Female-limited Polymorphism Research Articles

Evolution in Islands: contrasting morph frequencies in damselfly populations of the Balearic Islands

Abstract Colour polymorphism is an example of visible phenotypic variability that is often associated with ecological factors and may produce local adaptations. Small populations, particularly in islands, offer opportunities for evolutionary novelties, and are therefore of particular interest to the study of polymorphisms. Here we study the dynamics of female colour morphs in the damselfly Ischnura elegans in the Balearic Islands. We found that insular populations are small, show low density, low mating activity, and low androchrome frequency. Our surveys suggest that male harassment is a powerful force in the dynamics of this female-limited polymorphism, because high male densities result in lower presence of mature females around the water, where copulation takes place. Non-male-like (infuscans) females have higher mating frequency. Androchromes were rare (15%) in all populations, but the frequency of the two non-male like females (infuscans and aurantiaca) was reversed between islands, despite their geographical proximity. We found a possible novel morph, suggesting that insular conditions allow innovations. Fitness differences between the two non-male-like females of I. elegans are still understudied, because most previous research has concentrated on the maintenance of androchromes, and are therefore a priority for future research.

The genomics and evolution of inter-sexual mimicry and female-limited polymorphisms in damselflies

Sex-limited morphs can provide profound insights into the evolution and genomic architecture of complex phenotypes. Inter-sexual mimicry is one particular type of sex-limited polymorphism in which a novel morph resembles the opposite sex. While inter-sexual mimics are known in both sexes and a diverse range of animals, their evolutionary origin is poorly understood. Here, we investigated the genomic basis of female-limited morphs and male mimicry in the common bluetail damselfly. Differential gene expression between morphs has been documented in damselflies, but no causal locus has been previously identified. We found that male mimicry originated in an ancestrally sexually dimorphic lineage in association with multiple structural changes, probably driven by transposable element activity. These changes resulted in ~900 kb of novel genomic content that is partly shared by male mimics in a close relative, indicating that male mimicry is a trans-species polymorphism. More recently, a third morph originated following the translocation of part of the male-mimicry sequence into a genomic position ~3.5 mb apart. We provide evidence of balancing selection maintaining male mimicry, in line with previous field population studies. Our results underscore how structural variants affecting a handful of potentially regulatory genes and morph-specific genes can give rise to novel and complex phenotypic polymorphisms.

Intersexual social dominance mimicry drives female hummingbird polymorphism.

Female-limited polymorphisms, where females have multiple forms but males have only one, have been described in a variety of animals, yet are difficult to explain because selection typically is expected to decrease rather than maintain diversity. In the white-necked jacobin (Florisuga mellivora), all males and approximately 20% of females express an ornamented plumage type (androchromic), while other females are non-ornamented (heterochromic). Androchrome females benefit from reduced social harassment, but it remains unclear why both morphs persist. Female morphs may represent balanced alternative behavioural strategies, but an alternative hypothesis is that androchrome females are mimicking males. Here, we test a critical prediction of these hypotheses by measuring morphological, physiological and behavioural traits that relate to resource-holding potential (RHP), or competitive ability. In all these traits, we find little difference between female types, but higher RHP in males. These results, together with previous findings in this species, indicate that androchrome females increase access to food resources through mimicry of more aggressive males. Importantly, the mimicry hypothesis provides a clear theoretical pathway for polymorphism maintenance through frequency-dependent selection. Social dominance mimicry, long suspected to operate between species, can therefore also operate within species, leading to polymorphism and perhaps similarities between sexes more generally.

A single locus regulates a female-limited color pattern polymorphism in a reptile.

Animal coloration is often expressed in periodic patterns that can arise from differential cell migration, yet how these processes are regulated remains elusive. We show that a female-limited polymorphism in dorsal patterning (diamond/chevron) in the brown anole is controlled by a single Mendelian locus. This locus contains the gene CCDC170 that is adjacent to, and coexpressed with, the Estrogen receptor-1 gene, explaining why the polymorphism is female limited. CCDC170 is an organizer of the Golgi-microtubule network underlying a cell's ability to migrate, and the two segregating alleles encode structurally different proteins. Our agent-based modeling of skin development demonstrates that, in principle, a change in cell migratory behaviors is sufficient to switch between the two morphs. These results suggest that CCDC170 might have been co-opted as a switch between color patterning morphs, likely by modulating cell migratory behaviors.

