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.     

Integrating large‐scale geographic patterns in flight morphology,flight characteristics and sexual selection in a range‐expanding damselfly

While geographic trait variation along environmental clines is widespread, associated patterns in sexual selection remain largely unexplored. Geographic patterns in sexual selection may be expected if 1) phenotypes vary geographically and sexual selection is dependent on the local phenotypes in the population, and if 2) sexual selection is influenced by geographically structured environmental conditions. We quantified geographic variation in flight‐related traits and flight performance in mated and unmated males and tested for geographic variation in sexual selection on these traits in the poleward range‐expanding damselfly Coenagrion scitulum across a set of eleven core and edge populations ordered along thermal gradients in the larval and in the adult stage. We found little support for trait differentiation between core and edge populations, instead we found considerable geographic trait variation along the larval and adult thermal gradients. As expected under time constraints, body mass decreased with shorter larval growth seasons. Lower temperatures during the adult flight period were associated with a higher body mass, a higher flight speed and a higher fat content; these traits likely evolved to buffer flight ability at suboptimal temperatures and to optimize starvation resistance. Across the large geographic scale, we found a consistent higher flight duration in mated males. Instead, sexual selection for higher fat content was stronger in populations with lower adult flight temperatures and sexual selection for lower body mass acted only in edge populations. Our results indicate sexual selection on flight performance to be consistent over a large geographic scale and this despite the clear geographic patterns in sexual selection on the underlying morphological traits. Our results highlight that to fully understand the fitness implications of geographically changing trait patterns, researchers should consider the entire phenotype–performance–fitness axis and incorporate effects of geographically structured life‐stage specific environmental conditions on this axis.     

Sexual selection and temporal phenotypic variation in a damselfly population

Temporal variation in selection can be generated by temporal variation in either the fitness surface or phenotypic distributions around a static fitness surface, or both concurrently. Here, we use within- and between-generation sampling of fitness surfaces and phenotypic distributions over 2 years to investigate the causes of temporal variation in the form of sexual selection on body size in the damselfly Enallagma aspersum. Within a year, when the average female body size differed substantially from the average male body size, male body size experienced directional selection. In contrast, when male and female size distributions overlapped, male body size experienced stabilizing selection when variances in body size were large, but no appreciable selection when the variances in body size were small. The causes of temporal variation in the form of selection can only be inferred by accounting for changes in both the fitness surface and changes in the distribution of phenotypes.     

Sexual selection,genital morphology,and copulatory behavior in male Galagos

Variations in penile morphology among galago species are pronounced and complex. Comparative studies of galagos and other primate species show that elongation of the baculum (os penis)is associated with copulatory patterns involving a prolonged period of intromission. The enlarged penile “spines” of male galagos may be important in maintaining a genital “lock” during copulation. In primate species where females mate with a number of partners, sexual selection may have favored the rapid evolution of such features of penile morphology and masculine copulatory behavior. It is suggested that evolution of complex penile morphologies in galagos has been influenced by sexual selection and that such morphological variations are extremely useful in taxonomic studies.     

Components of lifetime mating success and body size in males of a scrambling damselfly

Sexual selection is hypothesized to favour small body size in males of scrambling species, that is, those in which males obtain matings by actively searching for females. I tested this hypothesis in a natural population of the scrambling emerald damselfly, Lestes sponsa. Mating efficiency (matings/visit to the pond) was the most important factor explaining variation in male lifetime mating success (LMS; 71%). This suggests a large potential for sexual selection. Path analysis of male LMS suggested a quality factor that positively affected both mating efficiency and life span. In contrast with the small-male mating advantage hypothesis, part of this potential for sexual selection was realized as stabilizing selection on male body size, indicating that there may also be a lower limit to body size for mating efficiency. This also illustrates that the constancy of body size may be explained by sexual selection alone. Survival explained about 20% of the variation in LMS and random processes were potentially important for determining LMS. My results show the problems of using mating efficiency as a measure for the intensity of sexual selection and the need to distinguish between potential and realized selection pressures, especially when comparing the importance of natural and sexual selection. I discuss mechanisms that may have caused the intermediate-male mating advantage in this scrambling species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sexual selection and the evolution of sperm morphology in sharks

