Differences in Mating Propensity Between Immature Female Color Morphs in the Damselfly Ischnura elegans (Insecta: Odonata)

Female-limited color polymorphisms occur in a variety of animal taxa where excessive male sexual harassment may explain the coexistence of multiple female color morphs. In the color polymorphic damselfly Ischnura elegans, mature and immature female color morphs coexist at the mating site where males are in search for suitable mating partners. Here, we study male preference and female mating propensity for the two immature female morphs. As would be expected, compared to mature morphs, both immature female morphs mate much less. Within immature females, one morph consistently mates more frequently compared to the other morph, a pattern that is similar for the ontogenetically corresponding mature female morphs. Preference experiments with the two differently colored immature female morphs, however, did not indicate male mate preference for either morph. Low mating frequencies of immature females at natural sites in combination with relatively high attractiveness of immature models in terms of male preference indicate that female behavior influences female mating success.     

Female prereproductive coloration reduces mating harassment in damselflies

Conspicuous female coloration can evolve through male mate choice or via female-female competition thereby increasing female mating success. However, when mating is not beneficial, such as in pre-reproductive females, selection should favor cryptic rather than conspicuous coloration to avoid male detection and the associated harassment. Nevertheless, conspicuous female coloration occurs in many prereproductive animals, and its evolution remains an enigma. Here, I studied conspicuous female coloration in Agriocnemis femina damselflies, in which the conspicuous red color of the immature females changes to a less conspicuous green approximately a week after their emergence. I measured body size, weight, and egg numbers of the female morphs and found that red females are smaller and lighter and do not carry developed eggs. Finally, I calculated the occurrence frequency and mating frequency of red and green females in several populations over a three-year period. The results demonstrate that red females mated less frequently than green females even when red females were the abundant morph in the populations. I concluded that conspicuous female coloration is likely to function as a warning signal of sexual unprofitability, thereby reducing sexual harassment for females and unprofitable mating for males.     

Why are female color polymorphisms rare in territorial damselflies?

In nonterritorial damselflies, females often come in multiple color morphs, perhaps because females with rare colors experience reduced sexual harassment, and thus have a frequency‐dependent fitness advantage, compared to females of the most common color morph, but such polymorphisms are rare in territorial species. We consider three hypotheses to explain the rarity of female color polymorphisms in territorial species: (a) misdirected male aggression, (b) poor male mate recognition, and (c) low mating harassment rates. The first hypothesis has some empirical support, and can account for the absence of andromorphs (i.e., females that resemble males), but does not explain the absence of multiple heteromorphs. We tested the second hypothesis by presenting females of two novel color morphs (green‐ or red‐banded abdomens) to territorial male Hetaerina capitalis. Females of both novel color morphs elicited fewer sexual responses than control females, and the red morph occasionally elicited aggressive responses. These results indicate that novel female color morphs would experience reduced mating harassment in this species, contradicting the hypothesis that male mate recognition is too poorly developed to reduce harassment of novel female morphs. By process of elimination, the third hypothesis, that harassment rates are too low in territorial species to provide rare female morphs a fitness advantage, is favored, but remains untested. Our findings also suggest that the common practice of color‐marking odonates for behavioral research is likely to interfere with mate choice, as has long been known to be the case in birds.     

Male mate choice based on ontogenetic colour changes of females in the damselfly <Emphasis Type="Italic">Ischnura senegalensis</Emphasis>

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.     

Evolution of female colour polymorphism in damselflies: testing the hypotheses

The existence of several female colour morphs is a conspicuous characteristic of many damselflies that show one male-like (androchrome) and several nonmale-like (gynochrome) morphs. We tested several adaptive hypotheses and the null model for the maintenance of female polychromatism (one androchrome and two gynochromes) in the damselfly Ceriagrion tenellum. We tested the null model by comparing the degree of genetic differentiation between the colour locus and a set of 19 neutral RAPD loci in five populations. Our results indicate that selection is acting to maintain similar frequencies between populations at the colour locus. Using mark–recapture techniques we found that mating success is not dependent on female coloration. We tested the mimicry hypothesis by presenting live and dead models to males. Dead models were highly attractive irrespective of coloration. In contrast, with live models males could not distinguish between androchromes and other males, and were more attracted to gynochrome females. Despite this, within populations morph frequencies remained constant over time and mating was at random with respect to female coloration. However, there was a positive relationship between male density and androchrome frequency in a comparative study of eight populations. We discuss our results in the framework of sexual conflict theory and suggest that andro- and gynochrome females are using different strategies to control their number of matings. The different morphs might be maintained in a balanced polymorphism by a combination of density- and frequency-dependent mechanisms.Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

