Genomics of Neotropical biodiversity indicators: Two butterfly radiations with rampant chromosomal rearrangements and hybridization

Eva S M van der Heijden; Karin Näsvall; Fernando A Seixas; Carlos Eduardo Beserra Nobre; Artur Campos D Maia; Patricio Salazar-Carrión; Jonah M Walker; Daiane Szczerbowski; Stefan Schulz; Ian A Warren; Kimberly Gabriela Gavilanes Córdova; María José Sánchez-Carvajal; Franz Chandi; Alex P Arias-Cruz; Nicol Rueda-M; Camilo Salazar; Kanchon K Dasmahapatra; Stephen H Montgomery; Melanie McClure; Dominic E Absolon; Thomas C Mathers; Camilla A Santos; Shane McCarthy; Jonathan M D Wood; Gerardo Lamas; Caroline Bacquet; André Victor Lucci Freitas; Keith R Willmott; Chris D Jiggins; Marianne Elias; Joana I Meier

Genomics of Neotropical biodiversity indicators: Two butterfly radiations with rampant chromosomal rearrangements and hybridization

Título traducido de la contribución: Genómica de los indicadores de biodiversidad neotropical: dos radiaciones de mariposas con abundantes reorganizaciones cromosómicas e hibridación.: Dos radiaciones de mariposas con abundantes reorganizaciones cromosómicas e hibridación.

Eva S M van der Heijden
, Karin Näsvall
, Fernando A Seixas
, Carlos Eduardo Beserra Nobre
, Artur Campos D Maia
, Patricio Salazar-Carrión
, Jonah M Walker
, Daiane Szczerbowski
, Stefan Schulz
, Ian A Warren
, Kimberly Gabriela Gavilanes Córdova
, María José Sánchez-Carvajal
, Franz Chandi
, Alex P Arias-Cruz
, Nicol Rueda-M
, Camilo Salazar
, Kanchon K Dasmahapatra
, Stephen H Montgomery
, Melanie McClure
, Dominic E Absolon

Thomas C Mathers, Camilla A Santos, Shane McCarthy, Jonathan M D Wood, Gerardo Lamas, Caroline Bacquet, André Victor Lucci Freitas, Keith R Willmott, Chris D Jiggins, Marianne Elias, Joana I Meier

Universidad del Rosario

Producción científica: Contribución a revista › Artículo de Investigación › revisión exhaustiva

5 Citas (Scopus)

Resumen

Una pregunta central en la biología evolutiva es qué impulsa la diversificación de los linajes. Las radiaciones rápidas y recientes son sistemas ideales para esta pregunta porque aún muestran adaptaciones morfológicas y ecológicas clave asociadas con la especiación. Mientras que la mayoría de la investigación sobre radiaciones recientes se enfoca en aquellas que ocurren en entornos insulares, se ha prestado menos atención a las radiaciones continentales con interacciones complejas entre especies.

Aquí estudiamos los impulsores de las radiaciones continentales de las mariposas Melinaea y Mechanitis (Nymphalidae: Ithomiini), que han experimentado una rápida radiación en los neotrópicos continentales. Son modelos clásicos para la biogeografía amazónica y el mimetismo de patrones de color, y han sido propuestos como indicadores de biodiversidad. Generamos genomas de referencia para cinco especies de cada género y datos de re-secuenciación del genoma completo de la mayoría de especies y subespecies que cubren un amplio rango geográfico, para evaluar relaciones filogeográficas, patrones de hibridación y reorganizaciones cromosómicas.

Nuestros datos ayudan a resolver la clasificación de estas mariposas taxonómicamente complejas y revelan tasas de diversificación muy altas. Encontramos evidencia abundante de hibridación histórica y especies híbridas putativas en ambas radiaciones, lo que puede haber facilitado su rápida diversificación al enriquecer la diversidad genética. Además, identificamos decenas de fusiones y fisiones cromosómicas entre especies del mismo género que probablemente aceleraron el aislamiento reproductivo.

Concluimos que las interacciones entre geografía, hibridación y reorganizaciones cromosómicas han contribuido a estas rápidas radiaciones en la altamente diversa región neotropical. Hipotetizamos que las radiaciones rápidas pueden ser impulsadas si períodos repetidos de aislamiento geográfico se combinan con una acumulación rápida de incompatibilidades específicas del linaje, seguidos por contacto secundario con algún grado de intercambio genético.

