Female-limited Mimicry Research Articles

Evolutionary origins of sexual dimorphism: Lessons from female-limited mimicry in butterflies.

The striking female-limited mimicry observed in some butterfly species is a text-book example of sexually dimorphic trait submitted to intense natural selection. Two main evolutionary hypotheses, based on natural and sexual selection respectively, have been proposed. Predation pressure favoring mimicry toward defended species could be higher in females because of their slower flight, and thus overcome developmental constraints favoring the ancestral trait that limits the evolution of mimicry in males but not in females. Alternatively, the evolution of mimicry in males could be limited by female preference for non-mimetic males. However, the evolutionary origin of female preference for non-mimetic males remains unclear. Here, we hypothesize that costly sexual interactions between individuals from distinct sympatric species might intensify because of mimicry, therefore promoting female preference for non-mimetic trait. Using a mathematical model, we compare the evolution of female-limited mimicry when assuming either alternative selective hypotheses. We show that the patterns of divergence of male and female trait from the ancestral traits can differ between these selection regimes. We specifically highlight that divergence in female trait is not a signature of the effect of natural selection. Our results also evidence why female-limited mimicry is more frequently observed in Batesianmimics.

Dorsal Forewing White Spots of Male Papilio polytes(Lepidoptera: Papilionidae) not Maintained by Female Mate Choice

Palatable animals sometimes mimic the color patterns of noxious animals to gain protection from predators. This phenomenon, known as Batesian mimicry, is seen in many butterflies of the genus Papilio, and in some species the mimicry is limited to females. Although female-limited Batesian mimicry has been hypothesized to be caused by females preferring to mate with non-mimetic males, this hypothesis is rarely tested. In this study, we tested whether female mate choice is driving female-limited Batesian mimicry in Papilio polytes. Males have white spots on the dorsal forewings, which are absent in mimetic female sand in the toxic model, Pachliopta aristolochiae. Hence, we conducted mate choice experiments to examine whether these white spots are important to females. We offered females a choice of males with intact dorsal forewing white spots and males with artificially blackened dorsal forewings, resembling the model. Females did not show a preference for males with the white spots, suggesting that they are not being maintained by female mate choice. Future studies should investigate the presence of female mate choice on other parts of males’ wings to further understand the role of female mate choice, as well as explore other factors driving female-limited mimicry in these butterflies.

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.

Identification of doublesex alleles associated with the female-limited Batesian mimicry polymorphism in Papilio memnon

The female-limited Batesian mimicry polymorphism in Papilio butterflies is an intriguing system for investigating the mechanism of maintenance of genetic polymorphisms. In Papilio polytes, an autosomal region encompassing the sex-determinant gene doublesex controls female-limited mimicry polymorphism. In the closely related species P. memnon, which also exhibits female-limited Batesian mimicry polymorphism, we identified two allelic sequences of the doublesex gene that corresponded exactly with the mimetic and non-mimetic female phenotypes. Thus, the genetic basis of the mimicry polymorphism in P. memnon is similar to that in P. polytes. However, the mimetic and non-mimetic alleles of the two species were not identical, and the divergence of alleles occurred independently in P. memnon and P. polytes. Different mutation-selection processes may have resulted in the convergent patterns of mimicry polymorphism in these Papilio butterflies.

Prey from the eyes of predators: Color discriminability of aposematic and mimetic butterflies from an avian visual perspective.

Predation exerts strong selection on mimetic butterfly wing color patterns, which also serve other functions such as sexual selection. Therefore, specific selection pressures may affect the sexes and signal components differentially. We tested three predictions about the evolution of mimetic resemblance by comparing wing coloration of aposematic butterflies and their Batesian mimics: (a) females gain greater mimetic advantage than males and therefore are better mimics, (b) due to intersexual genetic correlations, sexually monomorphic mimics are better mimics than female-limited mimics, and (c) mimetic resemblance is better on the dorsal wing surface that is visible to predators in flight. Using a physiological model of avian color vision, we quantified mimetic resemblance from predators' perspective, which showed that female butterflies were better mimics than males. Mimetic resemblance in female-limited mimics was comparable to that in sexually monomorphic mimics, suggesting that intersexual genetic correlations did not constrain adaptive response to selection for female-limited mimicry. Mimetic resemblance on the ventral wing surface was better than that on the dorsal wing surface, implying stronger natural and sexual selection on ventral and dorsal surfaces, respectively. These results suggest that mimetic resemblance in butterfly mimicry rings has evolved under various selective pressures acting in a sex- and wing surface-specific manner.