Temperature drives pre‐reproductive selection and shapes the biogeography of a female polymorphism

Conflicts of interests between males and females over reproduction is a universal feature of sexually reproducing organisms and has driven the evolution of intersexual mimicry, mating behaviours and reproductive polymorphisms. Here, we show how temperature drives pre‐reproductive selection in a female colour polymorphic insect that is subject to strong sexual conflict. These species have three female colour morphs, one of which is a male mimic. This polymorphism is maintained by frequency‐dependent sexual conflict caused by male mating harassment. The frequency of female morphs varies geographically, with higher frequency of the male mimic at higher latitudes. We show that differential temperature sensitivity of the female morphs and faster sexual maturation of the male mimic increases the frequency of this morph in the north. These results suggest that sexual conflict during the adult stage is shaped by abiotic factors and frequency‐independent pre‐reproductive selection that operate earlier during ontogeny of these female morphs.     

Tests of search image and learning in the wild: Insights from sexual conflict in damselflies

Search image formation, a proximal mechanism to maintain genetic polymorphisms by negative frequency‐dependent selection, has rarely been tested under natural conditions. Females of many nonterritorial damselflies resemble either conspecific males or background vegetation. Mate‐searching males are assumed to form search images of the majority female type, sexually harassing it at rates higher than expected from its frequency, thus selectively favoring the less common morph. We tested this and how morph coloration and behavior influenced male perception and intersexual encounters by following marked Ischnura elegans and noting their reactions to conspecifics. Contrary to search image formation and associative learning hypotheses, although males encountered the minority, male‐like morph more often, sexual harassment and clutch size were similar for both morphs. Prior mating attempts or copula with morphs did not affect a male''s subsequent reaction to them; males rarely attempted matings with immature females or males. Females mated early in the day, reducing the opportunity for males to learn their identity beforehand. Once encountered, the male‐like morph was more readily noticed by males than the alternative morph, which once noticed was more likely to receive mating attempts. Flexible behavior gave morphs considerable control over their apparency to males, influencing intersexual encounters. Results suggested a more subtle proximal mechanism than male learning maintains these color polymorphisms and call for inferences of learning to be validated by behavior of wild receivers and their signalers.     

Female Colour Polymorphism: Gender and the Eye of the Beholder in Damselflies

Damselflies provide a classic example of female colour polymorphism. Usually, one female morph resembles the blue male colour (andromorph) while one, or more, female morphs are seen as typically female (gynomorph). Damselfly species fall in two distinct groups with respect to recent developments in mimicry theory: in some species females are perfect, they match male colouration and black patterning, and in other species they are supposed to be imperfect mimics, only matching male colouration. However, the underlying assumption of one female morph looking male-like is mostly based on human vision. Therefore we investigated the black patterning and colour of the three female morphs in Coenagrion puella, an imperfect mimic, using image analysis. In C. puella the blue female morph is perceived as male-like. We found that the black patterning of such females cannot be distinguished from the other female morphs, and is clearly different from males. Furthermore, the blue colour of andromorph females differs from the blue colour of males. Intriguingly, however, the red content did not differ between blue males and females.     