Male-like ornamentation in female hummingbirds results from social harassment rather than sexual selection

Ornamentation is typically observed in sexually mature adults, is often dimorphic in expression, and is most apparent during breeding, supporting a role for sexual selection in its evolution.1-4 Yet, increasing evidence suggests that nonsexual social selection may also have a role in the evolution of ornamentation, especially in females.5-9 Distinguishing between these alternatives remains challenging because sexual and nonsexual factors may both play important and overlapping roles in trait evolution.7,10 Here, we show that female ornamentation in a dichromatic hummingbird, the white-necked jacobin (Florisuga mellivora), cannot be explained by sexual selection. Although all males are ornamented, nearly 30% of females have male-like plumage. Remarkably, all juveniles of both sexes express ornamented plumage similar to adult males (androchromatism), but 80% of females acquire non-ornamented plumage (heterochromatism) as they age. This unique ontogeny excludes competition for mates as an explanation for female ornamentation because non-reproductive juveniles are more likely to be ornamented than adults. Instead, avoidance of social harassment appears to underlie this female-limited polymorphism, as heterochrome taxidermy mounts received more aggressive and sexual attention than androchrome mounts from this and other hummingbird species. Monitoring electronically tagged birds at data-logging feeders showed that androchrome females accessed feeders more than heterochrome females, presumably because of reduced harassment. Our findings demonstrate that ornamentation can arise purely through nonsexual social selection, and this hypothesis must be considered in the evolution of not only female-limited polymorphism but also the spectacular ornamentation often assumed to result from sexual selection.

Male-like female morphs in hummingbirds: the evolution of a widespread sex-limited plumage polymorphism.

Differences in the way males and females look or behave are common in animals. However, discrete variation within sexes (sex-limited polymorphism) also occurs in several vertebrate and invertebrate lineages. In birds, female-limited polymorphism (FLP) in which some females resemble males in coloration is most prominent in hummingbirds, a group known for its morphological and behavioural sexual dimorphism. Yet, it remains unclear whether this intrasexual colour variation in hummingbirds arises through direct selection on females, or indirectly as a non-adaptive byproduct resulting from selection on males. Here, we analysed specimens from more than 300 hummingbird species to determine the extent, evolutionary history and function of FLP. We found that FLP evolved independently in every major clade and occurs in nearly 25% of hummingbird species. Using phylogenetically informed analyses, we rejected non-adaptive hypotheses that FLP is the result of indirect selection or pleiotropy across species. Instead, FLP is associated with ecology, migratory status, and marginally with social dominance, suggesting a socioecological benefit to females. Ultimately, we show that FLP is not only widespread in hummingbirds and likely adaptive, but may also be useful for understanding the evolution of female ornamentation in systems under strong sexual selection.

Mimicry genes reduce pre-adult survival rate in Papilio polytes: A possible new mechanism for maintaining female-limited polymorphism in Batesian mimicry.

Batesian mimicry, in which harmless organisms resemble unpalatable or harmful species, is a well-studied adaptation for predation avoidance. The females of some Batesian mimic species comprise mimetic and nonmimetic individuals. Mimetic females of such polymorphic species clearly have a selective advantage due to decreased predation pressure, but the selective forces that maintain nonmimetic females in a population remain unclear. In the swallowtail butterfly, Papilio polytes, female polymorphism is controlled by the H (mimetic) and h (nonmimetic) alleles at a single autosomal locus. Here, we examined whether the dominant H allele has a deleterious effect on the pre-adult survival rate (egg-to-adult emergence rate). We repeated an assortative mating-like treatment-that is breeding of males and females whose mothers had the same phenotype (mimetic or nonmimetic)-for three consecutive generations, while avoiding inbreeding. Results showed that pre-adult survival rate decreased over generations only in lines derived from mothers with the mimetic phenotype (hereafter, mimetic-assorted lines). This lowered survival was due to an increased mortality at the final instar larval stage and the pupal stages. Interestingly, the pre-adult mortality in the mimetic-assorted lines seemed to be associated with a male-biased sex ratio at adult emergence. These results suggest that the dominant H allele displays a mildly deleterious effect that is expressed more strongly in females and homozygous individuals than in heterozygous individuals. We propose that this cost of mimicry in larval and pupal stages contributes to the maintenance of female-limited polymorphism in P.polytes.

