specific differences in wing shape. We suggest that evolution of hind wing shape in males is accelerated by sexual selection on pre-copulatory displays and that this acceleration is reflected in females due to genetic correlations that somehow link the rates of wing shape evolution in the two sexes, but not the wing shapes themselves.

Wing shape allometry and aerodynamics in calopterygid damselflies: a comparative approach

BackgroundWing size and shape have important aerodynamic implications on flight performance. We explored how wing size was related to wing shape in territorial males of 37 taxa of the damselfly family Calopterygidae. Wing coloration was also included in the analyses because it is sexually and naturally selected and has been shown to be related to wing shape. We studied wing shape using both the non-dimensional radius of the second moment of wing area (RSM) and geometric morphometrics. Lower values of the RSM result in less energetically demanding flight and wider ranges of flight speed. We also re-analyzed previously published data on other damselflies and dragonflies.ResultsThe RSM showed a hump-shaped relationship with wing size. However, after correcting for phylogeny using independent contrast, this pattern changed to a negative linear relationship. The basal genus of the study family, Hetaerina, was mainly driving that change. The obtained patterns were specific for the study family and differed from other damselflies and dragonflies. The relationship between the RSM and wing shape measured by geometric morphometrics was linear, but relatively small changes along the RSM axis can result in large changes in wing shape. Our results also showed that wing coloration may have some effect on RSM.ConclusionsWe found that RSM showed a complex relationship with size in calopterygid damselflies, probably as a result of other selection pressures besides wing size per se. Wing coloration and specific behavior (e.g. courtship) are potential candidates for explaining the complexity. Univariate measures of wing shape such as RSM are more intuitive but lack the high resolution of other multivariate techniques such as geometric morphometrics. We suggest that the relationship between wing shape and size are taxa-specific and differ among closely-related insect groups.

Patterns of Phenotypic Divergence in Wing Covariance Structure of Calopterygid Damselflies

Comparing species differences in covariance patterns of traits subject to divergent selection pressures can increase our understanding to the mechanisms of phenotypic divergence. Different species of calopterygid damselflies have diverged in the melanized wing patch of males. This trait serves multiple ecological functions and has behavioral consequences in terms of sexual selection, interspecific interactions, reproductive isolation. We compared the phenotypic variance-covariance matrices (P) of wing traits among nine populations of four European species of calopterygid damselflies. We found modest divergence in covariance structure among populations of the same species, but strong divergence between species. Interestingly, the orientation of the first eigenvector of P (Pmax) differed more between closely related species than between distantly related species, although this pattern was absent when overall covariance structures were compared. We also found that distantly related species but geographically closer had converged towards a similar covariance structure. Finally, divergence in covariance structure was correlated with divergence in wing patch length, but not with other wing traits. This last finding suggests that divergent selection on wing patch length might have affected the stability of P. These results indicate that P might not only reflect ancestral developmental pathways but might also be influenced by current ecology.

Distribution of the Iberian Calopteryx Damselflies and Its Relation with Bioclimatic Belts: Evolutionary and Biogeographic Implications

Abstract Using bioclimatic belts as habitat and distribution predictors, the present study examines the implications of the potential distributions of the three Iberian damselflies, Calopteryx Leach (Odonata: Calopterygidae), with the aim of investigating the possible consequences in specific interactions among the species from a sexual selection perspective and of discussing biogeographical patterns. To obtain the known distributions, the literature on this genus was reviewed, relating the resulting distributions to bioclimatic belts. Specific patterns related to bioclimatic belts were clearly observed in the Mediterranean region. The potential distribution maps and relative frequencies might involve latitudinal differences in relative abundances, C. virgo meridionalis Sélys being the most abundant species in the Eurosiberian region, C. xanthostoma (Charpentier) in the northern half of the Mediterranean region and C. haemorrhoidalis (Vander Linden) in the rest of this region. These differences might explain some previously described latitudinal differences in secondary sexual traits in the three species. Changes in relative abundances may modulate interactions among these species in terms of sexual selection and may produce sexual character displacement in this genus. C. virgo meridionalis distribution and ecological requirements explain its paleobiogeography as a species which took refuge in Iberia during the Würm glaciation. Finally, possible consequences in species distributions and interactions are discussed within a global climate change context.

Bird predation selects for wing shape and coloration in a damselfly

Wing shape is related to flight performance, which is expected to be under selection for improving flight behaviours such as predator avoidance. Moreover, wing conspicuousness, usually involved in sexual selection processes, is also relevant in terms of predation risk. In this study, we examined how predation by a passerine bird, the white wagtail Motacilla alba, selects wing shape and wing colour patch size in males of the banded demoiselle Calopteryx splendens. The wing colour patch is intra‐ and intersexually selected in the study species. In a field study, we compared wings of live damselflies to wings of predated damselflies which are always discarded after predation. Based on aerodynamic theory and a previous study on wing shape of territorial tactics in damselflies, we predicted an overall short and broad wing, with a concave front margin shape to be selected by predation. This shape would be expected to improve escaping ability. Moreover, we predicted that wing patch size should be negatively selected by predation. We found that selection operated differently on fore‐ and hindwings. In contrast to our predictions, predation favoured a slender general forewing shape. However, the predicted wing shape was favoured in hindwings. We also found selection favouring a narrower wing colour patch. Our results suggest different roles of fore‐ and hindwings in flight, as previously suggested for Calopteryx damselflies and shown for butterflies and moths. Forewings would be more involved in sustained flight and hindwings in flight manoeuvrability. Our results differ somehow from a recently published work in the same study system, but using another population, suggesting that selection can fluctuate across space, despite the simplicity of this predator–prey system.