Alternative reproductive strategies and the maintenance of female color polymorphism in damselflies

Genetic polymorphisms are powerful model systems to study the maintenance of diversity in nature. In some systems, polymorphisms are limited to female coloration; these are thought to have arisen as a consequence of reducing male mating harassment, commonly resulting in negative frequency‐dependent selection on female color morphs. One example is the damselfly Ischnura elegans, which shows three female color morphs and strong sexual conflict over mating rates. Here, we present research integrating male tactics, and female evolutionary strategies (female mating behavior and morph‐specific female fecundity) in populations with different morph‐specific mating frequencies, to obtain an understanding of mating rates in nature that goes beyond the mere measure of color frequencies. We found that female morph behavior differed significantly among but not within morphs (i.e., female morph behavior was fixed). In contrast, male tactics were strongly affected by the female morph frequency in the population. Laboratory work comparing morph‐specific female fecundity revealed that androchrome females have lower fecundity than both of the gynochrome female morphs in the short term (3‐days), but over a 10‐day period one of the gynochrome female morphs became more fecund than either of the other morphs. In summary, our study found sex‐specific dynamics in response to different morph frequencies and also highlights the importance of studying morph‐specific fecundities across different time frames to gain a better understanding of the role of alternative reproductive strategies in the maintenance of female‐limited color polymorphism.     

Spectral Sensitivities and Color Signals in a Polymorphic Damselfly

Animal communication relies on conspicuous signals and compatible signal perception abilities. Good signal perception abilities are particularly important for polymorphic animals where mate choice can be a challenge. Behavioral studies suggest that polymorphic damselflies use their varying body colorations and/or color patterns as communication signal for mate choice and to control mating frequencies. However, solid evidence for this hypothesis combining physiological with spectral and behavioral data is scarce. We investigated this question in the Australian common blue tail damselfly, Ischnura heterosticta, which has pronounced female-limited polymorphism: andromorphs have a male-like blue coloration and gynomorphs display green/grey colors. We measured body color reflectance and investigated the visual capacities of each morph, showing that I. heterosticta have at least three types of photoreceptors sensitive to UV, blue, and green wavelength, and that this visual perception ability enables them to detect the spectral properties of the color signals emitted from the various color morphs in both males and females. We further demonstrate that different color morphs can be discriminated against each other and the vegetation based on color contrast. Finally, these findings were supported by field observations of natural mating pairs showing that mating partners are indeed chosen based on their body coloration. Our study provides the first comprehensive evidence for the function of body coloration on mate choice in polymorphic damselflies.     

Cues for Mate Recognition and the Effect of Prior Experience on Mate Recognition in Enallagma Damselflies

In many coenagrionid damselflies, sexually mature females exhibit color polymorphisms, with some females resembling conspecific males. Although it has been suggested that the latter function as male mimics, this does not appear to be the case for those in the genus Enallagma. We found that sexually dimorphic coloration of the female abdomen and thorax are important cues for sexual recognition by males. We demonstrate for the first time in the Odonata, that males learn to recognize andromorphs as potential mates. After 2 days in an enclosure, sexually mature males exposed to only andromorphic females initiated more sexual interactions with tethered andromorphs than with heteromorphs, the majority morph in the natural population. Exposure to only heteromorphic females tended to decrease males' sexual responses to andromorphs, but not significantly so. Because the frequency of female morphs often varies within a population, learned mate recognition would be advantageous for males that search for mates. Our results lead to a novel, frequency-dependent hypothesis for the occurrence and maintenance of female-limited color polymorphisms.     

Maintenance of a female-limited polymorphism in Ischnura ramburi (Zygoptera: Coenagrionidae)

Colour polymorphisms can be maintained in a population if all morphs have equal fitness on average, if fitness is frequency dependent or if fitness functions cross for some environmental or social variable. We studied female-limited colour polymorphism in the Rambur's forktail damselfly, Ischnura ramburi, in which one female morph looks like the male. The most commonly cited hypotheses to explain this polymorphism involve an advantage to andromorphs of avoiding costly matings through male mimicry. An alternative hypothesis argues that males learn the most common morph and that the polymorphism is maintained by a rare-morph advantage of mating avoidance, irrespective of male mimicry. We tested predictions of the male mimicry hypothesis, learned mate recognition hypothesis (LMR) and two new hypotheses. We used censuses and a mark-resight study to estimate density, sex ratio, morph frequency and mating frequencies. We observed interactions to test for male mimicry and female competition and to evaluate the frequency of mating attempts. Andromorphs were less likely than gynomorphs to receive mating attempts in encounters with males, but did not mate less frequently, or attack males or interrupt oviposition by other females more frequently. Contrary to the LMR hypothesis, the rarer morph was more likely to receive mating attempts. Andromorph frequency was greater in older females than in younger females, suggesting higher mortality or dispersal of gynomorphs. Our results support a modification of the male mimicry hypothesis, the signal detection hypothesis. Together with past studies, our results suggest that the female morphs may be alternative mating avoidance strategies.     

