Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant Analysis

Behavior is frequently predicted to be especially important for evolution in novel environments. If these predictions are accurate, there might be particular patterns of genetic architecture associated with recently diverged behaviors. Specifically, it has been predicted that behaviors linked to pop...

Full description

Bibliographic Details
Main Authors: Kyle M. Benowitz, Joshua M. Coleman, Luciano M. Matzkin
Format: Article
Language:English
Published: Oxford University Press 2019-05-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.119.400036
id doaj-3801614ed9dc46c79da1e954366b9072
record_format Article
spelling doaj-3801614ed9dc46c79da1e954366b90722021-07-02T08:27:59ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362019-05-01951767177510.1534/g3.119.40003643Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant AnalysisKyle M. BenowitzJoshua M. ColemanLuciano M. MatzkinBehavior is frequently predicted to be especially important for evolution in novel environments. If these predictions are accurate, there might be particular patterns of genetic architecture associated with recently diverged behaviors. Specifically, it has been predicted that behaviors linked to population divergence should be underpinned by a few genes of relatively large effect, compared to architectures of intrapopulation behavioral variation, which is considered to be highly polygenic. More mapping studies of behavioral variation between recently diverged populations are needed to continue assessing the generality of these predictions. Here, we used a bulk segregant mapping approach to dissect the genetic architecture of a locomotor trait that has evolved between two populations of the cactophilic fly Drosophila mojavensis. We created an F8 mapping population of 1,500 individuals from advanced intercross lines and sequenced the 10% of individuals with the highest and lowest levels of locomotor activity. Using three alternative statistical approaches, we found strong evidence for two relatively large-effect QTL that is localized in a region homologous to a region of densely packed behavior loci in Drosophila melanogaster, suggesting that clustering of behavior genes may display relatively deep evolutionary conservation. Broadly, our data are most consistent with a polygenic architecture, though with several loci explaining a high proportion of variation in comparison to similar behavioral traits. We further note the presence of several antagonistic QTL linked to locomotion and discuss these results in light of theories regarding behavioral evolution and the effect size and direction of QTL for diverging traits in general.http://g3journal.org/lookup/doi/10.1534/g3.119.400036advanced intercross linesbehaviorcactophilicgenetic mappinglarval activity
collection DOAJ
language English
format Article
sources DOAJ
author Kyle M. Benowitz
Joshua M. Coleman
Luciano M. Matzkin
spellingShingle Kyle M. Benowitz
Joshua M. Coleman
Luciano M. Matzkin
Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant Analysis
G3: Genes, Genomes, Genetics
advanced intercross lines
behavior
cactophilic
genetic mapping
larval activity
author_facet Kyle M. Benowitz
Joshua M. Coleman
Luciano M. Matzkin
author_sort Kyle M. Benowitz
title Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant Analysis
title_short Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant Analysis
title_full Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant Analysis
title_fullStr Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant Analysis
title_full_unstemmed Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant Analysis
title_sort assessing the architecture of drosophila mojavensis locomotor evolution with bulk segregant analysis
publisher Oxford University Press
series G3: Genes, Genomes, Genetics
issn 2160-1836
publishDate 2019-05-01
description Behavior is frequently predicted to be especially important for evolution in novel environments. If these predictions are accurate, there might be particular patterns of genetic architecture associated with recently diverged behaviors. Specifically, it has been predicted that behaviors linked to population divergence should be underpinned by a few genes of relatively large effect, compared to architectures of intrapopulation behavioral variation, which is considered to be highly polygenic. More mapping studies of behavioral variation between recently diverged populations are needed to continue assessing the generality of these predictions. Here, we used a bulk segregant mapping approach to dissect the genetic architecture of a locomotor trait that has evolved between two populations of the cactophilic fly Drosophila mojavensis. We created an F8 mapping population of 1,500 individuals from advanced intercross lines and sequenced the 10% of individuals with the highest and lowest levels of locomotor activity. Using three alternative statistical approaches, we found strong evidence for two relatively large-effect QTL that is localized in a region homologous to a region of densely packed behavior loci in Drosophila melanogaster, suggesting that clustering of behavior genes may display relatively deep evolutionary conservation. Broadly, our data are most consistent with a polygenic architecture, though with several loci explaining a high proportion of variation in comparison to similar behavioral traits. We further note the presence of several antagonistic QTL linked to locomotion and discuss these results in light of theories regarding behavioral evolution and the effect size and direction of QTL for diverging traits in general.
topic advanced intercross lines
behavior
cactophilic
genetic mapping
larval activity
url http://g3journal.org/lookup/doi/10.1534/g3.119.400036
work_keys_str_mv AT kylembenowitz assessingthearchitectureofdrosophilamojavensislocomotorevolutionwithbulksegregantanalysis
AT joshuamcoleman assessingthearchitectureofdrosophilamojavensislocomotorevolutionwithbulksegregantanalysis
AT lucianommatzkin assessingthearchitectureofdrosophilamojavensislocomotorevolutionwithbulksegregantanalysis
_version_ 1721334719301287936