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Publications

Little is known about the extent to which species use homologous regulatory architectures to achieve phenotypic convergence. By characterizing chromatin accessibility and gene expression in developing wing tissues, we compared the regulatory architecture of convergence between a pair of mimetic butterfly species. Although a handful of color pattern genes are known to be involved in their convergence, our data suggest that different mutational paths underlie the integration of these genes into wing pattern development. 

We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome.

The evolutionary importance of hybridization and introgression has long been debated 1. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation 2, 3, 4, 5. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. 

Mimicry—whereby warning signals in different species evolve to look similar—has long served as a paradigm of convergent evolution. Little is known, however, about the genes that underlie the evolution of mimetic phenotypes or to what extent the same or different genes drive such convergence. Here, we characterize one of the major genes responsible for mimetic wing pattern evolution in Heliconius butterflies.

Identifying the genomic changes that control morphological variation and understanding how they generate diversity is a major goal of evolutionary biology. In Heliconius butterflies, a small number of genes control the development of diverse wing colour patterns. Here, we used full-genome sequencing of individuals across the Heliconius erato radiation and closely related species to characterize genomic variation associated with wing pattern diversity.

2020

Many functionally connected loci foster adaptive diversification along a neotropical hybrid zone

JJ Lewis, SM Van Belleghem, R Papa, CG Danko, RD Reed

Science advances 6 (39), eabb8617

Correction to ‘Perfect mimicry between Heliconius butterflies is constrained by genetics and development’

Steven M Van Belleghem, Paola A Alicea Roman, Heriberto Carbia Gutierrez, Brian A Counterman, Riccardo Papa

Proceedings of the Royal Society B 287 (1933), 20201781

Divergence of chemosensing during the early stages of speciation

Bas van Schooten, Jesyka Meléndez-Rosa, Steven M Van Belleghem, Chris D Jiggins, John D Tan, W Owen McMillan, Riccardo Papa

Proceedings of the National Academy of Sciences 117 (28), 16438-16447

WntGenes in wing pattern development of Coliadinae butterflies

Jennifer Fenner, Caleb Benson, Luis Rodriguez-Caro, Anna Ren, Riccardo Papa, Arnaud Martin, Federico Hoffmann, Ryan Range, Brian A Counterman

Front. Ecol. Evol 8, 00197

Multiple loci control eyespot number variation on the hindwings of Bicyclus anynana butterflies

Angel G Rivera-Colón, Erica L Westerman, Steven M Van Belleghem, Antónia Monteiro, Riccardo Papa

Genetics 214 (4), 1059-1078

Selection and gene flow define polygenic barriers between incipient butterfly species

Steven M Van Belleghem, Jared M Cole, Gabriela Montejo Kovacevich, Caroline N Bacquet, W Owen McMillan, Riccardo Papa, Brian A Counterman

BioRxiv

Visual mate preference evolution during butterfly speciation is linked to neural processing genes

Matteo Rossi, Alexander E Hausmann, Timothy J Thurman, Stephen H Montgomery, Riccardo Papa, Chris D Jiggins, W Owen Mcmillan, Richard M Merrill

bioRxiv

Neural processing genes are linked to divergence in visual mate preference in sympatric Heliconius butterflies

Matteo Rossi, Timothy J Thurman, Alexander E Hausmann, Stephen H Montgomery, Riccardo Papa, Chris D Jiggins, W Owen Mcmillan, Richard M Merrill

bioRxiv

Perfect mimicry between Heliconius butterflies is constrained by genetics and development

Authors

Steven M Van Belleghem, Paola A Alicea Roman, Heriberto Carbia Gutierrez, Brian A Counterman, Riccardo Papa

bioRxiv

2019

Interplay between developmental flexibility and determinism in the evolution of mimetic Heliconius wing patterns

