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

Abstract 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 h...

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Autores principales: Daniel F. Paulo, Ana C. M. Junqueira, Alex P. Arp, André S. Vieira, Jorge Ceballos, Steven R. Skoda, Adalberto A. Pérez-de-León, Agustin Sagel, William O. McMillan, Maxwell J. Scott, Carolina Concha, Ana M. L. Azeredo-Espin
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Publicado: Nature Portfolio 2021
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spelling oai:doaj.org-article:4cab3329ded84116a188b64ebe75a9ed2021-12-02T17:50:41ZDisruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly10.1038/s41598-021-90649-x2045-2322https://doaj.org/article/4cab3329ded84116a188b64ebe75a9ed2021-05-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-90649-xhttps://doaj.org/toc/2045-2322Abstract 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.Daniel F. PauloAna C. M. JunqueiraAlex P. ArpAndré S. VieiraJorge CeballosSteven R. SkodaAdalberto A. Pérez-de-LeónAgustin SagelWilliam O. McMillanMaxwell J. ScottCarolina ConchaAna M. L. Azeredo-EspinNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-13 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Daniel F. Paulo
Ana C. M. Junqueira
Alex P. Arp
André S. Vieira
Jorge Ceballos
Steven R. Skoda
Adalberto A. Pérez-de-León
Agustin Sagel
William O. McMillan
Maxwell J. Scott
Carolina Concha
Ana M. L. Azeredo-Espin
Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly
description Abstract 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.
format article
author Daniel F. Paulo
Ana C. M. Junqueira
Alex P. Arp
André S. Vieira
Jorge Ceballos
Steven R. Skoda
Adalberto A. Pérez-de-León
Agustin Sagel
William O. McMillan
Maxwell J. Scott
Carolina Concha
Ana M. L. Azeredo-Espin
author_facet Daniel F. Paulo
Ana C. M. Junqueira
Alex P. Arp
André S. Vieira
Jorge Ceballos
Steven R. Skoda
Adalberto A. Pérez-de-León
Agustin Sagel
William O. McMillan
Maxwell J. Scott
Carolina Concha
Ana M. L. Azeredo-Espin
author_sort Daniel F. Paulo
title 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_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_sort disruption of the odorant coreceptor orco impairs foraging and host finding behaviors in the new world screwworm fly
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/4cab3329ded84116a188b64ebe75a9ed
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