Natural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila.
The winged insects of the order Diptera are colloquially named for their most recognizable phenotype: flight. These insects rely on flight for a number of important life history traits, such as dispersal, foraging, and courtship. Despite the importance of flight, relatively little is known about the...
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oai:doaj.org-article:4295191819b24473bf872086bdb9c2752021-12-02T20:02:58ZNatural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila.1553-73901553-740410.1371/journal.pgen.1008887https://doaj.org/article/4295191819b24473bf872086bdb9c2752021-03-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1008887https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404The winged insects of the order Diptera are colloquially named for their most recognizable phenotype: flight. These insects rely on flight for a number of important life history traits, such as dispersal, foraging, and courtship. Despite the importance of flight, relatively little is known about the genetic architecture of flight performance. Accordingly, we sought to uncover the genetic modifiers of flight using a measure of flies' reaction and response to an abrupt drop in a vertical flight column. We conducted a genome wide association study (GWAS) using 197 of the Drosophila Genetic Reference Panel (DGRP) lines, and identified a combination of additive and marginal variants, epistatic interactions, whole genes, and enrichment across interaction networks. Egfr, a highly pleiotropic developmental gene, was among the most significant additive variants identified. We functionally validated 13 of the additive candidate genes' (Adgf-A/Adgf-A2/CG32181, bru1, CadN, flapper (CG11073), CG15236, flippy (CG9766), CREG, Dscam4, form3, fry, Lasp/CG9692, Pde6, Snoo), and introduce a novel approach to whole gene significance screens: PEGASUS_flies. Additionally, we identified ppk23, an Acid Sensing Ion Channel (ASIC) homolog, as an important hub for epistatic interactions. We propose a model that suggests genetic modifiers of wing and muscle morphology, nervous system development and function, BMP signaling, sexually dimorphic neural wiring, and gene regulation are all important for the observed differences flight performance in a natural population. Additionally, these results represent a snapshot of the genetic modifiers affecting drop-response flight performance in Drosophila, with implications for other insects.Adam N SpiererJim A MossmanSamuel Pattillo SmithLorin CrawfordSohini RamachandranDavid M RandPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 3, p e1008887 (2021) |
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Genetics QH426-470 |
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Genetics QH426-470 Adam N Spierer Jim A Mossman Samuel Pattillo Smith Lorin Crawford Sohini Ramachandran David M Rand Natural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila. |
description |
The winged insects of the order Diptera are colloquially named for their most recognizable phenotype: flight. These insects rely on flight for a number of important life history traits, such as dispersal, foraging, and courtship. Despite the importance of flight, relatively little is known about the genetic architecture of flight performance. Accordingly, we sought to uncover the genetic modifiers of flight using a measure of flies' reaction and response to an abrupt drop in a vertical flight column. We conducted a genome wide association study (GWAS) using 197 of the Drosophila Genetic Reference Panel (DGRP) lines, and identified a combination of additive and marginal variants, epistatic interactions, whole genes, and enrichment across interaction networks. Egfr, a highly pleiotropic developmental gene, was among the most significant additive variants identified. We functionally validated 13 of the additive candidate genes' (Adgf-A/Adgf-A2/CG32181, bru1, CadN, flapper (CG11073), CG15236, flippy (CG9766), CREG, Dscam4, form3, fry, Lasp/CG9692, Pde6, Snoo), and introduce a novel approach to whole gene significance screens: PEGASUS_flies. Additionally, we identified ppk23, an Acid Sensing Ion Channel (ASIC) homolog, as an important hub for epistatic interactions. We propose a model that suggests genetic modifiers of wing and muscle morphology, nervous system development and function, BMP signaling, sexually dimorphic neural wiring, and gene regulation are all important for the observed differences flight performance in a natural population. Additionally, these results represent a snapshot of the genetic modifiers affecting drop-response flight performance in Drosophila, with implications for other insects. |
format |
article |
author |
Adam N Spierer Jim A Mossman Samuel Pattillo Smith Lorin Crawford Sohini Ramachandran David M Rand |
author_facet |
Adam N Spierer Jim A Mossman Samuel Pattillo Smith Lorin Crawford Sohini Ramachandran David M Rand |
author_sort |
Adam N Spierer |
title |
Natural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila. |
title_short |
Natural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila. |
title_full |
Natural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila. |
title_fullStr |
Natural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila. |
title_full_unstemmed |
Natural variation in the regulation of neurodevelopmental genes modifies flight performance in Drosophila. |
title_sort |
natural variation in the regulation of neurodevelopmental genes modifies flight performance in drosophila. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2021 |
url |
https://doaj.org/article/4295191819b24473bf872086bdb9c275 |
work_keys_str_mv |
AT adamnspierer naturalvariationintheregulationofneurodevelopmentalgenesmodifiesflightperformanceindrosophila AT jimamossman naturalvariationintheregulationofneurodevelopmentalgenesmodifiesflightperformanceindrosophila AT samuelpattillosmith naturalvariationintheregulationofneurodevelopmentalgenesmodifiesflightperformanceindrosophila AT lorincrawford naturalvariationintheregulationofneurodevelopmentalgenesmodifiesflightperformanceindrosophila AT sohiniramachandran naturalvariationintheregulationofneurodevelopmentalgenesmodifiesflightperformanceindrosophila AT davidmrand naturalvariationintheregulationofneurodevelopmentalgenesmodifiesflightperformanceindrosophila |
_version_ |
1718375655158054912 |