Female Colour Morphs Research Articles

Reproductive timing and patterns of development for the damselfly Coenagrion puella in the field

By a combination of detailed behavioral observations and molecular genetic approaches we have assessed development time, timing of first maturity, and the extent of genetic structure through the flying season in a wild population of the damselfly Coenagrion puella in England. This work provides the first estimate of development time (egg to mature adult) in the field based on individual damselflies. Development time was significantly longer for females than males. In contrast to reported laboratory studies, there was no difference in development times between different female color morphs. Development time ranged between 347 and 396 days and was negatively correlated with egg-laying date. As a result eggs laid early in one season reach adult maturity relatively late in the next; concurrently individuals developing from eggs laid late mature relatively early. We speculate that this pattern of development is a direct physiological response to seasonal environmental variation and results in reproductive synchrony within a population. Size, specifically hind wing length, declined with development time in males, but not in females. In one of the two years of the study there was evidence for weak clustering of related individuals during the reproductive season. This appeared to be the result of developmental synchronization within families: variance in timing of maturation was smaller in full-sib families than in half-sib families or randomly assigned unrelated groups.

Colour variation is incongruent with mitochondrial lineages: cryptic speciation and subsequent diversification in a Gulf of California reef fish (Teleostei: Blennioidei)

The Gulf of California endemic reef fish, Acanthemblemaria crockeri (Blennioidei, Chaenopsidae), reportedly has two colour morphs, one with melanic lateral spots ('Gulf' morph) and one with orange spots ('Cape' morph). In this study, we recorded colour morph in both males and females and collected mitochondrial DNA sequence data for cytochrome c oxidase I (COI) and tRNA-Pro/D-loop of specimens from throughout the Gulf to explore the genetic basis of the colour morphs. Two highly divergent (HKY + I distance = 11.9% for COI), reciprocally monophyletic lineages were identified, consistent with the presence of two parapatric species. A 30-km gap between the distributions of mitochondrial lineages roughly corresponds to a hypothesized former seaway across the Baja California peninsula north of La Paz, although the estimated divergence time (1.84 million years ago) is more recent than the hypothetical seaway (3-4 million years ago). Surprisingly, the distribution of mitochondrial species is not congruent with the distribution of either male or female colour morphs. Our analysis also revealed significant population differentiation within both species and no shared haplotypes among populations. The northern Gulf species includes four populations (NB, CB, NM and CM) corresponding to northern and central Baja and northern and central mainland sites, while the Cape species includes two populations (SB and SM) corresponding to the Baja and mainland sides of the southern Gulf. The NB/CB division corresponds to a hypothesized Plio-Pleistocene mid-peninsular seaway. The level of genetic divergence documented in this lineage is extraordinary for a marine fish with a pelagic larval stage within a semi-enclosed basin.

MAPPING INDIVIDUAL VARIATION IN MALE MATING PREFERENCE SPACE: MULTIPLE CHOICE IN A COLOR POLYMORPHIC CICHLID FISH

Sexual selection theory largely rests on the assumption that populations contain individual variation in mating preferences and that individuals are consistent in their preferences. However, there are few empirical studies of within-population variation and even fewer have examined individual male mating preferences. Here, we studied a color polymorphic population of the Lake Victoria cichlid fish Neochromis omnicaeruleus, a species in which color morphs are associated with different sex-determining factors. Wild-caught males were tested in three-way choice trials with multiple combinations of different females belonging to the three color morphs. Compositional log-ratio techniques were applied to analyze individual male mating preferences. Large individual variation in consistency, strength, and direction of male mating preferences for female color morphs was found and hierarchical clustering of the compositional data revealed the presence of four distinct preference groups corresponding to the three color morphs in addition to a no-preference class. Consistency of individual male mating preferences was higher in males with strongest preferences. We discuss the implications of these findings for our understanding of the mechanisms underlying polymorphism in mating preferences.

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.