Post‐copulatory sexual selection, and sperm competition in particular, is a powerful selective force shaping the evolution of sperm morphology. Although mounting evidence suggests that post‐copulatory sexual selection influences the evolution of sperm morphology among species, recent evidence also suggests that sperm competition influences variation in sperm morphology at the intraspecific level. However, contradictory empirical results and limited taxonomic scope have led to difficulty in assessing the generality of sperm morphological responses to variation in the strength of sperm competition. Here, we use phylogenetically controlled analyses to explore the effects of sperm competition on sperm morphology and variance in sharks, a basal vertebrate group characterized by wide variation in rates of multiple mating by females, and consequently sperm competition risk. Our analyses reveal that shark species experiencing greater levels of sperm competition produce sperm with longer flagella and that sperm flagellum length is less variable in species under higher sperm competition risk. In contrast, neither the length of the sperm head and midpiece nor variation in sperm head and midpiece length was associated with sperm competition risk. Our findings demonstrate that selection influences both the inter‐ and intraspecific variation in sperm morphology and suggest that the flagellum is an important target of sexual selection in sharks. These findings provide important insight into patterns of selection on the ejaculate in a basal vertebrate lineage.     

Morphological and physiological sexual selection targets in a territorial damselfly

• 1 Several morphological and physiological traits may shape fitness through the same performance measure. In such cases, differentiating between a scenario of many‐to‐one mapping, where phenotypic traits independently shape fitness leading to functional redundancy, and a scenario where traits strongly covary among each other and fitness, is needed.
• 2 A multivariate approach was used, including morphological and physiological traits related to flight ability, a crucial performance measure in flying insects, to identify independent correlates of short‐term mating success (mated versus unmated males) in the territorial damselfly Lestes viridis.
• 3 Males with higher flight muscle mass, higher relative thorax mass, and more symmetrical hindwings, all traits presumably linked to manoeuvrability, were more likely to be mated. Unexpectedly, although relative thorax mass is often used as a proxy for flight muscle mass, both traits were selected for independently. Mated males had a higher thorax fat content than unmated males, possibly because of enhanced flight endurance.
• 4 The finding of several independent targets of sexual selection linked to flight ability is consistent with a scenario of many‐to‐one mapping between phenotype and performance. Identifying such a scenario is important, because it may clarify situations where animals may show suboptimal values for some phenotypic traits shaping a performance measure, while still having high performance and fitness. We argue in the discussion that the functional approach of sexual selection provides a potent tool for examining unresolved issues in both sexual selection theory, as well as life‐history theory.

     

Higher investment in flight morphology does not trade off with fecundity estimates in a poleward range‐expanding damselfly

1. Evolutionary increases in dispersal‐related traits are frequently documented during range expansions. Investment in flight‐related traits is energetically costly and a trade‐off with fecundity may be expected during range expansion. 2. However, in contrast to wing‐dimorphic species, this trade‐off is not general in wing‐monomorphic species. In the absence of a dispersal‐‐fecundity trade‐off, an increased investment in clutch size at the expansion front is expected possibly at a cost of reduced offspring size. 3. The study evaluated investment in female flight morphology and fecundity‐related traits (clutch size, hatchling size) and potential trade‐offs among these traits in replicated populations of the poleward range‐expanding damselfly Coenagrion scitulum. 4. Females at the expansion front had a higher relative thorax length, indicating an increased investment in flight; this can be explained by spatial sorting of dispersal ability or in situ natural selection at the expansion front. Edge females produced larger hatchlings, however, this pattern was totally driven by the population‐specific thermal larval regimes and could not be attributed to the range expansion per se. By contrast, clutch sizes did not differ between core and edge populations. There was no signal of a dispersal–fecundity trade‐off either for a trade‐off between clutch size and hatchling size. 5. These results indicate that evolution of a higher dispersal ability at the expansion front of C. scitulum does not trade off with investment in fecundity, hence a dispersal–fecundity trade‐off is unlikely to slow down range expansion of this species.     

The effects of latitude,body size,and sexual selection on wing shape in a damselfly

Under natural selection, wing shape is expected to evolve to optimize flight performance. However, other selective factors besides flight performance may influence wing shape. One such factor could be sexual selection in wing sexual ornaments, which may lead to alternative variations in wing shape that are not necessarily related to flight performance. In the present study, we investigated wing shape variations in a calopterygid damselfly along a latitudinal gradient using geometric morphometrics. Both sexes show wing pigmentation, which is a known signal trait at intra‐ and interspecific levels. Wing shape differed between sexes and, within the same sex, the shape of the hind wing differed from the front wing. Latitude and body size explained a high percentage of the variation in wing shape for female front and hind wings, and male front wings. In male hind wings, wing pigmentation explained a high amount of the variation in wing shape. On the other hand, the variation in shape explained by pigmentation was very low in females. We suggest that the conservative morphology of front wings is maintained by natural selection operating on flight performance, whereas the sex‐specific differences in hind wings most likely could be explained by sexual selection. The observed sexual dimorphism in wing shape is likely a result of different sex‐specific behaviours. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 263–274.     

