Title: The evolution and genetics of sexually dimorphic ‘dual’ mimicry in the butterfly Elymnias hypermnestra
Sexual dimorphism is a major component of morphological variation across the tree of life, but the mechanisms underlying phenotypic differences between sexes of a single species are poorly understood. We examined the population genomics and biogeography of the common palmfly Elymnias hypermnestra , a dual mimic in which female wing colour patterns are either dark brown (melanic) or bright orange, mimicking toxic Euploea and Danaus species, respectively. As males always have a melanic wing colour pattern, this makes E. hypermnestra a fascinating model organism in which populations vary in sexual dimorphism. Population structure analysis revealed that there were three genetically distinct E. hypermnestra populations, which we further validated by creating a phylogenomic species tree and inferring historical barriers to gene flow. This species tree demonstrated that multiple lineages with orange females do not form a monophyletic group, and the same is true of clades with melanic females. We identified two single nucleotide polymorphisms (SNPs) near the colour patterning gene WntA that were significantly associated with the female colour pattern polymorphism, suggesting that this gene affects sexual dimorphism. Given WntA 's role in colour patterning across Nymphalidae, E. hypermnestra females demonstrate the repeatability of the evolution of sexual dimorphism. more »« less
Van Belleghem, Steven M.; Alicea Roman, Paola A.; Carbia Gutierrez, Heriberto; Counterman, Brian A.; Papa, Riccardo
(, Proceedings of the Royal Society B: Biological Sciences)
null
(Ed.)
Müllerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. Here, we first quantify wing colour pattern differences in the forewing region of 14 co-mimetic colour pattern morphs of the butterfly species Heliconius erato and Heliconius melpomene and measure the extent to which mimicking colour pattern morphs are not perfectly identical. Next, using gene-editing CRISPR/Cas9 KO experiments of the gene WntA , which has been mapped to colour pattern diversity in these butterflies, we explore the exact areas of the wings in which WntA affects colour pattern formation differently in H. erato and H. melpomene. We find that, while the relative size of the forewing pattern is generally nearly identical between co-mimics, the CRISPR/Cas9 KO results highlight divergent boundaries in the wing that prevent the co-mimics from achieving perfect mimicry. We suggest that this mismatch may be explained by divergence in the gene regulatory network that defines wing colour patterning in both species, thus constraining morphological evolution even between closely related species.
Loh, Ling S; Hanly, Joseph J; Carter, Alexander; Chatterjee, Martik; Tsimba, Martina; Shodja, Donya N; Livraghi, Luca; Day, Christopher R; Reed, Robert D; McMillan, W Owen; et al
(, PLOS Biology)
Khila, Abderrahman
(Ed.)
The evolution of sexual secondary characteristics necessitates regulatory factors that confer sexual identity to differentiating tissues and cells. InColias eurythemebutterflies, males exhibit two specialized wing scale types—ultraviolet-iridescent (UVI) and spatulate scales—which are absent in females and likely integral to male courtship behavior. This study investigates the regulatory mechanisms and single-nucleus transcriptomics underlying these two sexually dimorphic cell types during wing development. We show thatDoublesex(Dsx) expression is itself dimorphic and required to repress the UVI cell state in females, while unexpectedly, UVI activation in males is independent fromDsx. In the melanic marginal band,Dsxis required in each sex to enforce the presence of spatulate scales in males, and their absence in females. Single-nucleus RNAseq reveals that UVI and spatulate scale cell precursors each show distinctive gene expression profiles at 40% of pupal development, with marker genes that include regulators of transcription, cell signaling, cytoskeletal patterning, and chitin secretion. Both male-specific cell types share a low expression of theBric-a-brac(Bab) transcription factor, a key repressor of the UVI fate. Bab ChIP-seq profiling suggests that Bab binds thecis-regulatory regions of gene markers associated to UVI fate, including potential effector genes involved in the regulation of cytoskeletal processes and chitin secretion, and loci showing signatures of recent selective sweeps in a UVI-polymorphic population. These findings open new avenues for exploring wing patterning and scale development, shedding light on the mechanisms driving the specification of sex-specific cell states and the differentiation of specialized cell ultrastructures.
Ernst, David A.; Agcaoili, Gabrielle A.; Merrill, Abbigail N.; Westerman, Erica L.