Testing the role of coadapted genes versus bet-hedging for mating strategies in colour polymorphic pygmy grasshoppers

Recent investigations of mate choice indicate that the genetic effect of sires on offspring fitness may depend on the interaction between maternal and paternal genotypes and the environmental conditions experienced by the offspring. Alternative colour morphs of the pygmy grasshopper, Tetrix subulata , represent ecological strategies that differ in body size, life history, thermoregulatory behaviour, and habitat selection. The hypothesis that selection promotes behaviours maintaining coadapted gene complexes predicts individuals to mate assortatively with respect to colour morph. On the other hand, the bet-hedging hypothesis predicts that the temporal variability of the environment inhabited by these animals may select for disassortative mating behaviour resulting in heterogeneous offspring. To distinguish between these competing hypotheses, we investigated mating behaviours using dual-choice experiments. Our results were not in agreement with the prediction of assortative mating but suggest instead that matings were random with regard to colour morph. Polyandry was common, and females mated with the second male regardless of whether the first mating was assortative or disassortative. Polyandry also was equally frequent among females in triads in which the two males belonged to different colour morphs as in triads where both males belonged to the same colour morph. A field experiment confirmed that polyandry occurred also among free-ranging individuals, and uncovered variation in mating success among male colour morphs, probably due to indirect effects of coloration on activity or habitat use. The consequences of this random and polyandrous mating strategy for the evolutionary dynamics of the colour polymorphism remain to be explored.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 491–499.     

Sexual selection as a promoter of population divergence in male phenotypic characters: a study on mainland and islet lizard populations

Sexual selection is often viewed as a promoter of population divergence, although some forms of sexual selection could rather hamper divergence. In the present study, we investigated whether sexual selection promotes divergence in sexually‐selected traits. We studied population variation in sexual selection in relation to colour morph and body size in islet and mainland populations of the Skyros wall lizard (Podarcis gaigeae). Females were most likely to mate with orange‐throated males with small body sizes, and male body size and coloration were therefore subject to correlational sexual selection. By contrast, male mating probabilities were not affected by any female phenotypic character. We also found variation in a female resistance trait (escape propensity), with females being more prone to escape when exposed to males from other habitats. Sexual selection could potentially affect the frequencies of throat colour morphs in this species by favouring orange‐throated males of small body size, although there was no evidence of sexual selection for local mates or rare phenotypes. The results obtained in the present study thus do not support a role for sexual selection as a promoter of population divergence in this species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 374–389.     

Show your true colour: cues for male mate preference in an intra‐specific mimicry system

1. Polymorphism limited to the female sex occurs in a variety of animal species and has been shown to be an attractive model system for examining general questions in signal detection theory. 2. When observed in damselflies, typically one female morph is an example of sexual dimorphism, whereas the other is considered as a functional malemimic that resembles the male's phenotype in several traits. 3. While several studies focused on male harassment and subsequent cost/benefit trade‐offs in female morphs, it remains understudied at the proximate level, which precise cues are relevant to mate‐searching males for discriminating among potential mates. 4. In the present study, we scored male mate preference to natural and manipulated phenotypes in the polymorphic damselfly Nehalennia irene Hagen. 5. In contrast to expectation, male preference did not change when colour was manipulated and male preference remained consistently for andromorph > male > gynomorph across treatments. 6. This suggests that cues other than body coloration primarily affect male mate preference in the present study system.     

