Article

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

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Abstract

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.

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... As an alternative hypothesis, polymorphic Batesian mimicry may be explained by sexual selection and ecological-physiological trade-offs (Burns, 1966;Cook et al., 1994;Katoh et al., 2020;Ohsaki, 2005;Vane-Wright, 1984), or neutral evolutionary processes such as isolation by distance and phylogenetic constraint. In the simple neutral process, the mimetic and nonmimetic phenotypes have similar fitness independent of their frequencies. ...
... This would also enable us to address the evolution of the responsible gene, dsx, of polymorphic Batesian mimicry in Papilio butterflies (Iijima et al., 2018(Iijima et al., , 2019Komata et al., 2016;Kunte et al., 2014;Nishikawa et al., 2015;Palmer & Kronforst, 2020;Zhang et al., 2017), which should be the focus of further investigation. This dsx gene may not only control the mimetic forms, but also have pleiotropic, slightly deleterious epistatic effects potentially related to the "cost of mimics" (Katoh et al., 2020). Unveiling the molecular evolutionary dynamics of the dsx across the Ryukyu Islands in association with the NFDS for mimetic types is necessary to understand the establishment of P. polytes mimicry interacting with ecological factors. ...
Article
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Batesian mimicry is a striking example of Darwinian evolution, in which a mimetic species resembles toxic or unpalatable model species, thereby receiving protection from predators. In some species exhibiting Batesian mimicry, nonmimetic individuals coexist as polymorphism in the same population despite the benefits of mimicry. In a previous study, we proposed that the abundance of mimics is limited by that of the models, leading to polymorphic Batesian mimicry in the swallowtail butterfly, Papilio polytes, on the Ryukyu Islands in Japan. We found that their mimic ratios (MRs), which varied among the Islands, were explained by the model abundance of each habitat, rather than isolation by distance or phylogenetic constraint based on the mitochondrial DNA (mtDNA) analysis. In the present study, this possibility was reexamined based on hundreds of nuclear single nucleotide polymorphisms (SNPs) of 93 P. polytes individuals from five Islands of the Ryukyus. We found that the population genetic and phylogenetic structures of P. polytes largely corresponded to the geographic arrangement of the habitat Islands, and the genetic distances among island populations show significant correlation with the geographic distances, which was not evident by the mtDNA‐based analysis. A partial Mantel test controlling for the present SNP‐based genetic distances revealed that the MRs of P. polytes were strongly correlated with the model abundance of each island, implying that negative frequency‐dependent selection interacting with model species shaped and maintained the mimetic polymorphism. Taken together, our results support the possibility that predation pressure, not isolation by distance or other neutral factors, is a major driving force of evolution of the Batesian mimicry in P. polytes from the Ryukyus.
... Insects 2022, 13, x FOR PEER REVIEW 3 of 22 for predation, which is not affordable for males [44][45][46][47][48][49]. While this line of explanation is reasonable, it does not take phenotypic plasticity into account. ...
... Females are often under higher predation pressure than males due to their higher nutritious quality of eggs in the abdomen [44,45]. The mimetic form has some disadvantages; it is less active [47,48] and has shorter life expectancy [49]. The mimetic forms are not always effective; their effectiveness depends on the number of sympatric individuals of the model species [69][70][71][72][73][74]. ...
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... Phylogenetic analyses show that FLM derived from sexually monomorphic non-mimetic ancestors (Kunte 2009, Timmermans et al. 2017 suggesting that mimicry in FLM species is associated with a costly displacement from an ancestral non-mimetic phenotype. In the female-limited polymorphic butterfly Papilio polytes, where both mimetic and non-mimetic females co-exist, the mimetic allele reduces the pre-adult survival rate (Komata et al. 2020, Katoh et al. 2020) (but see Komata et al. 2018 in the FLM butterfly Papilio memnon), highlighting cost associated with mimicry. Such trade-off between developmental constraints favoring the ancestral trait and selection promoting mimicry might differ between sexes: if predation is lower in males, the constraints limiting mimicry may overcome the benefit from mimicry in males, whereas in females the higher predation pressure may promote mimicry. ...
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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 favouring mimicry toward defended species could be higher in females because of their slower flight, and thus overcome developmental constraints favouring 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 hypothesise 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 Batesian mimics. This article is protected by copyright. All rights reserved.
... As mentioned above, although parental genotypes likely play pivotal roles in offspring survival, we cannot conclude that offspring genotypes did not negatively affect larval survival, as insufficient sample size for a cross between heterozygous females and males might have biased our results. According to Katoh et al. 20 , dsx-H produces mild deleterious effects on larval survival; in that case, it may be difficult to detect this deleterious effect with insufficient sample size. ...