(, Molecular Ecology)
Abstract Sexually dimorphic behaviour is pervasive across animals, with males and females exhibiting different mate selection, parental care, foraging, dispersal, and territorial strategies. However, the genetic underpinnings of sexually dimorphic behaviours are poorly understood. Here we investigate gene networks and expression patterns associated with sexually dimorphic imprinting‐like learning in the butterflyBicyclus anynana. In this species, both males and females learn visual preferences, but learn preferences for different traits and use different signals as salient, unconditioned cues. To identify genes and gene networks associated with this behaviour, we examined gene expression profiles of the brains and eyes of male and female butterflies immediately post training and compared them to the same tissues of naïve individuals. We found more differentially expressed genes and a greater number of associated gene networks in the eyes, indicating a role of the peripheral nervous system in visual imprinting‐like learning. Females had higher chemoreceptor expression levels than males, supporting the hypothesized sexual dimorphic use of chemical cues during the learning process. In addition, genes that influenceB. anynanawing patterns (sexual ornaments), such asinvected,spalt, andapterous, were also differentially expressed in the brain and eye, suggesting that these genes may influence both sexual ornaments and the preferences for these ornaments. Our results indicate dynamic and sex‐specific responses to social scenario in both the peripheral and central nervous systems and highlight the potential role of wing patterning genes in mate preference and learning across the Lepidoptera.
Abstract Selection that acts in a sex-specific manner causes the evolution of sexual dimorphism. Sex-specific phenotypic selection has been demonstrated in many taxa and can be in the same direction in the two sexes (differing only in magnitude), limited to one sex, or in opposing directions (antagonistic). Attempts to detect the signal of sex-specific selection from genomic data have confronted numerous difficulties. These challenges highlight the utility of “direct approaches,” in which fitness is predicted from individual genotype within each sex. Here, we directly measured selection on Single Nucleotide Polymorphisms (SNPs) in a natural population of the sexually dimorphic, dioecious plant, Silene latifolia. We measured flowering phenotypes, estimated fitness over one reproductive season, as well as survival to the next year, and genotyped all adults and a subset of their offspring for SNPs across the genome. We found that while phenotypic selection was congruent (fitness covaried similarly with flowering traits in both sexes), SNPs showed clear evidence for sex-specific selection. SNP-level selection was particularly strong in males and may involve an important gametic component (e.g., pollen competition). While the most significant SNPs under selection in males differed from those under selection in females, paternity selection showed a highly polygenic tradeoff with female survival. Alleles that increased male mating success tended to reduce female survival, indicating sexual antagonism at the genomic level. Perhaps most importantly, this experiment demonstrates that selection within natural populations can be strong enough to measure sex-specific fitness effects of individual loci. Males and females typically differ phenotypically, a phenomenon known as sexual dimorphism. These differences arise when selection on males differs from selection on females, either in magnitude or direction. Estimated relationships between traits and fitness indicate that sex-specific selection is widespread, occurring in both plants and animals, and explains why so many species exhibit sexual dimorphism. Finding the specific loci experiencing sex-specific selection is a challenging prospect but one worth undertaking given the extensive evolutionary consequences. Flowering plants with separate sexes are ideal organisms for such studies, given that the fitness of females can be estimated by counting the number of seeds they produce. Determination of fitness for males has been made easier as thousands of genetic markers can now be used to assign paternity to seeds. We undertook just such a study in S. latifolia, a short-lived, herbaceous plant. We identified loci under sex-specific selection in this species and found more loci affecting fitness in males than females. Importantly, loci with major effects on male fitness were distinct from the loci with major effects on females. We detected sexual antagonism only when considering the aggregate effect of many loci. Hence, even though males and females share the same genome, this does not necessarily impose a constraint on their independent evolution.
Stevens, R.; Guest, E.