New records of polymorphism in Asian libellulid dragonflies (Insecta: Odonata)

Polymorphism has rarely been reported from dragonflies of the Libellulidae (Odonata: Anisoptera) family. Here, we report female-limited polymorphism in females of five species of the Libellulidae a...

Common cuckoo females may escape male sexual harassment by color polymorphism

Sexual conflict over mating rate is widely regarded as a selective force on the evolution of female-limited color polymorphism in invertebrates, such as damselflies and butterflies. However, evidence confirming its use in higher vertebrates remains limited. The common cuckoo, Cuculus canorus, is an avian brood parasite that does not provide parental care and represents a rare example of female-limited polymorphism in higher vertebrates. Specifically, males exhibit a monomorphic gray morph, while females are either gray or rufous colored, like juveniles. To test a prediction from the hypothesis that the rufous plumage of female cuckoos may help avoid excessive sexual harassment by males (the harassment avoidance hypothesis), we investigate color morph preference in male cuckoos. Mate choice experiments using playbacks of female calls with decoys mimicking both color morphs indicated that the attracted males immediately copulated with decoys without courtship displays, recognizing both color morphs as a sexual partner. However, the males attempted to copulate more frequently and excessively with the gray morph, which is consistent with the prediction from the harassment avoidance hypothesis. We propose that the absence of parental care augments sexual conflict over mating in cuckoos, resulting in the unusual evolution of female-limited polymorphism in this higher vertebrate.

Candidate genes associated with color morphs of female-limited polymorphisms of the damselfly Ischnura senegalensis.

Many Odonata species exhibit female-limited polymorphisms, where one morph is similar to the conspecific male in body color and other traits (andromorph), whereas one or more other morphs differ from the male (gynomorphs). Here we investigated the differentially expressed transcripts (DETs) among males and two female morph groups (gynomorphs and andromorphs) using RNA-seq to identify candidate transcripts encoding female-limited polymorphisms in the damselfly Ischnura senegalensis. Seven DETs that had significantly different expression levels between males and gynomorphs, but not between males and andromorphs, were identified. The expression levels of four of these candidate genes, doublesex (dsx), black, ebony, and chaoptin (chp), were selected for further analysis using qRT-PCR. Sequence analysis of the dsx amplicons revealed that this gene produced at least three transcripts. Two short transcripts were mainly expressed in males and andromorphs, whereas the long transcript was specifically expressed in both morph female groups; that is, the expression pattern of the dsx splice variants in andromorphs was an intermediate between that of males and gynomorphs. Because the dsx gene functions as a transcription factor that regulates the sex-specific expression of multiple genes, its splice variants in I. senegalensis may explain why the andromorph is female but exhibits some masculinized traits. Because we did not detect different coding sequences of the candidate genes among the different morphs, a diallelic genomic region controlling alternative splicing of dsx, thus determining female-limited polymorphism in I. senegalensis most likely lies in a non-coding region of the dsx gene or in a gene upstream of it.

Parallel evolution of Batesian mimicry supergene in two Papilio butterflies, P. polytes and P. memnon.