Behavioral dominance between female color morphs of a Lake Victoria cichlid fish

Species that exhibit genetic color polymorphism are suitable for studying the evolutionary forces that maintain heritable phenotypic variation in nature. Male color morphs often differ in behavioral dominance, affecting the evolution of color polymorphisms. However, behavioral dominance among female color morphs has received far less attention. We studied a polymorphic population of the cichlid fish Neochromis omnicaeruleus from Lake Victoria, in which 3 distinct female color morphs coexist, black-and-white blotched (WB), orange blotched (OB), and plain (P) color morphs. First, we investigated dominance relationships among female morphs using triadic and dyadic encounters in the laboratory. In triadic encounters, both WB and OB females dominated plain, whereas WB females dominated OB females. Dominance of WB over OB was confirmed using dyadic encounters. In a second experiment, blotched (WB or OB) and plain full-sib sisters were bred by crossing a blotched and a plain parent. In dyadic encounters, WB female morphs dominated their plain sisters, suggesting that dominance of WB females is a pleiotropic effect of color or that genes coding for color and those influencing behavioral dominance are genetically linked, explaining the association between color and behavioral dominance despite gene flow. We conclude that behavioral dominance asymmetries exist among female color morphs of the fish N. omnicaeruleus, and discuss possible mechanisms that may account for the tight association between color and behavioral dominance.

Effects of phenotypic variation onto body temperature and flight activity in a polymorphic insect

Abstract According to biophysical principles, colour and size are important phenotypic factors that may influence body temperature and activity in ectothermic insects. In taxa showing female‐limited polymorphism, males and female morphs differ in body colour, size and activity pattern. However, no previous study has evaluated whether such phenotypic and behavioural variation relates to differences between males and female morphs in thermal properties. In the present study, the relationships between body colour, size, activity and body temperature are examined under laboratory and field conditions, for the polymorphic damselfly Enallagma cyathigerum (Charpentier, 1840) (Odonata: Zygoptera). Contrary to expectation, males and female colour morphs of this species do not differ in thermal properties (i.e. heating characteristics or field body temperatures). When questioning phenotype and activity, temperature does not appear to be relevant for understanding the maintenance of female‐limited polymorphism.

SPATIAL AND TEMPORAL DYNAMICS IN A SEXUAL SELECTION MOSAIC

Selective regimes and phenotypic optima could either change smoothly and in a clinal fashion or be spatially organized in a more unpredictable mosaic pattern over the geographic landscape. When natural or sexual selection is driven by intra- or interspecific biotic interactions, fine-grained spatial variation in selective regimes could result in selection mosaics rather than clinal variation in selection. We investigated temporal variation and spatial organization in sexual selection on male body size along an ecological coastal-inland gradient of a polymorphic damselfly Ischnura elegans. Body size increased in a clinal fashion along this gradient: animals were smaller in size at the coast, but became larger in the inland areas. In contrast, the sexual selection regimes on male body size showed evidence of more fine-grained spatial organization with no evidence for a clinal pattern and low spatial autocorrelations between populations. These spatially fine-grained sexual selection regimes varied in sign and magnitude and were driven by a combination of the densities of heritable female color morphs and local female body sizes. We suggest that the spatial organization of the selective regimes can be interpreted as a sexual selection mosaic that is influenced by highly localized density- and frequency-dependent social interactions.

Individual variation in male mating preferences for female coloration in a polymorphic cichlid fish

Female color polymorphisms are common in the cichlid species radiations of Lake Victoria and Lake Malawi. According to theory, when a population harbors variation in sex-determining factors, polymorphism in female-linked coloration might generate individual variation in male mating preferences for female color morphs. We tested whether individual males exhibit consistent mating preferences for female color morphs in the Lake Malawi cichlid Pseudotropheus (Maylandia) ‘zebra gold’, a species polymorphic for female coloration and sex determination. We also explored whether male mating preferences could be predicted by maternal coloration or were acquired by imprinting on siblings’ coloration. We found large individual variation in the strength and direction of male preferences for sex-linked female color patterns. Male mating preferences could be predicted by the mother’s color morph and were not affected by visual imprinting. These findings represent the first evidence of male choice on sex-linked female coloration in a Lake Malawi cichlid. Our analysis indicates a strong genetic component to male preference for female coloration and large individual variation in the strength and direction of male mating preferences. Within-population variation in innate mating preferences might have important implications in cichlid fish species radiations.

Intrasexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish

The maintenance of colour polymorphisms within populations has been a long-standing interest in evolutionary ecology. African cichlid fish contain some of the most striking known cases of this phenomenon. Intrasexual selection can be negative frequency dependent when males bias aggression towards phenotypically similar rivals, stabilizing male colour polymorphisms. We propose that where females are territorial and competitive, aggression biases in females may also promote coexistence of female morphs. We studied a polymorphic population of the cichlid fish Neochromis omnicaeruleus from Lake Victoria, in which three distinct female colour morphs coexist: one plain brown and two blotched morphs. Using simulated intruder choice tests in the laboratory, we show that wild-caught females of each morph bias aggression towards females of their own morph, suggesting that females of all three morphs may have an advantage when their morph is locally the least abundant. This mechanism may contribute to the establishment and stabilization of colour polymorphisms. Next, by crossing the morphs, we generated sisters belonging to different colour morphs. We find no sign of aggression bias in these sisters, making pleiotropy unlikely to explain the association between colour and aggression bias in wild fish, which is maintained in the face of gene flow. We conclude that female-female aggression may be one important force for stabilizing colour polymorphism in cichlid fish.

Male-like females of a damselfly are not preferred by males even if they are the majority morph

Animals searching for prey and males searching for mates share similar problems of detection if their targets are diverse in colour or physical appearance. There is good evidence for predators switching their preferences for prey in a frequency-dependent way; predators focus on the most common form, and the decreased predation on rarer forms allows multiple forms to survive. Frequency-dependent mate selection has also been proposed to explain the maintenance of several female colour morphs in damselflies. However, the fact that one of the female morphs is coloured like a male (androchrome) and behaves similarly to males suggests the phenomenon of male mimicry in this system as an alternative explanation for the polymorphism. We compared androchrome frequencies in populations and mating pairs in Ischnura elegans, over a range of androchrome frequencies (8–90%). In 22 of 23 samples androchromes mated less often than expected (significantly in 13 samples). We found no evidence for males switching their preferences in a frequency-dependent way. A test of male preference for female morphs in a population with 85% androchromes indicated that males behaved indiscriminately and did not prefer the commonest (male-like) morph. Our results support androchrome male mimicry rather than learned mate recognition by males (a purely frequency-dependent model) as the main mechanism behind the maintenance of this sex-limited colour polymorphism.

Female Sexual Polymorphism and Fecundity Consequences of Male Mating Harassment in the Wild

Genetic and phenotypic variation in female response towards male mating attempts has been found in several laboratory studies, demonstrating sexually antagonistic co-evolution driven by mating costs on female fitness. Theoretical models suggest that the type and degree of genetic variation in female resistance could affect the evolutionary outcome of sexually antagonistic mating interactions, resulting in either rapid development of reproductive isolation and speciation or genetic clustering and female sexual polymorphisms. However, evidence for genetic variation of this kind in natural populations of non-model organisms is very limited. Likewise, we lack knowledge on female fecundity-consequences of matings and the degree of male mating harassment in natural settings. Here we present such data from natural populations of a colour polymorphic damselfly. Using a novel experimental technique of colour dusting males in the field, we show that heritable female colour morphs differ in their propensity to accept male mating attempts. These morphs also differ in their degree of resistance towards male mating attempts, the number of realized matings and in their fecundity-tolerance to matings and mating attempts. These results show that there may be genetic variation in both resistance and tolerance to male mating attempts (fitness consequences of matings) in natural populations, similar to the situation in plant-pathogen resistance systems. Male mating harassment could promote the maintenance of a sexual mating polymorphism in females, one of few empirical examples of sympatric genetic clusters maintained by sexual conflict.

