Yuma Takahashi

NEGATIVE FREQUENCY-DEPENDENT SELECTION IN FEMALE COLOR POLYMORPHISM OF A DAMSELFLY

Negative frequency‐dependent selection (NFDS) is one of the most powerful selective forces maintaining genetic polymorphisms in nature. Recently many prospective cases of polymorphisms by NFDS have been reported. Some of them are very complicated, although strongly supportive of the NFDS. Here we investigate NFDS in wild populations of the dimorphic damselfly Ischnura senegalensis, in which females occur as andromorphs and gynomorphs. Specifically, we (1) test fitness responses to morph frequencies, (2) built a simple population genetic model, and (3) compare the observed and predicted morph‐frequency dynamics. Fitnesses of the two morphs are an inverse function of its own frequency in a population, and are about equal when their frequencies are similar. Thus the conditions necessary for NFDS are satisfied. The long‐term field surveys show that the morph frequencies oscillate with a period of two generations. Morph frequencies in a small population undergo large oscillations whereas those in a large population do small oscillations. The demographic properties of the observed dynamics agree well with those of our model. This example is one of the simplest confirmed cases of NFDS maintaining genetic polymorphisms in nature.

Female reproductive success is affected by selective male harassment in the damselfly Ischnura senegalensis

In animals without any courtship behaviour, persistent mating attempts by males are frequently observed. Male harassment affects female reproductive success in the laboratory, but few studies have evaluated the costs of male harassment in the wild. In the damselfly Ischnura senegalensis, females exhibit colour dimorphism (andromorph and gynomorph), and the morph frequency varies between local populations. In two populations where gynomorphs were common, we found that males harassed more gynomorphs than andromorphs throughout their daily foraging and oviposition activity period. Gynomorphs excreted less faeces than andromorphs, indicating that preferential harassment of gynomorphs decreased their food intake. Gynomorphs also produced fewer eggs than andromorphs. As a result, gynomorphs laid 35% fewer eggs per day than andromorphs, suggesting that male harassment decreased their reproductive success.

Evolution of increased phenotypic diversity enhances population performance by reducing sexual harassment in damselflies.

The effect of evolutionary changes in traits and phenotypic/genetic diversity on ecological dynamics has received much theoretical attention; however, the mechanisms and ecological consequences are usually unknown. Female-limited colour polymorphism in damselflies is a counter-adaptation to male mating harassment, and thus, is expected to alter population dynamics through relaxing sexual conflict. Here we show the side effect of the evolution of female morph diversity on population performance (for example, population productivity and sustainability) in damselflies. Our theoretical model incorporating key features of the sexual interaction predicts that the evolution of increased phenotypic diversity will reduce overall fitness costs to females from sexual conflict, which in turn will increase productivity, density and stability of a population. Field data and mesocosm experiments support these model predictions. Our study suggests that increased phenotypic diversity can enhance population performance that can potentially reduce extinction rates and thereby influence macroevolutionary processes.

A geographic cline induced by negative frequency-dependent selection

BackgroundEstablishment of geographic morph frequency clines is difficult to explain in organisms with limited gene flow. Balancing selection, such as negative frequency-dependent selection (NFDS), is instead suggested to establish a morph frequency cline on a geographic scale at least theoretically. Here we tested whether a large-scale smooth cline in morph frequency is established by NFDS in the female-dimorphic damselfly, Ischnura senegalensis, where andromorphs and gynomorphs are maintained by NFDS.ResultsWe found a large-scale latitudinal cline in the morph frequency: andromorph frequency ranged from 0.05 (South) to 0.79 (North). Based on the empirical data on the numbers of eggs, the number of ovariole, abdomen length and latitude, the potential fitness of andromorphs was estimated to be lower than that of gynomorphs in the south, and higher in the north, suggesting the gene-by-environment interaction. From the morph-specific latitudinal cline in potential fitness, the frequency of andromorphs was expected to shift from 0 to 1 without NFDS, because a morph with higher potential fitness wins completely and the two morphs will switch at some point. In contrast, NFDS led to the coexistence of two morphs with different potential fitness in a certain geographic range along latitude due to rare morph advantage, and resulted in a smooth geographic cline of morph frequency.ConclusionOur results provide suggestive evidence that the combination of NFDS and gene-by-environment interaction, i.e., multi-selection pressure on color morphs, can explain the geographic cline in morph frequency in the current system.

Diurnal changes and frequency dependence in male mating preference for female morphs in the damselfly Ischnura senegalensis (Rambur) (Odonata : Coenagrionidae)

Ischnura senegalensis females exhibit color dimorphism, consisting of an andromorph and a gynomorph, which might be maintained under a frequency‐dependent process of mating harassment by mate‐searching males. Males change their mating preference for female morph depending on prior copulation experience. Binary choice experiments between two female morphs were carried out in four local populations in the early morning (07.00–09.00 hours) and the afternoon (12.00–14.00 hours), times which mark the onset and the end of diurnal mating activity, respectively. According to the line census along the waters edge, the proportion of andromorphs in the female population varied from 21 to 67% throughout the survey period for four local populations. Males showed non‐biased preference for female morphs in the early morning in each local population, while they chose the common morph in the afternoon. Male mating preference for female morphs was positively correlated to the proportion of female morphs in the population. If the selective mating attacks on the common female morphs inhibit their foraging and/or oviposition behavior, frequency‐dependent male mating attacks might provide a selective force for maintaining the female color dimorphism in I. senegalensis.