Carolina Concha, Richard WR Wallbank, Joseph J Hanly, Jennifer Fenner, Luca Livraghi, Edgardo Santiago Rivera, Daniel F Paulo, Carlos Arias, Marta Vargas, Manu Sanjeev, Colin Morrison, David Tian, Paola Aguirre, Sabrina Ferrara, Jessica Foley, Carolina Pardo-Diaz, Camilo Salazar, Mauricio Linares, Darli Massardo, Brian A Counterman, Maxwell J Scott, Chris D Jiggins, Riccardo Papa, Arnaud Martin, W Owen McMillan

Current Biology 29 (23), 3996-4009. e4

Parallel evolution of ancient, pleiotropic enhancers underlies butterfly wing pattern mimicry

James J Lewis, Rachel C Geltman, Patrick C Pollak, Kathleen E Rondem, Steven M Van Belleghem, Melissa J Hubisz, Paul R Munn, Linlin Zhang, Caleb Benson, Anyi Mazo-Vargas, Charles G Danko, Brian A Counterman, Riccardo Papa, Robert D Reed

Proceedings of the National Academy of Sciences 116 (48), 24174-24183

Genomic architecture and introgression shape a butterfly radiation

Nathaniel B Edelman, Paul B Frandsen, Michael Miyagi, Bernardo Clavijo, John Davey, Rebecca B Dikow, Gonzalo García-Accinelli, Steven M Van Belleghem, Nick Patterson, Daniel E Neafsey, Richard Challis, Sujai Kumar, Gilson RP Moreira, Camilo Salazar, Mathieu Chouteau, Brian A Counterman, Riccardo Papa, Mark Blaxter, Robert D Reed, Kanchon K Dasmahapatra, Marcus Kronforst, Mathieu Joron, Chris D Jiggins, W Owen McMillan, Federica Di Palma, Andrew J Blumberg, John Wakeley, David Jaffe, James Mallet

Science 366 (6465), 594-599

Comparative transcriptomics provides insights into reticulate and adaptive evolution of a butterfly radiation

Wei Zhang, Brian X Leon-Ricardo, Bas van Schooten, Steven M Van Belleghem, Brian A Counterman, W Owen McMillan, Marcus R Kronforst, Riccardo Papa

Genome biology and evolution 11 (10), 2963-2975

2018

Conserved microbiota among young Heliconius butterfly species

Bas van Schooten, Filipa Godoy-Vitorino, W Owen McMillan, Riccardo Papa

PeerJ 6, e5502

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

Steven M Van Belleghem, Margarita Baquero, Riccardo Papa, Camilo Salazar, W Owen McMillan, Brian A Counterman, Chris D Jiggins, Simon H Martin

Molecular ecology 27 (19), 3852-3872

patternize: An R package for quantifying colour pattern variation

Steven M Van Belleghem, Riccardo Papa, Humberto Ortiz‐Zuazaga, Frederik Hendrickx, Chris D Jiggins, W Owen McMillan, Brian A Counterman

Molecular ecology 27 (19), 3852-3872

The genetic basis of hindwing eyespot number variation in Bicyclus anynana butterflies

Angel G Rivera-Colón, Erica L Westerman, Steven M Van Belleghem, Antónia Monteiro, Riccardo Papa

bioRxiv, 504506

2017

Complex modular architecture around a simple toolkit of wing pattern genes

AuthorsSteven M Van Belleghem, Pasi Rastas, Alexie Papanicolaou, Simon H Martin, Carlos F Arias, Megan A Supple, Joseph J Hanly, James Mallet, James J Lewis, Heather M Hines, Mayte Ruiz, Camilo Salazar, Mauricio Linares, Gilson RP Moreira, Chris D Jiggins, Brian A Counterman, W Owen McMillan, Riccardo Papa

Nature Ecology & Evolution 1 (3), 1-12

2016

Genome-wide analysis of ionotropic receptors provides insight into their evolution in Heliconius butterflies

