Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain

The standard reference Caenorhabditis elegans strain, N2, has evolved marked behavioral changes in social feeding behavior since its isolation from the wild. We show that the causal, laboratory-derived mutations in two genes, npr-1 and glb-5, confer large fitness advantages in standard laboratory co...

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Main Authors: Yuehui Zhao, Lijiang Long, Wen Xu, Richard F Campbell, Edward E Large, Joshua S Greene, Patrick T McGrath
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/38675
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spelling doaj-e2419bf95fcc4a1abd409c499fa1aab32021-05-05T16:13:38ZengeLife Sciences Publications LtdeLife2050-084X2018-10-01710.7554/eLife.38675Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strainYuehui Zhao0https://orcid.org/0000-0002-9496-0023Lijiang Long1Wen Xu2https://orcid.org/0000-0003-2085-7223Richard F Campbell3Edward E Large4Joshua S Greene5Patrick T McGrath6https://orcid.org/0000-0002-1598-3746Department of Biological Sciences, Georgia Institute of Technology, Atlanta, United StatesDepartment of Biological Sciences, Georgia Institute of Technology, Atlanta, United StatesDepartment of Biological Sciences, Georgia Institute of Technology, Atlanta, United StatesDepartment of Biological Sciences, Georgia Institute of Technology, Atlanta, United StatesDepartment of Biological Sciences, Georgia Institute of Technology, Atlanta, United StatesThe Rockefeller University, New York, United StatesDepartment of Biological Sciences, Georgia Institute of Technology, Atlanta, United States; Department of Physics, Georgia Institute of Technology, Atlanta, United States; Institute of Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, United StatesThe standard reference Caenorhabditis elegans strain, N2, has evolved marked behavioral changes in social feeding behavior since its isolation from the wild. We show that the causal, laboratory-derived mutations in two genes, npr-1 and glb-5, confer large fitness advantages in standard laboratory conditions. Using environmental manipulations that suppress social/solitary behavior differences, we show the fitness advantages of the derived alleles remained unchanged, suggesting selection on these alleles acted through pleiotropic traits. Transcriptomics, developmental timing, and food consumption assays showed that N2 animals mature faster, produce more sperm, and consume more food than a strain containing ancestral alleles of these genes regardless of behavioral strategies. Our data suggest that the pleiotropic effects of glb-5 and npr-1 are a consequence of changes to O2 -sensing neurons that regulate both aerotaxis and energy homeostasis. Our results demonstrate how pleiotropy can lead to profound behavioral changes in a popular laboratory model.https://elifesciences.org/articles/38675laboratory adaptationfeedingsocial behaviorpleiotropyoxygen sensationpheromones
collection DOAJ
language English
format Article
sources DOAJ
author Yuehui Zhao
Lijiang Long
Wen Xu
Richard F Campbell
Edward E Large
Joshua S Greene
Patrick T McGrath
spellingShingle Yuehui Zhao
Lijiang Long
Wen Xu
Richard F Campbell
Edward E Large
Joshua S Greene
Patrick T McGrath
Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain
eLife
laboratory adaptation
feeding
social behavior
pleiotropy
oxygen sensation
pheromones
author_facet Yuehui Zhao
Lijiang Long
Wen Xu
Richard F Campbell
Edward E Large
Joshua S Greene
Patrick T McGrath
author_sort Yuehui Zhao
title Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain
title_short Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain
title_full Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain
title_fullStr Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain
title_full_unstemmed Changes to social feeding behaviors are not sufficient for fitness gains of the Caenorhabditis elegans N2 reference strain
title_sort changes to social feeding behaviors are not sufficient for fitness gains of the caenorhabditis elegans n2 reference strain
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2018-10-01
description The standard reference Caenorhabditis elegans strain, N2, has evolved marked behavioral changes in social feeding behavior since its isolation from the wild. We show that the causal, laboratory-derived mutations in two genes, npr-1 and glb-5, confer large fitness advantages in standard laboratory conditions. Using environmental manipulations that suppress social/solitary behavior differences, we show the fitness advantages of the derived alleles remained unchanged, suggesting selection on these alleles acted through pleiotropic traits. Transcriptomics, developmental timing, and food consumption assays showed that N2 animals mature faster, produce more sperm, and consume more food than a strain containing ancestral alleles of these genes regardless of behavioral strategies. Our data suggest that the pleiotropic effects of glb-5 and npr-1 are a consequence of changes to O2 -sensing neurons that regulate both aerotaxis and energy homeostasis. Our results demonstrate how pleiotropy can lead to profound behavioral changes in a popular laboratory model.
topic laboratory adaptation
feeding
social behavior
pleiotropy
oxygen sensation
pheromones
url https://elifesciences.org/articles/38675
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