Positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic Drosophila

Abstract Background Adaptation to new hosts in phytophagous insects often involves mechanisms of host recognition by genes of sensory pathways. Most often the molecular evolution of sensory genes has been explained in the context of the birth-and-death model. The role of positive selection is less u...

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Main Authors: Fernando Diaz, Carson W. Allan, Luciano M. Matzkin
Format: Article
Language:English
Published: BMC 2018-09-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-018-1250-x
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spelling doaj-b9894f48d3a04ba3a4284719ff99046e2021-09-02T09:14:27ZengBMCBMC Evolutionary Biology1471-21482018-09-0118111310.1186/s12862-018-1250-xPositive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic DrosophilaFernando Diaz0Carson W. Allan1Luciano M. Matzkin2Department of Entomology, University of ArizonaDepartment of Entomology, University of ArizonaDepartment of Entomology, University of ArizonaAbstract Background Adaptation to new hosts in phytophagous insects often involves mechanisms of host recognition by genes of sensory pathways. Most often the molecular evolution of sensory genes has been explained in the context of the birth-and-death model. The role of positive selection is less understood, especially associated with host adaptation and specialization. Here we aim to contribute evidence for this latter hypothesis by considering the case of Drosophila mojavensis, a species with an evolutionary history shaped by multiple host shifts in a relatively short time scale, and its generalist sister species, D. arizonae. Results We used a phylogenetic and population genetic analysis framework to test for positive selection in a subset of four chemoreceptor genes, one gustatory receptor (Gr) and three odorant receptors (Or), for which their expression has been previously associated with host shifts. We found strong evidence of positive selection at several amino acid sites in all genes investigated, most of which exhibited changes predicted to cause functional effects in these transmembrane proteins. A significant portion of the sites identified as evolving positively were largely found in the cytoplasmic region, although a few were also present in the extracellular domains. Conclusions The pattern of substitution observed suggests that some of these changes likely had an effect on signal transduction as well as odorant recognition and protein-protein interactions. These findings support the role of positive selection in shaping the pattern of variation at chemosensory receptors, both during the specialization onto one or a few related hosts, but as well as during the evolution and adaptation of generalist species into utilizing several hosts.http://link.springer.com/article/10.1186/s12862-018-1250-xOdorant receptorGustatory receptorPopulation geneticsMolecular evolutionAdaptationCactophilic Drosophila
collection DOAJ
language English
format Article
sources DOAJ
author Fernando Diaz
Carson W. Allan
Luciano M. Matzkin
spellingShingle Fernando Diaz
Carson W. Allan
Luciano M. Matzkin
Positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic Drosophila
BMC Evolutionary Biology
Odorant receptor
Gustatory receptor
Population genetics
Molecular evolution
Adaptation
Cactophilic Drosophila
author_facet Fernando Diaz
Carson W. Allan
Luciano M. Matzkin
author_sort Fernando Diaz
title Positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic Drosophila
title_short Positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic Drosophila
title_full Positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic Drosophila
title_fullStr Positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic Drosophila
title_full_unstemmed Positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic Drosophila
title_sort positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic drosophila
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2018-09-01
description Abstract Background Adaptation to new hosts in phytophagous insects often involves mechanisms of host recognition by genes of sensory pathways. Most often the molecular evolution of sensory genes has been explained in the context of the birth-and-death model. The role of positive selection is less understood, especially associated with host adaptation and specialization. Here we aim to contribute evidence for this latter hypothesis by considering the case of Drosophila mojavensis, a species with an evolutionary history shaped by multiple host shifts in a relatively short time scale, and its generalist sister species, D. arizonae. Results We used a phylogenetic and population genetic analysis framework to test for positive selection in a subset of four chemoreceptor genes, one gustatory receptor (Gr) and three odorant receptors (Or), for which their expression has been previously associated with host shifts. We found strong evidence of positive selection at several amino acid sites in all genes investigated, most of which exhibited changes predicted to cause functional effects in these transmembrane proteins. A significant portion of the sites identified as evolving positively were largely found in the cytoplasmic region, although a few were also present in the extracellular domains. Conclusions The pattern of substitution observed suggests that some of these changes likely had an effect on signal transduction as well as odorant recognition and protein-protein interactions. These findings support the role of positive selection in shaping the pattern of variation at chemosensory receptors, both during the specialization onto one or a few related hosts, but as well as during the evolution and adaptation of generalist species into utilizing several hosts.
topic Odorant receptor
Gustatory receptor
Population genetics
Molecular evolution
Adaptation
Cactophilic Drosophila
url http://link.springer.com/article/10.1186/s12862-018-1250-x
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