Título traducido de la contribución	Genómica de los indicadores de biodiversidad neotropical: dos radiaciones de mariposas con abundantes reorganizaciones cromosómicas e hibridación.: Dos radiaciones de mariposas con abundantes reorganizaciones cromosómicas e hibridación.
Idioma original	Inglés estadounidense
Número de artículo	e2410939122
Páginas (desde-hasta)	e2410939122
Publicación	Proceedings of the National Academy of Sciences of the United States of America
Volumen	122
N.º	31
Estado	Publicada - jul. 28 2025

ODS de las Naciones Unidas

Este resultado contribuye a los siguientes Objetivos de Desarrollo Sostenible

ODS 15: Vida de ecosistemas terrestres

Áreas temáticas de ASJC Scopus

Ecología, evolución, comportamiento y sistemática

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Citar esto

van der Heijden, E. S. M., Näsvall, K., Seixas, F. A., Beserra Nobre, C. E., Maia, A. C. D., Salazar-Carrión, P., Walker, J. M., Szczerbowski, D., Schulz, S., Warren, I. A., Gavilanes Córdova, K. G., Sánchez-Carvajal, M. J., Chandi, F., Arias-Cruz, A. P., Rueda-M, N., Salazar, C., Dasmahapatra, K. K., Montgomery, S. H., McClure, M., ... Meier, J. I. (2025). Genomics of Neotropical biodiversity indicators: Two butterfly radiations with rampant chromosomal rearrangements and hybridization. Proceedings of the National Academy of Sciences of the United States of America, 122(31), e2410939122. Artículo e2410939122.

@article{f708327dae6e4a3591668103e129d028,

title = "Genomics of Neotropical biodiversity indicators: Two butterfly radiations with rampant chromosomal rearrangements and hybridization",

abstract = "A central question in evolutionary biology is what drives the diversification of lineages. Rapid, recent radiations are ideal systems for this question because they still show key morphological and ecological adaptations associated with speciation. While most research on recent radiations focuses on those occurring in insular environments, less attention has been given to continental radiations with complex species interactions. Here, we study the drivers of continental radiations of Melinaea and Mechanitis butterflies (Nymphalidae: Ithomiini), which have rapidly radiated in the continental Neotropics. They are classical models for Amazonian biogeography and color pattern mimicry and have been proposed as biodiversity indicators. We generated reference genomes for five species of each genus and whole-genome resequencing data of most species and subspecies covering a wide geographic range to assess phylogeographic relationships, hybridization patterns, and chromosomal rearrangements. Our data help resolve the classification of these taxonomically challenging butterflies and reveal very high diversification rates. We find rampant evidence of historical hybridization and putative hybrid species in both radiations, which may have facilitated their rapid diversification by enriching the genetic diversity. Moreover, we identified dozens of chromosomal fusions and fissions between congeneric species that have likely expedited reproductive isolation. We conclude that interactions between geography, hybridization and chromosomal rearrangements have contributed to these rapid radiations in the highly diverse Neotropical region. We hypothesize that rapid radiations may be spurred if repeated periods of geographic isolation are combined with lineage-specific rapid accumulation of incompatibilities, followed by secondary contact with some gene exchange.",

author = "\{van der Heijden\}, \{Eva S M\} and Karin N{\"a}svall and Seixas, \{Fernando A\} and \{Beserra Nobre\}, \{Carlos Eduardo\} and Maia, \{Artur Campos D\} and Patricio Salazar-Carri{\'o}n and Walker, \{Jonah M\} and Daiane Szczerbowski and Stefan Schulz and Warren, \{Ian A\} and \{Gavilanes C{\'o}rdova\}, \{Kimberly Gabriela\} and S{\'a}nchez-Carvajal, \{Mar{\'i}a Jos{\'e}\} and Franz Chandi and Arias-Cruz, \{Alex P\} and Nicol Rueda-M and Camilo Salazar and Dasmahapatra, \{Kanchon K\} and Montgomery, \{Stephen H\} and Melanie McClure and Absolon, \{Dominic E\} and Mathers, \{Thomas C\} and Santos, \{Camilla A\} and Shane McCarthy and Wood, \{Jonathan M D\} and Gerardo Lamas and Caroline Bacquet and Freitas, \{Andr{\'e} Victor Lucci\} and Willmott, \{Keith R\} and Jiggins, \{Chris D\} and Marianne Elias and Meier, \{Joana I\}",

note = "Publisher Copyright: Copyright {\textcopyright} 2025 the Author(s).",

year = "2025",

month = jul,

day = "28",

language = "English (US)",

volume = "122",

pages = "e2410939122",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

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van der Heijden, ESM, Näsvall, K, Seixas, FA, Beserra Nobre, CE, Maia, ACD, Salazar-Carrión, P, Walker, JM, Szczerbowski, D, Schulz, S, Warren, IA, Gavilanes Córdova, KG, Sánchez-Carvajal, MJ, Chandi, F, Arias-Cruz, AP, Rueda-M, N, Salazar, C, Dasmahapatra, KK, Montgomery, SH, McClure, M, Absolon, DE, Mathers, TC, Santos, CA, McCarthy, S, Wood, JMD, Lamas, G, Bacquet, C, Freitas, AVL, Willmott, KR, Jiggins, CD, Elias, M & Meier, JI 2025, 'Genomics of Neotropical biodiversity indicators: Two butterfly radiations with rampant chromosomal rearrangements and hybridization', Proceedings of the National Academy of Sciences of the United States of America, vol. 122, n.º 31, e2410939122, pp. e2410939122.