Bas van Schooten, Chris D Jiggins, Adriana D Briscoe, Riccardo Papa

BMC genomics 17 (1), 254

2015

Divergence with gene flow across a speciation continuum of Heliconius butterflies

Megan A Supple, Riccardo Papa, Heather M Hines, W Owen McMillan, Brian A Counterman

BMC evolutionary biology 15 (1), 204

The functional basis of wing patterning in Heliconius butterflies: the molecules behind mimicry

Marcus R Kronforst, Riccardo Papa

Genetics 200 (1), 1-19

What barcode sequencing reveals about the shark fishery in Peru

Ximena Velez-Zuazo, Joanna Alfaro-Shigueto, Jeffrey Mangel, Riccardo Papa, Ingi Agnarsson

Fisheries Research 161, 34-41

2014

Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato

Nicola J Nadeau, Mayté Ruiz, Patricio Salazar, Brian Counterman, Jose Alejandro Medina, Humberto Ortiz-Zuazaga, Anna Morrison, W Owen McMillan, Chris D Jiggins, Riccardo Papa

Genome research 24 (8), 1316-1333

Population ecology and genetics of the invasive lionfish in Puerto Rico.

Carlos Toledo-Hernández, Ximena Vélez-Zuazo, Claudia Patricia Ruiz-Diaz, Ana Rita Patricio, Pascal Mege, Melissa Navarro, Alberto Miguel Sabat, Ricardo Betancur-R, Riccardo Papa

Aquatic Invasions 9 (2)

The Genomics of an Adaptive Radiation: Insights Across the Heliconius Speciation Continuum

Megan Supple, Riccardo Papa, Brian Counterman, W Owen McMillan

Ecological genomics, 249-271

2013

Molecular barcoding of an atypical cyprinid population assessed by cytochrome b gene sequencing

Stefania Chiesa, Laura Filonzi, Marina Vaghi, Riccardo Papa, Francesco Nonnis Marzano

Zoological science 30 (5), 408-413

Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in Heliconius erato

Riccardo Papa, Durrell D Kapan, Brian A Counterman, Karla Maldonado, Daniel P Lindstrom, Robert D Reed, H Frederik Nijhout, Tomas Hrbek, W Owen McMillan

PLoS One 8 (3), e57033

2012

Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation

Heather M Hines, Riccardo Papa, Mayte Ruiz, Alexie Papanicolaou, Charles Wang, H Frederik Nijhout, W Owen McMillan, Robert D Reed

BMC genomics 13 (1), 288

532012

Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand

Arnaud Martin, Riccardo Papa, Nicola J Nadeau, Ryan I Hill, Brian A Counterman, Georg Halder, Chris D Jiggins, Marcus R Kronforst, Anthony D Long, W Owen McMillan, Robert D Reed

Proceedings of the National Academy of Sciences 109 (31), 12632-12637

Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

Kanchon K Dasmahapatra, James R Walters, Adriana D Briscoe, John W Davey, Annabel Whibley, Nicola J Nadeau, Aleksey V Zimin, Daniel ST Hughes, Laura C Ferguson, Simon H Martin, Camilo Salazar, James J Lewis, Sebastian Adler, Seung-Joon Ahn, Dean A Baker, Simon W Baxter, Nicola L Chamberlain, Ritika Chauhan, Brian A Counterman, Tamas Dalmay, Lawrence E Gilbert, Karl Gordon, David G Heckel, Heather M Hines, Katharina J Hoff, Peter WH Holland, Emmanuelle Jacquin-Joly, Francis M Jiggins, Robert T Jones, Durrell D Kapan, Paul Kersey, Gerardo Lamas, Daniel Lawson, Daniel Mapleson, Luana S Maroja, Arnaud Martin, Simon Moxon, William J Palmer, Riccardo Papa, Alexie Papanicolaou, Yannick Pauchet, David A Ray, Neil Rosser, Steven L Salzberg, Megan A Supple, Alison Surridge, Ayse Tenger-Trolander, Heiko Vogel, Paul A Wilkinson, Derek Wilson, James A Yorke, Furong Yuan, Alexi L Balmuth, Cathlene Eland, Karim Gharbi, Marian Thomson, Richard A Gibbs, Yi Han, Joy C Jayaseelan, Christie Kovar, Tittu Mathew, Donna M Muzny, Fiona Ongeri, Ling-Ling Pu, Jiaxin Qu, Rebecca L Thornton, Kim C Worley, Yuan-Qing Wu, Mauricio Linares, Mark L Blaxter, Mathieu Joron, Marcus R Kronforst, Sean P Mullen, Robert D Reed, Steven E Scherer, Stephen Richards, James Mallet, W Owen McMillan, Chris D Jiggins, Heliconius Genome Consortium