Batesian mimicry protects animals from predators when mimics resemble distasteful models. The female-limited Batesian mimicry in Papilio butterflies is controlled by a supergene locus switching mimetic and nonmimetic forms. In Papilio polytes, recent studies revealed that a highly diversified region (HDR) containing doublesex (dsx-HDR) constitutes the supergene with dimorphic alleles and is likely maintained by a chromosomal inversion. In the closely related Papilio memnon, which exhibits a similar mimicry polymorphism, we performed whole-genome sequence analyses in 11 butterflies, which revealed a nearly identical dsx-HDR containing three genes (dsx, Nach-like, and UXT) with dimorphic sequences strictly associated with the mimetic/nonmimetic phenotypes. In addition, expression of these genes, except that of Nach-like in female hind wings, showed differences correlated with phenotype. The dimorphic dsx-HDR in P. memnon is maintained without a chromosomal inversion, suggesting that a separate mechanism causes and maintains allelic divergence in these genes. More abundant accumulation of transposable elements and repetitive sequences in the dsx-HDR than in other genomic regions may contribute to the suppression of chromosomal recombination. Gene trees for Dsx, Nach-like, and UXT indicated that mimetic alleles evolved independently in the two Papilio species. These results suggest that the genomic region involving the above three genes has repeatedly diverged so that two allelic sequences of this region function as developmental switches for mimicry polymorphism in the two Papilio species. The supergene structures revealed here suggest that independent evolutionary processes with different genetic mechanisms have led to parallel evolution of similar female-limited polymorphisms underlying Batesian mimicry in Papilio butterflies.

Does male preference play a role in maintaining female limited polymorphism in a Batesian mimetic butterfly?

Female-limited polymorphism occurs in multiple butterfly species with Batesian mimicry. While frequency-dependent selection is often argued as the driving force behind polymorphism in Batesian mimicry systems, male preference and alternative female mating strategies may also influence the maintenance of multiple female forms. Through a series of behavioural assays with the female-limited Batesian mimetic butterfly Papilio polytes, we show that males prefer stationary mimetic females over stationary non-mimetic females, but weigh female activity levels more heavily than female wing pattern when choosing between active mimetic and active non-mimetic females. Male preference for mimetic vs. non-mimetic females is independent of male genotype at the locus responsible for the female wing pattern, the autosomal gene doublesex. However male genotype does influence their response to active females. Male emphasis on female behaviour instead of appearance may reduce sexual selection pressures on female morphology, thereby facilitating frequency-dependent natural selection due to predation risk and toxic model abundance.

Tracing the origin and evolution of supergene mimicry in butterflies

Supergene mimicry is a striking phenomenon but we know little about the evolution of this trait in any species. Here, by studying genomes of butterflies from a recent radiation in which supergene mimicry has been isolated to the gene doublesex, we show that sexually dimorphic mimicry and female-limited polymorphism are evolutionarily related as a result of ancient balancing selection combined with independent origins of similar morphs in different lineages and secondary loss of polymorphism in other lineages. Evolutionary loss of polymorphism appears to have resulted from an interaction between natural selection and genetic drift. Furthermore, molecular evolution of the supergene is dominated not by adaptive protein evolution or balancing selection, but by extensive hitchhiking of linked variants on the mimetic dsx haplotype that occurred at the origin of mimicry. Our results suggest that chance events have played important and possibly opposing roles throughout the history of this classic example of adaptation.

Independent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas).

Several species of swallowtail butterflies (genus Papilio) are Batesian mimics that express multiple mimetic female forms, while the males are monomorphic and nonmimetic. The evolution of such sex-limited mimicry may involve sexual dimorphism arising first and mimicry subsequently. Such a stepwise scenario through a nonmimetic, sexually dimorphic stage has been proposed for two closely related sexually dimorphic species: Papilio phorcas, a nonmimetic species with two female forms, and Papilio dardanus, a female-limited polymorphic mimetic species. Their close relationship indicates that female-limited polymorphism could be a shared derived character of the two species. Here, we present a phylogenomic analysis of the dardanus group using 3964 nuclear loci and whole mitochondrial genomes, showing that they are not sister species and thus that the sexually dimorphic state has arisen independently in the two species. Nonhomology of the female polymorphism in both species is supported by population genetic analysis of engrailed, the presumed mimicry switch locus in P.dardanus. McDonald-Kreitman tests performed on SNPs in engrailed showed the signature of balancing selection in a polymorphic population of P.dardanus, but not in monomorphic populations, nor in the nonmimetic P.phorcas. Hence, the wing polymorphism does not balance polymorphisms in engrailed in P.phorcas. Equally, unlike in P.dardanus, none of the SNPs in P.phorcas engrailed were associated with either female morph. We conclude that sexual dimorphism due to female polymorphism evolved independently in both species from monomorphic, nonmimetic states. While sexual selection may drive male-female dimorphism in nonmimetic species, in mimetic Papilios, natural selection for protection from predators in females is an alternative route to sexual dimorphism.