Article
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Dimorphic female-limited Batesian mimicry in the swallowtail butterfly Papilio polytes is regulated by the supergene locus H, harbouring the mimetic (H) and non-mimetic (h) doublesex (dsx) gene. In the present study, we demonstrated that dsx-H negatively affects the number of eggs laid, hatching rate, larval survival rate, and adult lifespan. When crossed with hh males, the number of eggs laid of mimetic females (genotype HH) was lower than that of non-mimetic females (hh). Moreover, hh and Hh females laid fewer eggs when crossed with HH males. The hatching and larval survival rates were lower when both female and male parents harboured dsx-H. The adult lifespan of HH females was shorter than that of hh females, while it was similar in males regardless of the genotype. These findings suggest the presence of a cost–benefit balance of Batesian mimicry, which is evolved to avoid predation but is accompanied by physiological deficits, in this species.
... As an alternative hypothesis, polymorphic Batesian mimicry may be explained by neutral evolutionary processes, such as isolation-by-distance and phylogenetic constraint, in addition to other hypotheses including sexual selection and ecological-physiological trade-offs (Burns 1966;Vane-Wright 1984;Cook et al. 1994;Ohsaki 2005;Katoh et al. 2020). In the simple neutral process, the mimetic and non-mimetic phenotypes have similar fitness independent of their frequencies. ...
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Experiments were conducted to examine the adaptive significance of Batesian mimicry in the swallowtail butterfly, Papilio polytes, with its model, Pacbliopta aristolochiae, an alkaloidal butterfly. The female of Pap. polytes is polymorphic, whereas the male is monomorphic. Two forms of the female, f. polytes mimic and f. cyrus non-mimic, were used in these experiments. Naive birds, brown-eared bulbuls Hypsipetes amaurotis pryeri, were trained to take food from two feeders in captivity, and then were offered Pach. aristolochiae in one of the feeders. After experiencing an uncomfortable encounter with this species, the birds reduced the frequency of taking regular food from the feeder where the butterfly had been placed. This result suggests that the birds can learn not only the model itself but also the place where they have experienced it. Thereafter, the birds also came to avoid the mimetic form of f. polytes. It is suspected that wild predators behave in the same way. These findings imply that it is adaptive for the mimic to overlap its habitats and daily activity with those of the model species.
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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.
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Summary • Batesian mimicry describes the situation in which a palatable mimic resembles an unpalatable model. In some species of butterflies, both sexes mimic, but in others only females do. Two mechanisms have been proposed to generate female-limited mimicry: sexual selection via female choice, and sexual selection via male–male competition. Each is not satisfactory because of too many exceptions. • I hypothesized that reductions in physiological life span because of mimicry constituted the costs, while extensions of ecological life span because of mimicry constituted the benefits. Mimicry would result from the balance of a costs/benefits relationship; when balances are favourable, mimicry occurs. • Non-mimetic females of female-limited mimicry butterfly Papilio polytes lived longer than its mimetic females in a butterfly farm greenhouse. Therefore, reduction in physiological life span must be a cost of mimicry. • Male-biased sex ratios were found in 11 of the 14 non-mimetic and non-model species netted in the Kakamega tropical rainforest in west Kenya, in other one species almost equivalent, and in remaining two species female-biased. For each species, the sexes netted less frequently had more beak marks than those netted more frequently. That is, the biased sex ratios could be responsible for the higher predation rates of the opposite sex. • Predators may have selectively attacked females with wider thoraxes, which flew at higher levels and flew more quickly. However, attack rates on males of some species may be high or low regardless of thorax width. • As the benefits accrue largely to females with wider thorax due to female-biased predation, balances of costs/benefits relationships divide participating species into three theoretical groups: those in which the adaptation is favourable for both sexes; favourable only for females; and unfavourable for both sexes. • In female-limited mimics of five species, thorax widths varied, whereas thoraxes tended to be wider in both-sex mimics of four species. Journal of Animal Ecology (2005) doi: 10.1111/j.1365-2656.2005.00972.x
Article
The B-chromosomes (B's; supernumeraries) of the mealy bug, Pseudococcus obscurus Essig, segregate preferentially into the two functional products of male meiosis. This segregation thus serves as an accumulation mechanism. A cytological study of a population from Oakland, California, confirmed the results obtained earlier that the B's are harmful and are maintained only because of their accumulation mechanism. The wild females were studied directly. The number of B's in the males was determined by analyzing ten or more daughters of females without B's (0B females) after these were inseminated by wild males. The 0B females were exposed to the wild males in screen cages. The analysis of 4732 daughters of 231 caged females indicated that among the males which inseminated these females, there were 19.9% 0B males and the mean number of B's was 1.46 0.07. Among 224 wild females which were collected at about the same time there were 12.5% 0B females, and the mean number of B's was 1.88 0.09. Since the frequencies of the B's in the population changed only slightly from generation to generation, the expected zygotes of this generation were assumed to be similar to those from which both the males and the females developed. The expected zygotes were calculated from the observed frequencies of the B's among the sperm and the known rates of transmission in females. The zygotes were very similar to the females but quite different from the males. It was concluded, therefore, that the B's had little or no effect on the females carrying them, but reduced the fitness of the males. The fitness of the 0B, 1B, 2B, 3B and 4B males was calculated to be 1.00, 0.64, 0.56, 0.38 and 0.20 respectively. The rate of transmission of the B's decreased with the increase in the number of B's, from 0.84 in 1B males to 0.51 in 4B males. This decrease, and the decrease in male fitness with the increase in the number of B's are expected to help stabilize the number of B's in the population.