Ontogeny of sexual dimorphism and phenotypic integration in heritable morphs

In this study we investigated the developmental basis of adult phenotypes in a non-model organism, a polymorphic damselfly (Ischnura elegans) with three female colour morphs. This polymorphic species presents an ideal opportunity to study intraspecific variation in growth trajectories, morphological variation in size and shape during the course of ontogeny, and to relate these juvenile differences to the phenotypic differences of the discrete adult phenotypes; the two sexes and the three female morphs. We raised larvae of different families in individual enclosures in the laboratory, and traced morphological changes during the course of ontogeny. We used principal components analysis to examine the effects of Sex, Maternal morph, and Own morph on body size and body shape. We also investigated the larval fitness consequences of variation in size and shape by relating these factors to emergence success. Females grew faster than males and were larger as adults, and there was sexual dimorphism in body shape in both larval and adult stages. There were also significant effects of both maternal morph and own morph on growth rate and body shape in the larval stage. There were significant differences in body shape, but not body size, between the adult female morphs, indicating phenotypic integration between colour, melanin patterning, and body shape. Individuals that emerged successfully grew faster and had different body shape in the larval stage, indicating internal (non-ecological) selection on larval morphology. Overall, morphological differences between individuals at the larval stage carried over to the adult stage. Thus, selection in the larval stage can potentially result in correlated responses in adult phenotypes and vice versa.

Colour polymorphism in femaleCoenagrion puella:differences in egg shape (Odonata: Coenagrionidae)

Abstract The maintenance of female colour polymorphism in coenagrionids is still an open issue. Here we ask if the three different female morphs of Coenagrion puella represent different reproductive traits in terms of clutch and egg size. Therefore clutch size and egg morphometry of the three female colour morphs were examined. We found that female colour morphs did not differ in clutch or egg size. However, we also found that the female morphs differ in egg shape, with the intermediate morph having more elongated eggs compared to the hetero- and and romorphic females. Our results are discussed in terms of potential different preferences in oviposition substrate.

Fiery red heads: female dominance among head color morphs in the Gouldian finch

Although the evolution of genetic color polymorphisms has received much theoretical interest, few empirical studies have investigated the adaptive function of alternative color morphs. Furthermore, most studies have focused almost exclusively on the evolution and adaptive expression of male coloration, leaving the role of conspicuous female coloration largely unknown. Using the color polymorphic Gouldian finch (Erythrura gouldiae), this study experimentally tests the status signaling function of head color (red, yellow, and black) among the 3 female color morphs. In standardized dominance contests between unfamiliar females of different head colors, red-headed females dominated both black- and yellow-headed females. During contests between the morphs, red-headed females passively displaced black- and yellow-headed opponents, whereas interactions between red-headed dyads were particularly aggressive and more frequent than interactions within dyads of the other color morphs. This effect of red dominance further persisted when head color was experimentally altered; red-manipulated females (of the other morphs) dominated both black- and yellow-headed females, whereas blackened red-headed females were dominated by naturally red-headed birds. Together with similar dominance-related differences among male morphs, these results suggest that the 3 color morphs may display alternative strategies in dominance behavior.

Host nest defense against a color-dimorphic brood parasite: great reed warblers (Acrocephalus arundinaceus) versus common cuckoos (Cuculus canorus)

We tested great reed warbler (Acrocephalus arundinaceus) discrimination against two common cuckoo (Cuculus canorus) female color morphs (gray and rufous) in two areas with different parasitism rates and proportions of the two morphs. Hosts recognized the two cuckoo morphs from a control, the feral pigeon (Columba livia), at Apaj, Hungary (where brood parasitism was heavy), whereas no significant differences among the models were recorded at Lužice, Czech Republic (where the parasitism rate was moderate). At Apaj, the hosts discriminated the rufous morph (which is slightly predominant there) better than the gray morph from the control. Between-site comparison (after controlling for background aggression) revealed that great reed warblers were more aggressive towards the rufous morph at Apaj than at Lužice, whereas their responses to the gray morph did not differ, corresponding with much higher between-site difference in the relative abundance of the rufous morph. Our results suggest that both local parasitism pressure and relative abundance of two female color morphs of a brood parasite may significantly influence host nest defenses.

Lifetime fitness components in female colour morphs of a damselfly: density- or frequency-dependent selection?

