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Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation

Neotropical Heliconius butterflies are well known for their intricate behaviors and multiple instances of incipient speciation. Chemosensing plays a fundamental role in the life history of these groups of butterflies and in the establishment of reproductive isolation. However, chemical communication...

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Autores principales: Wu, Ningning, Evans, Elizabeth, van Schooten, Bas, Meléndez-Rosa, Jesyka, Ortiz, Yadira, Planas Soto-Navarro, Silvia M, Van Belleghem, Steven M, Counterman, Brian A, Papa, Riccardo, Zhang, Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9641979/
https://www.ncbi.nlm.nih.gov/pubmed/36251882
http://dx.doi.org/10.1093/molbev/msac225
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author Wu, Ningning
Evans, Elizabeth
van Schooten, Bas
Meléndez-Rosa, Jesyka
Ortiz, Yadira
Planas Soto-Navarro, Silvia M
Van Belleghem, Steven M
Counterman, Brian A
Papa, Riccardo
Zhang, Wei
author_facet Wu, Ningning
Evans, Elizabeth
van Schooten, Bas
Meléndez-Rosa, Jesyka
Ortiz, Yadira
Planas Soto-Navarro, Silvia M
Van Belleghem, Steven M
Counterman, Brian A
Papa, Riccardo
Zhang, Wei
author_sort Wu, Ningning
collection PubMed
description Neotropical Heliconius butterflies are well known for their intricate behaviors and multiple instances of incipient speciation. Chemosensing plays a fundamental role in the life history of these groups of butterflies and in the establishment of reproductive isolation. However, chemical communication involves synergistic sensory and accessory functions, and it remains challenging to investigate the molecular mechanisms underlying behavioral differences. Here, we examine the gene expression profiles and genomic divergence of three sensory tissues (antennae, legs, and mouthparts) between sexes (females and males) and life stages (different adult stages) in two hybridizing butterflies, Heliconius melpomene and Heliconius cydno. By integrating comparative transcriptomic and population genomic approaches, we found evidence of widespread gene expression divergence, supporting a crucial role of sensory tissues in the establishment of species barriers. We also show that sensory diversification increases in a manner consistent with evolutionary divergence based on comparison with the more distantly related species Heliconius charithonia. The findings of our study strongly support the unique chemosensory function of antennae in all three species, the importance of the Z chromosome in interspecific divergence, and the nonnegligible role of nonchemosensory genes in the divergence of chemosensory tissues. Collectively, our results provide a genome-wide illustration of diversification in the chemosensory system under incomplete reproductive isolation, revealing strong molecular separation in the early stage of speciation. Here, we provide a unique perspective and relevant view of the genetic architecture (sensory and accessory functions) of chemosensing beyond the classic chemosensory gene families, leading to a better understanding of the magnitude and complexity of molecular changes in sensory tissues that contribute to the establishment of reproductive isolation and speciation.
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spelling pubmed-96419792022-11-14 Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation Wu, Ningning Evans, Elizabeth van Schooten, Bas Meléndez-Rosa, Jesyka Ortiz, Yadira Planas Soto-Navarro, Silvia M Van Belleghem, Steven M Counterman, Brian A Papa, Riccardo Zhang, Wei Mol Biol Evol Discoveries Neotropical Heliconius butterflies are well known for their intricate behaviors and multiple instances of incipient speciation. Chemosensing plays a fundamental role in the life history of these groups of butterflies and in the establishment of reproductive isolation. However, chemical communication involves synergistic sensory and accessory functions, and it remains challenging to investigate the molecular mechanisms underlying behavioral differences. Here, we examine the gene expression profiles and genomic divergence of three sensory tissues (antennae, legs, and mouthparts) between sexes (females and males) and life stages (different adult stages) in two hybridizing butterflies, Heliconius melpomene and Heliconius cydno. By integrating comparative transcriptomic and population genomic approaches, we found evidence of widespread gene expression divergence, supporting a crucial role of sensory tissues in the establishment of species barriers. We also show that sensory diversification increases in a manner consistent with evolutionary divergence based on comparison with the more distantly related species Heliconius charithonia. The findings of our study strongly support the unique chemosensory function of antennae in all three species, the importance of the Z chromosome in interspecific divergence, and the nonnegligible role of nonchemosensory genes in the divergence of chemosensory tissues. Collectively, our results provide a genome-wide illustration of diversification in the chemosensory system under incomplete reproductive isolation, revealing strong molecular separation in the early stage of speciation. Here, we provide a unique perspective and relevant view of the genetic architecture (sensory and accessory functions) of chemosensing beyond the classic chemosensory gene families, leading to a better understanding of the magnitude and complexity of molecular changes in sensory tissues that contribute to the establishment of reproductive isolation and speciation. Oxford University Press 2022-10-17 /pmc/articles/PMC9641979/ /pubmed/36251882 http://dx.doi.org/10.1093/molbev/msac225 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Wu, Ningning
Evans, Elizabeth
van Schooten, Bas
Meléndez-Rosa, Jesyka
Ortiz, Yadira
Planas Soto-Navarro, Silvia M
Van Belleghem, Steven M
Counterman, Brian A
Papa, Riccardo
Zhang, Wei
Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation
title Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation
title_full Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation
title_fullStr Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation
title_full_unstemmed Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation
title_short Widespread Gene Expression Divergence in Butterfly Sensory Tissues Plays a Fundamental Role During Reproductive Isolation and Speciation
title_sort widespread gene expression divergence in butterfly sensory tissues plays a fundamental role during reproductive isolation and speciation
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9641979/
https://www.ncbi.nlm.nih.gov/pubmed/36251882
http://dx.doi.org/10.1093/molbev/msac225
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