Genomics of Neotropical biodiversity indicators: Two butterfly radiations with rampant chromosomal rearrangements and hybridization. / van der Heijden, Eva S M; Näsvall, Karin; Seixas, Fernando A et al.
En: Proceedings of the National Academy of Sciences of the United States of America, Vol. 122, N.º 31, e2410939122, 28.07.2025, p. e2410939122.

Producción científica: Contribución a revista › Artículo de Investigación › revisión exhaustiva

TY - JOUR

T1 - Genomics of Neotropical biodiversity indicators

T2 - Two butterfly radiations with rampant chromosomal rearrangements and hybridization

AU - van der Heijden, Eva S M

AU - Näsvall, Karin

AU - Seixas, Fernando A

AU - Beserra Nobre, Carlos Eduardo

AU - Maia, Artur Campos D

AU - Salazar-Carrión, Patricio

AU - Walker, Jonah M

AU - Szczerbowski, Daiane

AU - Schulz, Stefan

AU - Warren, Ian A

AU - Gavilanes Córdova, Kimberly Gabriela

AU - Sánchez-Carvajal, María José

AU - Chandi, Franz

AU - Arias-Cruz, Alex P

AU - Rueda-M, Nicol

AU - Salazar, Camilo

AU - Dasmahapatra, Kanchon K

AU - Montgomery, Stephen H

AU - McClure, Melanie

AU - Absolon, Dominic E

AU - Mathers, Thomas C

AU - Santos, Camilla A

AU - McCarthy, Shane

AU - Wood, Jonathan M D

AU - Lamas, Gerardo

AU - Bacquet, Caroline

AU - Freitas, André Victor Lucci

AU - Willmott, Keith R

AU - Jiggins, Chris D

AU - Elias, Marianne

AU - Meier, Joana I

PY - 2025/7/28

Y1 - 2025/7/28

N2 - A central question in evolutionary biology is what drives the diversification of lineages. Rapid, recent radiations are ideal systems for this question because they still show key morphological and ecological adaptations associated with speciation. While most research on recent radiations focuses on those occurring in insular environments, less attention has been given to continental radiations with complex species interactions. Here, we study the drivers of continental radiations of Melinaea and Mechanitis butterflies (Nymphalidae: Ithomiini), which have rapidly radiated in the continental Neotropics. They are classical models for Amazonian biogeography and color pattern mimicry and have been proposed as biodiversity indicators. We generated reference genomes for five species of each genus and whole-genome resequencing data of most species and subspecies covering a wide geographic range to assess phylogeographic relationships, hybridization patterns, and chromosomal rearrangements. Our data help resolve the classification of these taxonomically challenging butterflies and reveal very high diversification rates. We find rampant evidence of historical hybridization and putative hybrid species in both radiations, which may have facilitated their rapid diversification by enriching the genetic diversity. Moreover, we identified dozens of chromosomal fusions and fissions between congeneric species that have likely expedited reproductive isolation. We conclude that interactions between geography, hybridization and chromosomal rearrangements have contributed to these rapid radiations in the highly diverse Neotropical region. We hypothesize that rapid radiations may be spurred if repeated periods of geographic isolation are combined with lineage-specific rapid accumulation of incompatibilities, followed by secondary contact with some gene exchange.

AB - A central question in evolutionary biology is what drives the diversification of lineages. Rapid, recent radiations are ideal systems for this question because they still show key morphological and ecological adaptations associated with speciation. While most research on recent radiations focuses on those occurring in insular environments, less attention has been given to continental radiations with complex species interactions. Here, we study the drivers of continental radiations of Melinaea and Mechanitis butterflies (Nymphalidae: Ithomiini), which have rapidly radiated in the continental Neotropics. They are classical models for Amazonian biogeography and color pattern mimicry and have been proposed as biodiversity indicators. We generated reference genomes for five species of each genus and whole-genome resequencing data of most species and subspecies covering a wide geographic range to assess phylogeographic relationships, hybridization patterns, and chromosomal rearrangements. Our data help resolve the classification of these taxonomically challenging butterflies and reveal very high diversification rates. We find rampant evidence of historical hybridization and putative hybrid species in both radiations, which may have facilitated their rapid diversification by enriching the genetic diversity. Moreover, we identified dozens of chromosomal fusions and fissions between congeneric species that have likely expedited reproductive isolation. We conclude that interactions between geography, hybridization and chromosomal rearrangements have contributed to these rapid radiations in the highly diverse Neotropical region. We hypothesize that rapid radiations may be spurred if repeated periods of geographic isolation are combined with lineage-specific rapid accumulation of incompatibilities, followed by secondary contact with some gene exchange.

UR - https://www.scopus.com/pages/publications/105012458300

UR - https://www.scopus.com/pages/publications/105012458300#tab=citedBy

M3 - Research Article

C2 - 40720651

SN - 0027-8424

VL - 122

SP - e2410939122

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 31

M1 - e2410939122

ER -