Tracing the Origin and Evolution of Supergene Mimicry in Butterflies

Overview

Journal Nat Commun

Specialty Biology

Date 2017 Nov 9

PMID 29116078

Citations 21

Authors

Wei Zhang

Erica Westerman

Eyal Nitzany

Stephanie Palmer

Marcus R Kronforst

Affiliations

Soon will be listed here.

Abstract

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.

Citing Articles

Evolution: A kit for fooling your rivals.

Kopp A Curr Biol. 2024; 34(20):R921-R923.

PMID: 39437728 PMC: 11630061. DOI: 10.1016/j.cub.2024.09.024.

Supergene evolution via gain of autoregulation.

VanKuren N, Sheikh S, Fu C, Massardo D, Lu W, Kronforst M bioRxiv. 2024; .

PMID: 38260248 PMC: 10802445. DOI: 10.1101/2024.01.09.574839.

Acute and Long-Term Consequences of Co-opted doublesex on the Development of Mimetic Butterfly Color Patterns.

VanKuren N, Doellman M, Sheikh S, Palmer Droguett D, Massardo D, Kronforst M Mol Biol Evol. 2023; 40(9).

PMID: 37668300 PMC: 10498343. DOI: 10.1093/molbev/msad196.

Evolutionary genomics of camouflage innovation in the orchid mantis.

Huang G, Song L, Du X, Huang X, Wei F Nat Commun. 2023; 14(1):4821.

PMID: 37563121 PMC: 10415354. DOI: 10.1038/s41467-023-40355-1.

Lactobacillus for ribosome peptide editing cancer.

Yue S, He Q, Picimbon J Clin Transl Oncol. 2023; 25(6):1522-1544.

PMID: 36694080 PMC: 9873400. DOI: 10.1007/s12094-022-03066-5.

References

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

Tuttle E, Bergland A, Korody M, Brewer M, Newhouse D, Minx P . Divergence and Functional Degradation of a Sex Chromosome-like Supergene. Curr Biol. 2016; 26(3):344-50. PMC: 4747794. DOI: 10.1016/j.cub.2015.11.069. View

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

Llaurens V, Whibley A, Joron M . Genetic architecture and balancing selection: the life and death of differentiated variants. Mol Ecol. 2017; 26(9):2430-2448. DOI: 10.1111/mec.14051. View

Hines H, Counterman B, Papa R, Albuquerque de Moura P, Cardoso M, Linares M . Wing patterning gene redefines the mimetic history of Heliconius butterflies. Proc Natl Acad Sci U S A. 2011; 108(49):19666-71. PMC: 3241772. DOI: 10.1073/pnas.1110096108. View

Jones R, Le Poul Y, Whibley A, Merot C, Ffrench-Constant R, Joron M . Wing shape variation associated with mimicry in butterflies. Evolution. 2013; 67(8):2323-34. DOI: 10.1111/evo.12114. View

Smith J, Kronforst M . Do Heliconius butterfly species exchange mimicry alleles?. Biol Lett. 2013; 9(4):20130503. PMC: 3730661. DOI: 10.1098/rsbl.2013.0503. View

Supple M, Hines H, Dasmahapatra K, Lewis J, Nielsen D, Lavoie C . Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies. Genome Res. 2013; 23(8):1248-57. PMC: 3730099. DOI: 10.1101/gr.150615.112. View

McDonald J, Kreitman M . Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991; 351(6328):652-4. DOI: 10.1038/351652a0. View

10.

Browning S, Browning B . Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet. 2007; 81(5):1084-97. PMC: 2265661. DOI: 10.1086/521987. View

11.

Librado P, Rozas J . DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25(11):1451-2. DOI: 10.1093/bioinformatics/btp187. View

12.

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

13.

Guindon S . Bayesian estimation of divergence times from large sequence alignments. Mol Biol Evol. 2010; 27(8):1768-81. DOI: 10.1093/molbev/msq060. View

14.

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

15.

Kunte K . Mimetic butterflies support Wallace's model of sexual dimorphism. Proc Biol Sci. 2008; 275(1643):1617-24. PMC: 2602815. DOI: 10.1098/rspb.2008.0171. View

16.

Gronau I, Hubisz M, Gulko B, Danko C, Siepel A . Bayesian inference of ancient human demography from individual genome sequences. Nat Genet. 2011; 43(10):1031-4. PMC: 3245873. DOI: 10.1038/ng.937. View

17.

Kronforst M, Papa R . The functional basis of wing patterning in Heliconius butterflies: the molecules behind mimicry. Genetics. 2015; 200(1):1-19. PMC: 4423356. DOI: 10.1534/genetics.114.172387. View

18.

Ashkenazy H, Penn O, Doron-Faigenboim A, Cohen O, Cannarozzi G, Zomer O . FastML: a web server for probabilistic reconstruction of ancestral sequences. Nucleic Acids Res. 2012; 40(Web Server issue):W580-4. PMC: 3394241. DOI: 10.1093/nar/gks498. View

19.

Walraven P . A closer look at the tritanopic convergence point. Vision Res. 1974; 14(12):1339-43. DOI: 10.1016/0042-6989(74)90007-8. View

20.

Huang W, Li L, Myers J, Marth G . ART: a next-generation sequencing read simulator. Bioinformatics. 2011; 28(4):593-4. PMC: 3278762. DOI: 10.1093/bioinformatics/btr708. View