Habitat variation and wing coloration affect wing shape evolution in dragonflies.

Habitats are spatially and temporally variable, and organisms must be able to track these changes. One potential mechanism for this is dispersal by flight. Therefore, we would expect flying animals to show adaptations in wing shape related to habitat variation. In this work, we explored variation in wing shape in relation to preferred water body (flowing water or standing water with tolerance for temporary conditions) and landscape (forested to open) using 32 species of dragonflies of the genus Trithemis (80% of the known species). We included a potential source of variation linked to sexual selection: the extent of wing coloration on hindwings. We used geometric morphometric methods for studying wing shape. We also explored the phenotypic correlation of wing shape between the sexes. We found that wing shape showed a phylogenetic structure and therefore also ran phylogenetic independent contrasts. After correcting for the phylogenetic effects, we found (i) no significant effect of water body on wing shape; (ii) male forewings and female hindwings differed with regard to landscape, being progressively broader from forested to open habitats; (iii) hindwings showed a wider base in wings with more coloration, especially in males; and (iv) evidence for phenotypic correlation of wing shape between the sexes across species. Hence, our results suggest that natural and sexual selection are acting partially independently on fore‐ and hindwings and with differences between the sexes, despite evidence for phenotypic correlation of wing shape between males and females.

Male wing shape differs between condition-dependent alternative reproductive tactics in territorial damselflies

Territorial contests between males without weaponry are based on costly displays and can result in condition-dependent alternative reproductive tactics that maximize male fitness. Physiological and morphological traits such as fat content, body size or the expression of secondary sexual traits have been shown to contribute to male territory-holding potential. When territorial contests are based on flight displays, wing morphology is expected to contribute to the territory-holding potential of a male through its effects on flight performance. We explored whether wing shape contributed to the territory-holding potential of males of three species of Calopteryx damselflies. Males of these species show two distinct, condition-dependent behavioural tactics: territorial and nonterritorial. Previous studies have shown that territorial males have higher fitness than nonterritorial males. We used mark–recapture to determine male tactics within the populations and compared wing shape, size and wing coloured spot size (a secondary sexual trait) between tactics. Territorial males of all three species had shorter and slightly broader hindwings than nonterritorial males. In two species, forewings of territorial males were longer and broader than forewings of nonterritorial males. Wing size and wing spot size did not differ between tactics. We suggest that the wing shape of territorial males might confer better flight manoeuvrability, which would be advantageous for territorial contests. Therefore, wing shape is likely to be an important trait contributing to territory-holding potential in condition-dependent alternative reproductive tactics based on flight displays.

A potential pitfall in studies of biological shape: Does size matter?

The number of published studies using geometric morphometrics (GM) for analysing biological shape has increased steadily since the beginning of the 1990s, covering multiple research areas such as ecology, evolution, development, taxonomy and palaeontology. Unfortunately, we have observed that many published studies using GM do not evaluate the potential allometric effects of size on shape, which normally require consideration or assessment. This might lead to misinterpretations and flawed conclusions in certain cases, especially when size effects explain a large part of the shape variation. We assessed, for the first time and in a systematic manner, how often published studies that have applied GM consider the potential effects of allometry on shape. We reviewed the 300 most recent published papers that used GM for studying biological shape. We also estimated how much of the shape variation was explained by allometric effects in the reviewed papers. More than one-third (38%) of the reviewed studies did not consider the allometric component of shape variation. In studies where the allometric component was taken into account, it was significant in 88% of the cases, explaining up to 87.3% of total shape variation. We believe that one reason that may cause the observed results is a misunderstanding of the process that superimposes landmark configurations, i.e. the Generalized Procrustes Analysis, which removes isometric effects of size on shape, but not allometric effects. Allometry can be a crucial component of shape variation. We urge authors to address, and report, size effects in studies of biological shape. However, we do not propose to always remove size effects, but rather to evaluate the research question with and without the allometric component of shape variation. This approach can certainly provide a thorough understanding of how much size contributes to the observed shaped variation.

Antagonistic natural and sexual selection on wing shape in a scrambling damselfly.

Wings are a key trait underlying the evolutionary success of birds, bats, and insects. For over a century, researchers have studied the form and function of wings to understand the determinants of flight performance. However, to understand the evolution of flight, we must comprehend not only how morphology affects performance, but also how morphology and performance affect fitness. Natural and sexual selection can either reinforce or oppose each other, but their role in flight evolution remains poorly understood. Here, we show that wing shape is under antagonistic selection with regard to sexual and natural selection in a scrambling damselfly. In a field setting, natural selection (survival) favored individuals with long and slender forewings and short and broad hindwings. In contrast, sexual selection (mating success) favored individuals with short and broad forewings and narrow‐based hindwings. Both types of selection favored individuals of intermediate size. These results suggest that individuals face a trade‐off between flight energetics and maneuverability and demonstrate how natural and sexual selection can operate in similar directions for some wing traits, that is, wing size, but antagonistically for others, that is, wing shape. Furthermore, they highlight the need to study flight evolution within the context of species’ mating systems and mating behaviors.