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.
Complex modular architecture around a simple toolkit of wing pattern genes
-Nature Ecology & Evolution
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
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
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
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