Genomic Architecture and Functional Unit of Mimicry Supergene in Female Limited Batesian Mimic Butterflies

Overview

Journal Philos Trans R Soc Lond B Biol Sci

Specialty Biology

Date 2022 Jun 13

PMID 35694751

Authors

Shinya Komata

Rei Kajitani

Takehiko Itoh

Haruhiko Fujiwara

Affiliations

Soon will be listed here.

Abstract

It has long been suggested that dimorphic female-limited Batesian mimicry of two closely related butterflies, and is controlled by supergenes. Whole-genome sequencing, genome-wide association studies and functional analyses have recently identified mimicry supergenes, including the gene. Although supergenes of both the species are composed of highly divergent regions between mimetic and non-mimetic alleles and are located at the same chromosomal locus, they show critical differences in genomic architecture, particularly with or without an inversion: . has an inversion, but . does not. This review introduces and compares the detailed genomic structure of mimicry supergenes in two species, including gene composition, repetitive sequence composition, breakpoint/boundary site structure, chromosomal inversion and linkage disequilibrium. Expression patterns and functional analyses of the respective genes within or flanking the supergene suggest that and other genes are involved in mimetic traits. In addition, structural comparison of the corresponding region for the mimicry supergene among further species suggests three scenarios for the evolution of the mimicry supergene between the two species. The structural features revealed in the mimicry supergene provide insight into the formation, maintenance and evolution of supergenes. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.

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References

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60. PMC: 2705234. DOI: 10.1093/bioinformatics/btp324. View

Perez C, Adachi S, Nong Q, Adhitama N, Matsuura T, Natsume T . Sense-overlapping lncRNA as a decoy of translational repressor protein for dimorphic gene expression. PLoS Genet. 2021; 17(7):e1009683. PMC: 8351930. DOI: 10.1371/journal.pgen.1009683. View

Thompson M, Jiggins C . Supergenes and their role in evolution. Heredity (Edinb). 2014; 113(1):1-8. PMC: 4815649. DOI: 10.1038/hdy.2014.20. View

Kunte K, Zhang W, Tenger-Trolander A, Palmer D, Martin A, Reed R . doublesex is a mimicry supergene. Nature. 2014; 507(7491):229-32. DOI: 10.1038/nature13112. View

Nishikawa H, Iga M, Yamaguchi J, Saito K, Kataoka H, Suzuki Y . Molecular basis of wing coloration in a Batesian mimic butterfly, Papilio polytes. Sci Rep. 2013; 3:3184. PMC: 3822385. DOI: 10.1038/srep03184. View

Sanchez-Morgan N, Kirsch K, Trackman P, Sonenshein G . UXT Is a LOX-PP Interacting Protein That Modulates Estrogen Receptor Alpha Activity in Breast Cancer Cells. J Cell Biochem. 2017; 118(8):2347-2356. DOI: 10.1002/jcb.25893. View

Hassan B, Li L, Bremer K, Chang W, Pinsonneault J, Vaessin H . Prospero is a panneural transcription factor that modulates homeodomain protein activity. Proc Natl Acad Sci U S A. 1997; 94(20):10991-6. PMC: 23559. DOI: 10.1073/pnas.94.20.10991. View

Li S, Zhang G, Yuan J, Deng C, Gao W . Repetitive sequences and epigenetic modification: inseparable partners play important roles in the evolution of plant sex chromosomes. Planta. 2016; 243(5):1083-95. DOI: 10.1007/s00425-016-2485-7. View

Caceres M, Ranz J, Barbadilla A, Long M, Ruiz A . Generation of a widespread Drosophila inversion by a transposable element. Science. 1999; 285(5426):415-8. DOI: 10.1126/science.285.5426.415. View

10.

Schwander T, Libbrecht R, Keller L . Supergenes and complex phenotypes. Curr Biol. 2014; 24(7):R288-94. DOI: 10.1016/j.cub.2014.01.056. View

11.

Zhou Y, Ge R, Wang R, Liu F, Huang Y, Liu H . UXT potentiates angiogenesis by attenuating Notch signaling. Development. 2015; 142(4):774-86. PMC: 4325377. DOI: 10.1242/dev.112532. View

12.

Iijima T, Yoda S, Fujiwara H . The mimetic wing pattern of butterflies is regulated by a -orchestrated gene network. Commun Biol. 2019; 2:257. PMC: 6620351. DOI: 10.1038/s42003-019-0510-7. View

13.

Fujiwara H, Nishikawa H . Functional analysis of genes involved in color pattern formation in Lepidoptera. Curr Opin Insect Sci. 2016; 17:16-23. DOI: 10.1016/j.cois.2016.05.015. View

14.

Charlesworth D, Charlesworth B . Theoretical genetics of Batesian mimicry II. Evolution of supergenes. J Theor Biol. 1975; 55(2):305-24. DOI: 10.1016/s0022-5193(75)80082-8. View

15.

Kato Y, Perez C, Ishak N, Nong Q, Sudo Y, Matsuura T . A 5' UTR-Overlapping LncRNA Activates the Male-Determining Gene doublesex1 in the Crustacean Daphnia magna. Curr Biol. 2018; 28(11):1811-1817.e4. DOI: 10.1016/j.cub.2018.04.029. View

16.

Latorre-Estivalis J, Almeida F, Pontes G, Dopazo H, Barrozo R, Lorenzo M . Evolution of the Insect PPK Gene Family. Genome Biol Evol. 2021; 13(9). PMC: 8438182. DOI: 10.1093/gbe/evab185. View

17.

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A . The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010; 20(9):1297-303. PMC: 2928508. DOI: 10.1101/gr.107524.110. View

18.

VanKuren N, Massardo D, Nallu S, Kronforst M . Butterfly Mimicry Polymorphisms Highlight Phylogenetic Limits of Gene Reuse in the Evolution of Diverse Adaptations. Mol Biol Evol. 2019; 36(12):2842-2853. PMC: 7968384. DOI: 10.1093/molbev/msz194. View

19.

Westerman E, Antonson N, Kreutzmann S, Peterson A, Pineda S, Kronforst M . Behaviour before beauty: signal weighting during mate selection in the butterfly . Ethology. 2021; 125(8):565-574. PMC: 7938376. DOI: 10.1111/eth.12884. View

20.

Zelle K, Lu B, Pyfrom S, Ben-Shahar Y . The genetic architecture of degenerin/epithelial sodium channels in Drosophila. G3 (Bethesda). 2013; 3(3):441-50. PMC: 3583452. DOI: 10.1534/g3.112.005272. View