Sexual dimorphism in the pyrgomorphid grasshopper Phymateus morbillosus: from wing morphometry and flight behaviour to flight physiology and endocrinology

Abstract In the field, adult males of the grasshopper Phymateus morbillosus are able to fly for up to 1 min and cover up to c. 100 m, whereas females, although fully winged, are apparently unable to get airborne. Morphometric data indicate that the males are lighter, have longer wings, a higher ratio of flight muscles to body mass, and a lower wing load value than females. It was investigated whether this inability of females to fly is related to fuel storage, flight muscle enzymatic design and/or the presence and quantitative capacity of the endocrine system to mobilize fuels. In both sexes, readily available potential energy substrates are present in the haemolymph in similar concentrations, and the amount of glycogen in flight muscles and fat bodies does not differ significantly between males and females. Mass-specific activities of the enzymes GAPDH (glycolysis), HOAD (fatty acid oxidation) and MDH (citric acid cycle) in flight muscles are significantly lower in females compared with males, and mitochondria are less abundant in the flight muscles of females. There is no significant difference between the ability of the two sexes to oxidize various important substrates. Both sexes contain three adipokinetic peptides in their corpora cardiaca; the amount of each peptide in female grasshoppers is higher than in males.
Thus, despite some differences listed above, both sexes appear to have sufficient substrates and the necessary endocrine complement to engage in flight. It seems more likely, from the morphometric data above, that the chief reason for flightlessness is that P. morbillosus females cannot produce sufficient lift for flight; alternatively, the neuronal functioning associated with the flight muscles may be impaired in females.     

Sexual selection by cryptic female choice on male seminal products - a new bridge between sexual selection and reproductive physiology

Selection clearly focuses on differences in reproduction, but studies of reproductive physiology generally have been carried out in a near vacuum of modern evolutionary theory. This lack of contact between the two fields may be about to change. New ideas indicate that sexual selection by cryptic female choice has affected the evolution of products in male semen that influence female reproductive behavior and physiology.     

Integrating life history and physiology to understand latitudinal size variation in a damselfly

Our understanding of latitudinal life history patterns may benefit by jointly considering age and mass at maturity and growth rate. Additional insight may be gained by exploring potential constraints through pushing growth rates to their maximum and scoring physiological cost‐related variables. Therefore, we reared animals of a univoltine Spanish and Belgian population and of a semivoltine Swedish population of the damselfly Enallagma cyathigerum (spanning a latitude gradient of ca 2350 km) in a common environment from the eggs until adult emergence and exposed them to a transient starvation period to induce compensatory growth. Besides age and mass at maturity and growth rate we also scored investment in energy storage (i.e. triglycerides) and immune function (i.e. total activity of phenoloxidase). At emergence, body mass was greater in Spain and Sweden and lower in Belgium, suggesting a genetic component for the U‐shaped latitudinal pattern that was found also in a previous study based on field‐collected adults. The mass difference between univoltine populations can be explained by the shorter development time in the Belgian population, and this despite a higher growth rate, a pattern consistent with undercompensating countergradient variation. In line with the assumed shorter growth seasons, Belgian and Swedish animals showed higher routine growth rates and compensatory growth after transient starvation. Despite a strong link with metabolic rates (as measured by oxygen consumption) populations with higher routine growth rates had no lower fat content and had higher immune function (i.e. immune function decreased from Sweden to Spain), which was unexpected. Rapid compensatory growth did, however, result in a lowered immune function. This may contribute to the absence of perfect compensating countergradient variation in the Belgian population and the lowest routine growth rates in the Spanish population. Our results underscore the importance of integrating key life historical with physiological traits for understanding latitudinal population differentiation.     

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.     

