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Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly

The evolution of obligate ectoparasitism in blowflies (Diptera: Calliphoridae) has intrigued scientists for over a century, and surprisingly, the genetics underlying this lifestyle remain largely unknown. Blowflies use odors to locate food and oviposition sites; therefore, olfaction might have playe...

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Autores principales: Paulo, Daniel F., Junqueira, Ana C. M., Arp, Alex P., Vieira, André S., Ceballos, Jorge, Skoda, Steven R., Pérez-de-León, Adalberto A., Sagel, Agustin, McMillan, William O., Scott, Maxwell J., Concha, Carolina, Azeredo-Espin, Ana M. L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8167109/
https://www.ncbi.nlm.nih.gov/pubmed/34059738
http://dx.doi.org/10.1038/s41598-021-90649-x
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author Paulo, Daniel F.
Junqueira, Ana C. M.
Arp, Alex P.
Vieira, André S.
Ceballos, Jorge
Skoda, Steven R.
Pérez-de-León, Adalberto A.
Sagel, Agustin
McMillan, William O.
Scott, Maxwell J.
Concha, Carolina
Azeredo-Espin, Ana M. L.
author_facet Paulo, Daniel F.
Junqueira, Ana C. M.
Arp, Alex P.
Vieira, André S.
Ceballos, Jorge
Skoda, Steven R.
Pérez-de-León, Adalberto A.
Sagel, Agustin
McMillan, William O.
Scott, Maxwell J.
Concha, Carolina
Azeredo-Espin, Ana M. L.
author_sort Paulo, Daniel F.
collection PubMed
description The evolution of obligate ectoparasitism in blowflies (Diptera: Calliphoridae) has intrigued scientists for over a century, and surprisingly, the genetics underlying this lifestyle remain largely unknown. Blowflies use odors to locate food and oviposition sites; therefore, olfaction might have played a central role in niche specialization within the group. In insects, the coreceptor Orco is a required partner for all odorant receptors (ORs), a major gene family involved in olfactory-evoked behaviors. Hence, we characterized the Orco gene in the New World screwworm, Cochliomyia hominivorax, a blowfly that is an obligate ectoparasite of warm-blooded animals. In contrast, most of the closely related blowflies are scavengers that lay their eggs on dead animals. We show that the screwworm Orco orthologue (ChomOrco) is highly conserved within Diptera, showing signals of strong purifying selection. Expression of ChomOrco is broadly detectable in chemosensory appendages, and is related to morphological, developmental, and behavioral aspects of the screwworm biology. We used CRISPR/Cas9 to disrupt ChomOrco and evaluate the consequences of losing the OR function on screwworm behavior. In two-choice assays, Orco mutants displayed an impaired response to floral-like and animal host-associated odors, suggesting that OR-mediated olfaction is involved in foraging and host-seeking behaviors in C. hominivorax. These results broaden our understanding of the chemoreception basis of niche occupancy by blowflies.
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spelling pubmed-81671092021-06-02 Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly Paulo, Daniel F. Junqueira, Ana C. M. Arp, Alex P. Vieira, André S. Ceballos, Jorge Skoda, Steven R. Pérez-de-León, Adalberto A. Sagel, Agustin McMillan, William O. Scott, Maxwell J. Concha, Carolina Azeredo-Espin, Ana M. L. Sci Rep Article The evolution of obligate ectoparasitism in blowflies (Diptera: Calliphoridae) has intrigued scientists for over a century, and surprisingly, the genetics underlying this lifestyle remain largely unknown. Blowflies use odors to locate food and oviposition sites; therefore, olfaction might have played a central role in niche specialization within the group. In insects, the coreceptor Orco is a required partner for all odorant receptors (ORs), a major gene family involved in olfactory-evoked behaviors. Hence, we characterized the Orco gene in the New World screwworm, Cochliomyia hominivorax, a blowfly that is an obligate ectoparasite of warm-blooded animals. In contrast, most of the closely related blowflies are scavengers that lay their eggs on dead animals. We show that the screwworm Orco orthologue (ChomOrco) is highly conserved within Diptera, showing signals of strong purifying selection. Expression of ChomOrco is broadly detectable in chemosensory appendages, and is related to morphological, developmental, and behavioral aspects of the screwworm biology. We used CRISPR/Cas9 to disrupt ChomOrco and evaluate the consequences of losing the OR function on screwworm behavior. In two-choice assays, Orco mutants displayed an impaired response to floral-like and animal host-associated odors, suggesting that OR-mediated olfaction is involved in foraging and host-seeking behaviors in C. hominivorax. These results broaden our understanding of the chemoreception basis of niche occupancy by blowflies. Nature Publishing Group UK 2021-05-31 /pmc/articles/PMC8167109/ /pubmed/34059738 http://dx.doi.org/10.1038/s41598-021-90649-x Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Paulo, Daniel F.
Junqueira, Ana C. M.
Arp, Alex P.
Vieira, André S.
Ceballos, Jorge
Skoda, Steven R.
Pérez-de-León, Adalberto A.
Sagel, Agustin
McMillan, William O.
Scott, Maxwell J.
Concha, Carolina
Azeredo-Espin, Ana M. L.
Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly
title Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly
title_full Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly
title_fullStr Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly
title_full_unstemmed Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly
title_short Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly
title_sort disruption of the odorant coreceptor orco impairs foraging and host finding behaviors in the new world screwworm fly
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8167109/
https://www.ncbi.nlm.nih.gov/pubmed/34059738
http://dx.doi.org/10.1038/s41598-021-90649-x
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