THE DIVERSITY AND EVOLUTION OF BATESIAN MIMICRY INPAPILIOSWALLOWTAIL BUTTERFLIES

Papilio swallowtail butterflies exhibit a remarkable diversity of Batesian mimicry, manifested in several sex-limited and polymorphic types. There is little understanding of how this diversity is distributed within Papilio, and how different mimicry types have evolved in relation to each other. To answer these questions, I present a graphical model that connects various mimicry types by hypothetical character state changes within a phylogenetic framework. A maximum likelihood analysis of evolution of mimicry types on the Papilio phylogeny showed that sexually monomorphic mimicry and female-limited mimicry have evolved repeatedly but predominantly independently in different clades. However, transitions between these mimicry types are rarely observed. The frequency distribution of character state changes was skewed in favor of the evolution of mimicry, whereas many theoretically plausible character state changes, especially evolutionary loss of mimicry, were not evident. I discuss these findings in relation to studying the tempo of evolutionary change, loss of traits, and directionality and connectivity among character states. The pathway approach and phylogenetic patterns of mimicry demonstrated in Papilio are useful to test novel hypotheses regarding the diversity and evolutionary directionality of Batesian mimicry in other systems.

No association between mitochondrial DNA haplotypes and a female-limited mimicry phenotype in Papilio glaucus.

Alternative alleles at a locus on the W chromosome of Papilio glaucus (causing dark or yellow wing colors, respectively) underlie a female-limited mimicry polymorphism thought to be maintained by balancing selection. In species with heterogametic females (i.e., the ZZ-male/ZW-female sex chromosome system), the mitochondrial DNA and the W chromosome are genetically linked because they are both maternally transmitted. We investigate the association of COI and COII mitochondrial DNA haplotypes with alternative W-linked phenotypes. Surprisingly, we find no congruence between mitochondrial DNA genealogies and inferred W-linked color alleles in P. glaucus. Using a maximum-likelihood phylogenetic approach, we reject the hypothesis of monophyly for dark-morph mitochondrial DNA lineages, even in the presence of putative low-frequency mimicry suppressor alleles or alternative melanizing factors. The most likely genealogical tree topologies assume more than one exchange event between mitochondrial DNA cytotype and the W-linked color morph. These results suggest that there is either paternal leakage of mitochondrial DNA or that more than two W-linked alleles underlie the alternative color morphs. Using data from an additional mitochondrial DNA locus, ND5, we show that pairwise linkage disequilibrium decays with physical distance between polymorphic sites. This finding suggests that genetic exchanges between maternal and paternal mitochondrial DNAs may have contributed to the lack of association we observe between phenotype and genotype.

NO ASSOCIATION BETWEEN MITOCHONDRIAL DNA HAPLOTYPES AND A FEMALE-LIMITED MIMICRY PHENOTYPE IN PAPILIO GLAUCUS

Alternative alleles at a locus on the W chromosome of Papilio glaucus (causing dark or yellow wing colors, respectively) underlie a female-limited mimicry polymorphism thought to be maintained by balancing selection. In species with heterogametic females (i.e., the ZZ-male/ZW-female sex chromosome system), the mitochondrial DNA and the W chromosome are genetically linked because they are both maternally transmitted. We investigate the association of COI and COII mitochondrial DNA haplotypes with alternative W-linked phenotypes. Surprisingly, we find no congruence between mitochondrial DNA genealogies and inferred W-linked color alleles in P. glaucus. Using a maximum-likelihood phylogenetic approach, we reject the hypothesis of monophyly for dark-morph mitochondrial DNA lineages, even in the presence of putative low-frequency mimicry suppressor alleles or alternative melanizing factors. The most likely genealogical tree topologies assume more than one exchange event between mitochondrial DNA cytotype and the W-linked color morph. These results suggest that there is either paternal leakage of mitochondrial DNA or that more than two W-linked alleles underlie the alternative color morphs. Using data from an additional mitochondrial DNA locus, ND5, we show that pairwise linkage disequilibrium decays with physical distance between polymorphic sites. This finding suggests that genetic exchanges between maternal and paternal mitochondrial DNAs may have contributed to the lack of association we observe between phenotype and genotype.

Evolution of the mimetic African swallowtail butterfly Papilio dardanus: molecular data confirm relationships with P. phorcas and P. constantinus

Sister group relationships of the African Mocker Swallowtail, Papilio dardanus, were determined using mitochondrial 16S rRNA and Cytochrome B sequences, and nuclear Elongation Factor EF-la and the ITS-1 region of the ribosomal RNA locus. All four data sets placed P. dardanus as the sister species of P. phorcas, with P. constantinus as the next closest relative, and quite distinct from other African Papilios such as P. nobilis. These data support earlier morphological studies indicating that the only two African Papilio species with multiple female colour forms have a common ancestor not shared with any other living species. This information is important for conclusions about the evolution of female-limited mimicry in swallowtail butterflies, and successful use of the ITS-1 gene opens up new possibilities for studying this phenomenon within P. dardanus.

Evolution of the mimetic African swallowtail butterflyPapilio dardanus: molecular data confirm relationships withP. phorcasandP. constantinus

Sister group relationships of the African Mocker Swallowtail,Papilio dardanus, were determined using mitochondrial 16S rRNA and Cytochrome B sequences, and nuclear Elongation Factor EF-1α and the ITS-1 region of the ribosomal RNA locus. All four data sets placedP. dardanusas the sister species ofP. phorcas, withP. constantinusas the next closest relative, and quite distinct from other African Papilios such asP. nobilis. These data support earlier morphological studies indicating that the only two AfricanPapiliospecies with multiple female colour forms have a common ancestor not shared with any other living species. This information is important for conclusions about the evolution of female-limited mimicry in swallowtail butterflies, and successful use of the ITS-1 gene opens up new possibilities for studying this phenomenon withinP. dardanus.