Pesticide exposure affects flight dynamics and reduces flight endurance in bumblebees

The emergence of agricultural land use change creates a number of challenges that insect pollinators, such as eusocial bees, must overcome. Resultant fragmentation and loss of suitable foraging habitats, combined with pesticide exposure, may increase demands on foraging, specifically the ability to collect or reach sufficient resources under such stress. Understanding effects that pesticides have on flight performance is therefore vital if we are to assess colony success in these changing landscapes. Neonicotinoids are one of the most widely used classes of pesticide across the globe, and exposure to bees has been associated with reduced foraging efficiency and homing ability. One explanation for these effects could be that elements of flight are being affected, but apart from a couple of studies on the honeybee (Apis mellifera), this has scarcely been tested. Here, we used flight mills to investigate how exposure to a field realistic (10 ppb) acute dose of imidacloprid affected flight performance of a wild insect pollinator—the bumblebee, Bombus terrestris audax. Intriguingly, observations showed exposed workers flew at a significantly higher velocity over the first ¾ km of flight. This apparent hyperactivity, however, may have a cost because exposed workers showed reduced flight distance and duration to around a third of what control workers were capable of achieving. Given that bumblebees are central place foragers, impairment to flight endurance could translate to a decline in potential forage area, decreasing the abundance, diversity, and nutritional quality of available food, while potentially diminishing pollination service capabilities.     

Sexual selection in gallus: Effects of morphology and dominance on female spatial behavior

Sexual selection has received a great deal of attention from field and laboratory researchers for over a century, but hard evidence of female choice of mates in mixed-sex groups remains scarce. Dominant males typically mate much more often than subordinants but evidence that females “choose” such males is elusive. In $\text{Gallus}$, which includes junglefowl and their domestic fowl descendants, females stay near and mate with dominant, territorial males. We demonstrate here that $\text{Gallus}$ females in mixed-sex flocks who have no information about the social dominance status of males orient to, approach and stay near males with larger than average combs whereas females which $\text{do}$ not have information about male dominance orient toward and stay near high ranking males. We verify that comb size correlates with male social rank. Hence, $\text{Gallus}$ females do actively respond to “high quality” males; they apparently identify such males by male physical characteristics and, if available, information concerning male-male interactions.     

Sexual comparisons in immune ability, survival and parasite intensity in two damselfly species

Recent evolutionary studies have suggested that females have a more robust immune system than males. Using two damselfly species (Hetaerina americana and Argia tezpi), we tested if females produced higher immune responses (as phenoloxidase and hydrolytic enzymes), had a higher survival (using a nylon implant inserted in the abdomen and measuring survival after 24h) and fewer parasites (gregarines and water mites) than males. We also tested whether immune differences should emerge in different body areas (thorax vs. abdomen) within each sex with the prediction that only females will differ with the abdomen having a higher immune response than their thorax since the former area, for ecological and physiological reasons, may be a target zone for increased immune investment. Animals were adults of approximately the same age. In both species, females were more immunocompetent than males, but only in H. americana females were immune responses greater in the abdomen than in the thorax. However, there were no differences in survival and parasite intensity or the probability of being parasitised between the sexes in either of the two species. Thus, this study lends partial support to the principle that females are better at defending than males despite the null difference in parasitism and survival.     

Sexual size dimorphism,prey morphology and catch success in relation to flight mechanics in the peregrine falcon: a simulation study

In common with many other raptors, female peregrine falcons Falco peregrinus are about 50% heavier than males. Their sexual dimorphism is thought to allow breeding pairs to exploit a wider range of prey through a division of labor: the male being able to catch more maneuverable prey species; the female capable of carrying larger ones. Given the difficulty of assessing the catch success and load carrying capacity of both sexes of falcon in the field, we here adopt a novel approach to test the division‐of‐labor theory by using a detailed physics‐based flight simulator of birds. We study attacks by male and female peregrines on prey species ranging from small passerines to large ducks, testing how catch success relates to the flight performance of predator and prey. Males prove to be better than females at catching highly maneuverable prey in level flight, but the catch success of both sexes improves and becomes more similar when diving, because of the higher aerodynamic forces that are available to both sexes for maneuvering in high‐speed flight. The higher maximum roll acceleration of the male peregrine explains its edge over the female in catching maneuverable prey in level flight. Overall, catch success is more strongly influenced by the differences in maneuverability that exist between different species of prey than between the different sexes of falcon. On the other hand, the female can carry up to 50% greater loads than the male. More generally, our detailed simulation approach highlights the importance of several previously overlooked features of attack and escape. In particular, we find that it is not the prey's instantaneous maximum centripetal acceleration but the prey's ability to sustain a high centripetal acceleration for an extended period of time that is the primary driver of the variation in catch success across species.