In many damselfly species mature females exhibit colour polymorphism: one female morph resembles the conspecific male (androchrome) while the others do not (gynochromes). Hypotheses for the maintenance of such polymorphisms differ mainly as to whether they are based on density- and/or frequency-dependent selection and on the nature of the frequency dependence. We collected lifetime fitness data (individual lifespan, number of copulations and number of ovipositions) for female morphs of the damselfly Ischnura elegans from 15 insectaries differing in population parameters (density, sex ratio and ratio of andro- to gynochromes). Both density and frequency affected a specific set of the studied fitness components. While morph frequency influenced lifespan, sex ratio influenced the number of copulations, and density affected lifespan and the number of ovipositions. Clearly, discrepancies among studies may be generated if the studied fitness components differ. Our final fitness estimate, the number of ovipositions, was only influenced by density, thereby not supporting frequency-based hypotheses. Contrary to expectation under the current density-based hypothesis, androchromes compared to gynochromes had a lower number of ovipositions at high density. We discuss our findings in the light of mechanisms maintaining the female polymorphism. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86, 515–523.

Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly

Although colour polymorphisms in adult organisms of many taxa are often adaptive in the context of sexual selection or predation, genetic correlations between colour and other phenotypic traits expressed early in ontogeny could also play an important role in polymorphic systems. We studied phenotypic and genetic variation in development time among female colour morphs in the polymorphic damselfly Ischnura elegans in the field and by raising larvae in a common laboratory environment. In the field, the three different female morphs emerged at different times. Among laboratory-raised families, we found evidence of a significant correlation between maternal morph and larval development time in both sexes. This suggests that the phenotypic correlation between morph and emergence time in the field has a parallel in a genetic correlation between maternal colour and offspring development time. Maternal colour morph frequencies could thus potentially change as correlated responses to selection on larval emergence dates. The similar genetic correlation in male offspring suggests that sex-limitation in this system is incomplete, which may lead to an ontogenetic sexual conflict between selection for early male emergence (protandry) and emergence times associated with maternal morph.

The evolution and frequency of female color morphs in Holarctic Odonata: why are male-like females typically the minority?

Abstract We compiled data on the occurrence and frequency of distinct female variants among Holarctic Odonata and interpreted the data in light of harassment-based hypotheses. The major source of male confusion for male mimicry hypotheses is predicted to be signal similarity between andromorphs and male distractors; for the learned mate recognition hypothesis (LMR), it is predicted to be variation in female signals. Mapping morphism state onto molecular phylogenies of Ischnura and Enallagma failed to resolve the general ancestral female condition. However, it appeared that the andromorphic state may be ancestral in one case, and that blue structural colors were ancestral to orange and green pigmentations. Of the polymorphic species surveyed, 13% had more than two morphs, 4% had multiple heteromorphs but no andromorph, and 7% of ‘monomorphic’ congeners were functionally polymorphic because developmental variants mate. Such female signal variation lies beyond the scope of simple male mimicry, but neverthele...

Reversible switches between male–male and male–female mating behaviour by male damselflies

For many animal groups, both sexes have been reported to attempt to mate with members of their own sex. Such behaviour challenges theories of sexual selection, which predict optimization of reproductive success. We tested male mate choice between opposite- and same-sex members in the damselfly Ischnura elegans. Binary choice experiments were conducted following exposure periods in insectaries with only males or with both sexes present. We show that switches in choice between the opposite sex and the same sex can be induced and reversed again by changing the social context. We argue that the observed reversibility in male-male- and male-female-directed mating behaviour is maladaptive and a consequence of strong selection on a male's ability to alter choice between different female colour morphs.

Sex- and morph-specific predation risk: Colour or behaviour dependency?

The coexistence of discrete morphs within a species, with one morph more conspicuous than the other(s) is often thought to result from both sexual selection and predation. In many damselflies, sexual dimorphism occurs jointly with multiple female colour morphs. Typically, one morph is coloured like the male (andromorph), while the other(s) is not (gynomorph(s)). The mecha- nisms contributing to the maintenance of such female polymorphism in damselflies remain poorly understood, especially the role of predation. We tested the detectability of two different female colour morphs of the damselfly, Enallagma cyathigerum, using human observers as model predators; andromorphs were detected more frequently than gynomorphs. Field data on mortality of males and the two different female morphs due to predation or drowning were also collected, and these observations support morph-specific mortality. In natural populations predation risk was higher in males than females; gynomorphs, however, were more prone to preda- tion than andromorphs. Differences in behaviour between morphs, rather than colour, may explain this result.