Male mate choice based on ontogenetic colour changes of females in the damselfly Ischnura senegalensis

While male mate choice behaviour has been reported in many taxa, little is known about its plasticity and evolutionary consequences. In the damselfly Ischnura senegalensis, females exhibit colour dimorphism (gynomorph and andromorph). The body colour of gynomorphs changed ontogenetically in accordance with sexual maturation, while little change occurred in andromorphs. To test the male mate choice between sexually immature and mature females of both morphs, binary choice experiments were conducted. Virgin males that were reared separately from females after emergence did not show significant preference between sexually immature and mature females for both morphs, indicating that virgin males were unable to discriminate female reproductive status. On the other hand, males that had experienced copulation with gynomorphs preferred sexually mature gynomorphs to sexually immature ones. However, males that had experienced copulation with andromorphs could not discriminate between sexually immature and mature andromorphs, probably due to the absence of significant ontogenetic change in their thoracic colour. Therefore, female body colour is an important cue for males in discriminating between sexual maturation stages. Learned mate discrimination depending on copulation experience might help males to detect potential mates effectively and avoid sexually unreceptive immature female. We finally discuss the adaptive significance of the ontogenetic colour change in females.

Morph-Specific Fecundity and Egg Size in the Female-Dimorphic Damselfly Ischnura senegalensis

Females of coenagrionid damselflies exhibit color dimorphism, consisting of an andromorph and a gynomorph. This study compared reproductive traits between the female morphs in both field-captured and laboratory-reared females of the female-dimorphic damselfly Ischnura senegalensis. No difference was found in the onset of egg development between the morphs. The andromorphs developed significantly smaller mature eggs and had significantly more immature eggs than the gynomorphs. These results suggest that the andromorphs are r-strategists (high fecundity with small eggs), whereas the gynomorphs are K-strategists (low fecundity with large eggs). Fecundity and egg size might determine the quantity and quality of the offspring, respectively, indicating that morph-specific reproductive traits would contribute to the overall fitness of each female morph, and consequently be key factors affecting morph frequency in a population.

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.

Sexual selection on wing interference patterns in Drosophila melanogaster.

Significance Recently, it was discovered that small insects like flies and wasps, with seemingly transparent wings, display vivid coloration against dark backgrounds because of so-called “wing interference patterns” (WIPs). It was proposed that such wing coloration could function in sexual selection and species recognition, but direct evidence for this hypothesis has been lacking. Here, to our knowledge we present the first experimental evidence that WIPs in male Drosophila melanogaster are targets of mate choice from females. Comparison of attractiveness of different male WIPs between black and white backgrounds revealed that two different color traits, saturation and hue, experience directional and stabilizing sexual selection, respectively. Our results suggest that vivid coloration in WIPs is a target of mate choice and might have evolved by sexual selection. Animals with color vision use color information in intra- and interspecific communication, which in turn may drive the evolution of conspicuous colored body traits via natural and sexual selection. A recent study found that the transparent wings of small flies and wasps in lower-reflectance light environments display vivid and stable structural color patterns, called “wing interference patterns” (WIPs). Such WIPs were hypothesized to function in sexual selection among small insects with wing displays, but this has not been experimentally verified. Here, to our knowledge we present the first experimental evidence that WIPs in males of Drosophila melanogaster are targets of mate choice from females, and that two different color traits—saturation and hue—experience directional and stabilizing sexual selection, respectively. Using isogenic lines from the D. melanogaster Genetic Reference Panel, we compare attractiveness of different male WIPs against black and white visual backgrounds. We show that males with more vivid wings are more attractive to females than are males with dull wings. Wings with a large magenta area (i.e., intermediate trait values) were also preferred over those with a large blue or yellow area. These experimental results add a visual element to the Drosophila mating array, integrating sexual selection with elements of genetics and evo-devo, potentially applicable to a wide array of small insects with hyaline wings. Our results further underscore that the mode of sexual selection on such visual signals can differ profoundly between different color components, in this case hue and saturation.

Antagonistic selection factors induce a continuous population divergence in a polymorphism

Understanding the relative importance of selection and stochastic factors in population divergence of adaptive traits is a classical topic in evolutionary biology. However, it is difficult to separate these factors and detect the effects of selection when two or more contrasting selective factors are simultaneously acting on a single locus. In the damselfly Ischnura senegalensis, females exhibit color dimorphism and morph frequencies change geographically. We here evaluated the role of selection and stochastic factors in population divergence of morph frequencies by comparing the divergences in color locus and neutral loci. Comparisons between population pairwise FST for neutral loci and for the color locus did not detect any stochastic factors affecting color locus. Although comparison between population divergence in color and neutral loci using all populations detected only divergent selection, we detected two antagonistic selective factors acting on the color locus, that is, balancing and divergent selection, when considering geographical distance between populations. Our results suggest that a combination of two antagonistic selective factors, rather than stochastic factors, establishes the geographic cline in morph frequency in this system.