Article
Mimicry theory played a prominent role in the development of natural selection theory, and sparked a long-lasting interest in the observation that Batesian mimicry in some butterflies is female limited and polymorphic. Mimetic females of polymorphic species clearly have a selective advantage due to reduced predation pressure, but the selective forces that maintain nonmimetic female forms remain unclear. Attention has lately been focused on three explanations based on sexual selection: (1) male mate preference, (2) pseudo-sexual selection and (3) sexual harassment avoidance. These are thought to favour nonmimetic female forms and allow them to persist in the population via balancing selection. Here I review the assumptions and evidence for each of these hypotheses and assess their relative merit. I find that: (a) key predictions of the hypotheses have not been tested, (b) the hypotheses interpret surrogate measures of fitness trade-offs implicit in balancing selection (e.g. mating frequency) differently, and (c) sexual selection may not maintain nonmimetic females at high mimic frequencies if male mate preference is frequency dependent. As a result, none of the hypotheses is unequivocally supported by available data. I show that a fourth, non-sexual selectionist hypothesis, namely that physiological trade-offs maintain mimetic female polymorphism, is based on unclear assumptions and probably explains minor variation in female polymorphism. Finally, I show that the basic framework of frequency-dependent mimetic advantage, independent of sexual selection, can adequately explain female-limited mimetic polymorphism in a broad range of species. Testing this framework should be a priority in resolving this problem.
Article
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.
Article
Papilio polytes L. is a mimetic Swallowtail butterfly widely distributed in South East Asia. It has four female forms, three mimetic, and one non-mimetic resembling the monomorphic male in appearance. The various female forms are now shown to be controlled by allelomorphs at a single autosomal locus and not by independent genes as previously thought. The effects of the allelomorphs controlling the mimetic patterns are sex-limited to the female. There is some evidence that the locus is a complex one consisting of two or more tightly linked genes. As in previous investigations into mimicry in Swallowtails the dominance tends to be complete between sympatric forms. The accuracy of the mimicry depends not only on the presence of the appropriate major genes but also on the rest of the gene complex. Thus within a race there is an integrated genetic system and on outcrossing this becomes disturbed, leading to poorer mimicry. The system of modifiers controlling the accuracy of the mimetic pattern is closely paralleled by that in P. dardanus. In particular, in P. polytes f. theseus appears to differ from f. polytes only as a result of the presence of a modifier system, as does f. hippocoon from f. hippocoonides in P. dardanus. In P. dardanus from Ethiopia it was found that specific modifiers adjusting the tail length of mimetic females have been selected for, thus improving the mimicry. An analogous situation has been found in P. polytes although here the control is more effective in that the resulting difference in tail length between the mimetic and non-mimetic forms can be as much as 10 mm, whereas in P. dardanus it rarely exceeds 3 mm. The great similarity in the genetic structure of P. polytes and P. dardanus (as well as P. memnon) strongly suggests that selection for a mimetic polymorphism results in the evolution of very similar genetic control mechanisms in different species - that is to say it is the nature of the selection rather than the species involved which determines the genetic architecture.
Article
Y chromosome haplotyping based on microsatellites or single nucleotide polymorphisms has recently proven to be a powerful approach for evolutionary studies of human populations, and also holds great promise for the studies of wild species. However, the use of the approach is hampered in most natural populations by the lack of Y chromosome markers and sequence information. Here, we report the large-scale development of Y chromosome conserved anchor tagged sequence (YCATS) markers in mammals by a polymerase chain reaction screening approach. Exonic primers flanking 48 different introns of Y-linked genes were developed based on human and mouse sequences, and screened on a set of 20 different mammals. On average about 10 introns were amplified for each species and a total of 100 kb of Y chromosome sequence were obtained. Intron size in humans was a reasonable predictor of intron size in other mammals (r2 = 0.45) and there was a negative correlation between human fragment size and amplification success. We discuss a number of factors affecting the possibility of developing conserved Y chromosome markers, including fast evolution of Y chromosome sequences due to male-biased mutation and adaptive evolution of male-specific genes, dynamic evolution of the Y chromosome due to being a nonrecombining unit, and homology with X chromosome sequences.
Temporal change in records of the mimetic butterfly Papilio polytes with establishment of its model Pachliopta aristolochiae in the Ryukyu Island
  • K Uesugi
Uesugi, K. (1991). Temporal change in records of the mimetic butterfly Papilio polytes with establishment of its model Pachliopta aristolochiae in the Ryukyu Island. Japanese Journal of Entomology, 59, 183-198.
Genes in conflict: The biology of selfish genetic elements
  • B Austin
  • T Robert
Austin, B., & Robert, T. (2006). Genes in conflict: The biology of selfish genetic elements. Cambridge, UK: Harvard University Press.
Introduction to conservation genetics
  • R Frankham
  • J D Ballou
  • D A Briscoe
Frankham, R., Ballou, J. D., & Briscoe, D. A. (2002). Introduction to conservation genetics. Cambridge, UK: Cambridge University Press.
Proceedings of the Entomological Society of London
  • A. R. Wallace