Role of visual and non-visual cues in damselfly mate recognition

In many species of damselflies, sexual conflict in the form of male harassment is thought to explain the widespread existence of female-limited color polymorphisms. With a few exceptions, the majority of investigations into these mating systems have assumed that male damselflies primarily use visual cues to detect and recognize their mates. Recently, laboratory studies have demonstrated that damselflies orient to olfactory signals from prey and that males orient to chemical cues from conspecific females. However, to date there are no field experiments which explicitly test the role that chemical cues play in sex recognition. Here we used a field experiment on Enallagma civile damselflies to test if free flying males detect and recognize females in the absence of visual cues through the use of non-visual signals. In the absence of visual cues males did not exhibit positive responses toward female conspecifics, whereas when both visual and non-visual cues were present, males readily detected females and oft...

A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly.

In Batesian mimicry, animals avoid predation by resembling distasteful models. In the swallowtail butterfly Papilio polytes, only mimetic-form females resemble the unpalatable butterfly Pachliopta aristolochiae. A recent report showed that a single gene, doublesex (dsx), controls this mimicry; however, the detailed molecular mechanisms remain unclear. Here we determined two whole-genome sequences of P. polytes and a related species, Papilio xuthus, identifying a single ∼130-kb autosomal inversion, including dsx, between mimetic (H-type) and non-mimetic (h-type) chromosomes in P. polytes. This inversion is associated with the mimicry-related locus H, as identified by linkage mapping. Knockdown experiments demonstrated that female-specific dsx isoforms expressed from the inverted H allele (dsx(H)) induce mimetic coloration patterns and simultaneously repress non-mimetic patterns. In contrast, dsx(h) does not alter mimetic patterns. We propose that dsx(H) switches the coloration of predetermined wing patterns and that female-limited polymorphism is tightly maintained by chromosomal inversion.

A preliminary study on female-limited colour polymorphism inLestes sponsa

Female-limited colour polymorphisms are widespread in Odonata, usually showing an androchrome and one or more gynochromes. Androchromes have been hypothesized to function as male mimics with a cons ...

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.

Color Change from male-mimic to Gynomorphic: a New Aspect of Signaling Sexual Status in Damselflies (Odonata, Zygoptera)

Body color variations are used by many animal species to communicate their sexual state and are believed to have evolved through sexual selection. In damselfly species (Odonata, Zygoptera), females sometimes come in different color morphs: gynomorphs and male-like andromorphs, pursuing different reproductive strategies. These distinct female color morphs are usually mature females and their color remains stable throughout the female's life. Here, we show for the first time that blue andromorph females of the Australian damselfly Ischnura heterosticta, are still sexually immature, and change their body color to green-grey gynomorph when they are ready to mate. The color change occurs within 24h and is irreversible. Males of I. heterosticta rarely recognize blue andromorphs as potential mates, but mistake them for other males. The andromorphs thus avoid male sexual harassment, giving them the advantage of additional time to forage and sexually mature. The color change to gynomorph signals the readiness to mate, and the former andromorphs have equal mating success after the color change as other gynomorph females. Our results demonstrate that andromorph I. heterosticta use a complete and unique body color change from male-mimic to gynomorphic to signal sexual maturity and regulate reproduction. Our discovery gives rise to a novel hypothesis regarding maintenance of female-limited polymorphism in Ischnura damselflies via this color change mechanism.

Female-limited polymorphism and its significance in Appias (Catophaga) nero corazonae Schröder and Treadaway, 1989 (Lepidoptera: Pieridae)

Diagnostic characters are presented for Appias nero corazonae, a pierid butterfly from the Sulu Archipelago, Philippines, that exhibits female-limited polymorphism. The potential significance of A. n. corazonae for genetic investigations into Darwinian transference, the hypothetical process whereby bright colouration first evolves in the males of a species and is later ‘transferred’ to the females, is discussed.