Use of stable isotopes to assess the intraspecific foraging niche of males and female colour morphs of the damselfly Enallagma hageni

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Male‐mimicking females increase male‐male interactions,and decrease male survival and condition in a female‐polymorphic damselfly

Biologists are still discovering diverse and powerful ways sexual conflicts shape biodiversity. The present study examines how the proportion of females in a population that exhibit male mimicry, a mating resistance trait, influences conspecific males’ behavior, condition, and survival. Like most female‐polymorphic damselflies, Ischnura ramburii harbors both “andromorph” females, which closely resemble males, and sexually dimorphic “gynomorph” counterparts. There is evidence that male mimicry helps andromorphs evade detection and harassment, but males can also learn to target locally prevalent morph(s) via prior mate encounters. I hypothesized that the presence of male mimics could therefore predispose males to mate recognition errors, and thereby increase rates of costly male‐male interactions. Consistent with this hypothesis, male‐male interaction rates were highest in mesocosms containing more andromorph (vs. gynomorph) females. Males in andromorph‐biased mesocosms also had lower final body mass and higher mortality than males assigned to gynomorph‐majority treatments. Male survival and body mass were each negatively affected by mesocosm density, and mortality data revealed a marginally significant interaction between andromorph frequency and population density. These findings suggest that, under sufficiently crowded conditions, female mating resistance traits such as male mimicry could have pronounced indirect effects on male behavior, condition, and survival.     

Ontogenetic colour change signals sexual maturity in a non-territorial damselfly

Conspicuous colouration increases male reproductive success through female preferences and/or male–male competition. Despite the advantages of conspicuous colouration, inconspicuous male morphs can exist simultaneously in a population due to genetic diversity, condition dependence or developmental constraints. We are interested in explaining the male dichromatism in Xanthagrion erythroneurum damselflies. We reared these damselflies in outdoor insectaries under natural conditions and showed that this species undergoes ontogenetic colour changes. The younger males are yellow and change colour to red 6–7 days after their emergence. We took red and yellow male reflectance spectra and found that red males are brighter than yellow males. Next, we aimed to determine whether ontogenetic colour change signals sexual maturity with field observations and laboratory experiments. Our field observational data showed that red males are in higher abundance in the breeding territory, and they have a higher mating frequency than yellow males. We confirmed these field observations by enclosing a red and a yellow male with two females and found that yellow males do not mate in presence of red males. To determine whether colour change signals sexual maturity, we measured mating success of males before and after colour changes by enclosing a single male at different age (day 3-day 7) and colour (yellow, intermediate and red) with a single female in a mating cage. Males did not mate when yellow but the same male mated after it changed colour to red, suggesting the ontogenetic colour change signals sexual maturity in this species. Our study shows that male dichromatism can be age-dependent and ontogenetic colour change can signal age and sexual readiness in non-territorial insects.     

Reversible frequency-dependent switches in male mate choice

Current sexual-selection theories predict that mating should occur preferentially with the highest-quality partner, and assume that for distinguishing among potential mates the choosy sex applies an internal representation of the characteristics of the desired mate, i.e. a template. Binary choice experiments were performed to test male mate choice between two different female colour morphs in the damselfly Ischnura elegans. Choice experiments were conducted before and after an habituation period, during which males were exposed to only one female colour morph. Given the choice between the two female morphs, males did exhibit a choice for the most recently experienced female morph. This is the first evidence for a reversible switch in mate choice in a frequency-dependent way. In contrast with previous studies on mate choice, template formation in male I. elegans seems not to be based on quality. Switching mate choice in a frequency-dependent manner, choosing the most common morph, probably allows males to minimize their search efforts and to maximize fitness.     

Sexual selection and non-random mating for shell colour in a natural population of the marine snailLittorina mariae (Gastropoda: Prosobranchia)

In order to estimate the three independent components of mating behaviour, sexual selection in females, sexual selection in males and mating pattern, we studied the distribution of shell colour morphs among mating pairs and between copulating and non-copulating snails in four subsamples of a natural population ofL. mariae. The colour of the shell, the sex and a qualitative estimate of age was recorded for every snail. We found sexual selection acting against one of the two commonest colours (yellow) among the young females. However, in males none of the eight shell colour morphs was favoured during matings. Male sexual choice or differences in female sexual activity may cause the sexual fitness disadvantage of yellow females. Moreover, individuals of different colour morphs did not mate at random, rather dissasortatively. A behavioural choice among shell colour morphs or a non-random microdistribution of the morphs may cause the departure from random mating in this population.