(, Biological Journal of the Linnean Society)
Phenotypic variability is ubiquitous. This is especially true in bats where families such as Phyllostomidae encompass as much phenotypic variability as some entire orders of mammals. Typically, phenotypic variability is characterized based on cranial morphology with studies of other functionally important aspects of the phenotype such as legs, feet and wings less frequent. We examined patterns of secondary-sexual dimorphism and allometry of wing elements of the fringed fruit-eating bat (Artibeus fimbriatus) as well as examined for the first time modularity of bat wings. Patterns were based on 13 wing measurements taken from 21 female and 15 males from eastern Paraguay. From a multivariate perspective A. fimbriatus exhibited significant secondary-sexual dimorphism. Females were larger than males for all 13 wing characteristics with significant differences involving the last phalanx of the 4th and 5th digits. Female wings were also relatively larger than male wings from a multivariate perspective as well as the last phalanx of the 4th and 5th digit, after adjusting for wing size based on forearm length. Wing elements were highly variable regarding allometric relationships with some exhibiting no allometric patterns, and others exhibiting isometry or hyperallometry depending on the element. Wings exhibited significant modularity with metacarpals, proximal phalanges and distal phalanges each representing a discrete module. Wings of A. fimbriatus exhibit substantive patterns of dimorphism, allometry and modularity. While the Big Mother Hypothesis is a strong theoretical construct to explain wing dimorphism, there is yet no sound theoretical basis to patterns of allometry and modularity of the wing. Indeed, trying to understand the determinants of variation in wing morphology is ripe for future investigation.
Ruttenberg, Dee M., VanKuren, Nicholas W., Nallu, Sumitha, Yen, Shen-Horn, Peggie, Djunijanti, Lohman, David J., and Kronforst, Marcus R. The evolution and genetics of sexually dimorphic ‘dual’ mimicry in the butterfly Elymnias hypermnestra. Retrieved from https://par.nsf.gov/biblio/10390025. Proceedings of the Royal Society B: Biological Sciences 288.1942 Web. doi:10.1098/rspb.2020.2192.
Ruttenberg, Dee M., VanKuren, Nicholas W., Nallu, Sumitha, Yen, Shen-Horn, Peggie, Djunijanti, Lohman, David J., & Kronforst, Marcus R. The evolution and genetics of sexually dimorphic ‘dual’ mimicry in the butterfly Elymnias hypermnestra. Proceedings of the Royal Society B: Biological Sciences, 288 (1942). Retrieved from https://par.nsf.gov/biblio/10390025. https://doi.org/10.1098/rspb.2020.2192
Ruttenberg, Dee M., VanKuren, Nicholas W., Nallu, Sumitha, Yen, Shen-Horn, Peggie, Djunijanti, Lohman, David J., and Kronforst, Marcus R.
"The evolution and genetics of sexually dimorphic ‘dual’ mimicry in the butterfly Elymnias hypermnestra". Proceedings of the Royal Society B: Biological Sciences 288 (1942). Country unknown/Code not available. https://doi.org/10.1098/rspb.2020.2192.https://par.nsf.gov/biblio/10390025.
@article{osti_10390025,
place = {Country unknown/Code not available},
title = {The evolution and genetics of sexually dimorphic ‘dual’ mimicry in the butterfly Elymnias hypermnestra},
url = {https://par.nsf.gov/biblio/10390025},
DOI = {10.1098/rspb.2020.2192},
abstractNote = {Sexual dimorphism is a major component of morphological variation across the tree of life, but the mechanisms underlying phenotypic differences between sexes of a single species are poorly understood. We examined the population genomics and biogeography of the common palmfly Elymnias hypermnestra , a dual mimic in which female wing colour patterns are either dark brown (melanic) or bright orange, mimicking toxic Euploea and Danaus species, respectively. As males always have a melanic wing colour pattern, this makes E. hypermnestra a fascinating model organism in which populations vary in sexual dimorphism. Population structure analysis revealed that there were three genetically distinct E. hypermnestra populations, which we further validated by creating a phylogenomic species tree and inferring historical barriers to gene flow. This species tree demonstrated that multiple lineages with orange females do not form a monophyletic group, and the same is true of clades with melanic females. We identified two single nucleotide polymorphisms (SNPs) near the colour patterning gene WntA that were significantly associated with the female colour pattern polymorphism, suggesting that this gene affects sexual dimorphism. Given WntA 's role in colour patterning across Nymphalidae, E. hypermnestra females demonstrate the repeatability of the evolution of sexual dimorphism.},
journal = {Proceedings of the Royal Society B: Biological Sciences},
volume = {288},
number = {1942},
author = {Ruttenberg, Dee M. and VanKuren, Nicholas W. and Nallu, Sumitha and Yen, Shen-Horn and Peggie, Djunijanti and Lohman, David J. and Kronforst, Marcus R.},
}
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