Nature 487 (7405), 94

2011

Wing patterning gene redefines the mimetic history of Heliconius butterflies

Heather M Hines, Brian A Counterman, Riccardo Papa, Priscila Albuquerque De Moura, Marcio Z Cardoso, Mauricio Linares, James Mallet, Robert D Reed, Chris D Jiggins, Marcus R Kronforst, W Owen McMillan

Proceedings of the National Academy of Sciences 108 (49), 19666-19671

Optix drives the repeated convergent evolution of butterfly wing pattern mimicry

Robert D Reed, Riccardo Papa, Arnaud Martin, Heather M Hines, Brian A Counterman, Carolina Pardo-Diaz, Chris D Jiggins, Nicola L Chamberlain, Marcus R Kronforst, Rui Chen, Georg Halder, H Frederik Nijhout, W Owen McMillan

Science 333 (6046), 1137-1141

Albuquerque de Moura P, Cardoso MZ, Linares M, et al. Wing patterning gene redefines the mimetic history of Heliconius butterflies

HM Hines, BA Counterman, R Papa

Proc Natl Acad Sci 108 (49), 19666-19671

2010

Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in Heliconius erato

Brian A Counterman, Felix Araujo-Perez, Heather M Hines, Simon W Baxter, Clay M Morrison, Daniel P Lindstrom, Riccardo Papa, Laura Ferguson, Mathieu Joron, Christopher P Smith, Dahlia M Nielsen, Rui Chen, Chris D Jiggins, Robert D Reed, Georg Halder, Jim Mallet, W Owen McMillan

PLoS Genet 6 (2), e1000796

2008

Genomic hotspots of adaptation in butterfly wing pattern evolution

Riccardo Papa, Arnaud Martin, Robert D Reed

Current opinion in genetics & development 18 (6), 559-564

Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies

Riccardo Papa, Clayton M Morrison, James R Walters, Brian A Counterman, Rui Chen, Georg Halder, Laura Ferguson, Nicola Chamberlain, Durrell D Kapan, Chris D Jiggins, Robert D Reed, William O McMillan

BMC genomics 9 (1), 345

Convergent evolution in the genetic basis of Müllerian mimicry in Heliconius butterflies

Simon W Baxter, Riccardo Papa, Nicola Chamberlain, Sean J Humphray, Mathieu Joron, Clay Morrison, W Owen McMillan, Chris D Jiggins

Genetics 180 (3), 1567-1577

Conserved but flexible: Genetic control of mimicry in Heliconius butterfly wing patterns

Mathieu Joron, Riccardo Papa, James Mallet, W Owen McMillan, Chris D Jiggins

JOURNAL OF INSECT SCIENCE 7

A conserved supergene locus controls colour pattern diversity in Heliconius butterflies

Mathieu Joron, Riccardo Papa, Margarita Beltrán, Nicola Chamberlain, Jesús Mavárez, Simon Baxter, Moisés Abanto, Eldredge Bermingham, Sean J Humphray, Jane Rogers, Helen Beasley, Karen Barlow, James Mallet, W Owen McMillan, Chris D Jiggins

PLoS Biol 4 (10), e303

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