Preferential predation of female butterflies and the evolution of batesian mimicry

BATESIAN mimicry, in which a palatable mimic resembles an unpalatable model, functions to protect insect mimics from birds. In butterflies that show batesian mimicry, female-limited mimicry is common1–3. The orthodox theory to explain this is sexual selection against males4–6. In these theoretical arguments, no difference in predation pressure between the sexes was assumed, but the existence of female-biased predation would enhance the evolution of sex-limited mimicry. To test for differences in attack rate between the sexes, I examined the rates of beak marks on wings of palatable butterflies of Papilionidae and Pieridae, and unpalatable Danaidae. Here I report that females were attacked more frequently than males, though danaids were generally attacked less. The papilionid and pierid males had low attack rates similar to those of danaid females. Analysis of a mathematical model highlighted these tendencies. Comparing a batesian mimetic species and its 'model' species, non-mimetic females were selectively attacked and the males, mimetic females and 'models' were attacked less. Therefore females benefit greatly when they become mimetic, whereas males will benefit much less should they become mimetic. Thus female-limited mimicry will be favoured even if the costs of mimicry to both sexes are the same.

On the myrmecomorph Coquillettia insignis Uhler (Hemiptera: Miridae): arthropod predators as operators in an ant-mimetic system

The nature of female-limited mimicry in the myrmecomorphic plant bug Coquillettia insignis Uhler is described, including aspects of its relation to possible ant models and to co-occurring visual arthropod predators. Twelve species of ants were collected with C. insignis on its host plant Lupinus caudatus Kell., of which six species were common: third instar to adult female mimics closely resemble four of these six species, in both morphology and behaviour. The mimetic significance of these close correspondences is indicated by the results of over 500 feeding trials, using the three most common species of co-occurring visual arthropod predators as operators. Two of these three species (Sussacus papenhoei Gertsch: Salticidae; and Sinea diadema (Fabricius): Reduviidae), classified C. insignis with corresponding models and not with closely related, non-mimetic plant bugs. Furthermore, after having had a single ‘unpleasant’ experience with the ant Formica fusca assassin bugs that had previously accepted C. insignis as prey rejected them in 19 out of 23 trials. These findings indicate that C. insignis is a Batesian mimic, with visual arthropod predators functioning as one class of potential operator. Implications for future research on perception and learning in arthropod predators is briefly discussed.

Why male butterflies are non-mimetic: natural selection, sexual selection, group selection, modification and sieving*

Thomas Belt suggested that the frequent limitation of mimicry in butterflies to the female resulted from sexual selection. Because female butterflies store sperm they can be fully fertile after only one mating; the reproductive success of a male is proportional to the number of times he mates. Sexual selection is therefore much stronger in males than females, with selection coefficients being greater by a small multiple of the number of times a female is courted during her life (long-lived species) or of the reciprocal of the female mortality rate between courtships (short-lived species). As butterflies of both sexes respond to colour when courting, sexual selection resists colour changes especially strongly in males. As a result, genes conferring new mimetic colour patterns can often become established in a butterfly population much more readily if their expression is initially limited to females; when the population size of a Batesian mimic, its model, and its predator fluctuates, such sex-limited genes have an enhanced probability of ultimate fixation in the population, and a reduced chance of loss; this effect is accentuated by the selection of modifiers which improve the mimicry. When the establishment of unimodal mimicry (expressed in both sexes) is favoured in a Batesian mimic, the gene tends to rise to an equilibrium frequency at which modifiers suppressing the expression of the mimicry only in males and'modifiers enhancing the mimicry only in females are favoured. The outcome is female-limited mimicry, or unimodal mimicry with better mimicry in the females, the males either retaining some of their sexual colour or the selective behaviour of the females becoming altered. In a Muellerian mimic there is no such equilibrium and selection ultimately favours expression of mimicry in both sexes and an appropriate alteration in the courtship responses. Hence Muellerian mimicry is seldom female-limited. Exceptional cases appear to result from the sexes flying in separate habitats. The genetical evidence in Papilio and Heliconius favours initial limitation of expression over subsequent modification as the usual basis for female-limited mimicry. Other explanations of female-limited mimicry can be found wanting in various ways; a higher predation rate on females could produce sex-limitation, but is probably not a strong factor. But the greater variability of the female in Lepidoptera may indicate lesser developmental stability, which could result in greater penetrance of mutants in the female, and hence account for the initial female-limitation. At very high densities of a mimetic species which has no non-mimetic form, mimicry tends to deteriorate more rapidly in a unimodal than in an otherwise identical sex-limited species. Although by itself this would equally favour male-limitation, and hence cannot explain the predominance of female-limitation, this effect may over evolutionary time be causing a slight increase in the proportion of sex-limited species among mimics. The stability of some mimetic polymorphisms is investigated by linear approximation: in some instances a stable equilibrium can be changed into an oscillating equilibrium by changes in the population size.