Rapid Evolution of Phenotypic Plasticity and Shifting Thresholds of Genetic Assimilation in the Nematode Caenorhabditis remanei
Abstract Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve. However, the rate and genetic basis of plasticity evolution remain largely unknown. We experimentally evolved outbred populations of the n...
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Published in | G3 : genes - genomes - genetics Vol. 4; no. 6; pp. 1103 - 1112 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
England
Oxford University Press
01.06.2014
Genetics Society of America |
Subjects | |
Online Access | Get full text |
ISSN | 2160-1836 2160-1836 |
DOI | 10.1534/g3.114.010553 |
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Abstract | Abstract
Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve. However, the rate and genetic basis of plasticity evolution remain largely unknown. We experimentally evolved outbred populations of the nematode Caenorhabditis remanei under an acute heat shock during early larval development. When raised in a nonstressful environment, ancestral populations were highly sensitive to a 36.8° heat shock and exhibited high mortality. However, initial exposure to a nonlethal high temperature environment resulted in significantly reduced mortality during heat shock (hormesis). Lines selected for heat shock resistance rapidly evolved the capacity to withstand heat shock in the native environment without any initial exposure to high temperatures, and early exposure to high temperatures did not lead to further increases in heat resistance. This loss of plasticity would appear to have resulted from the genetic assimilation of the heat induction response in the noninducing environment. However, analyses of transcriptional variation via RNA-sequencing from the selected populations revealed no global changes in gene regulation correlated with the observed changes in heat stress resistance. Instead, assays of the phenotypic response across a broader range of temperatures revealed that the induced plasticity was not fixed across environments, but rather the threshold for the response was shifted to higher temperatures over evolutionary time. These results demonstrate that apparent genetic assimilation can result from shifting thresholds of induction across environments and that analysis of the broader environmental context is critically important for understanding the evolution of phenotypic plasticity. |
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AbstractList | Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve. However, the rate and genetic basis of plasticity evolution remain largely unknown. We experimentally evolved outbred populations of the nematode Caenorhabditis remanei under an acute heat shock during early larval development. When raised in a nonstressful environment, ancestral populations were highly sensitive to a 36.8° heat shock and exhibited high mortality. However, initial exposure to a nonlethal high temperature environment resulted in significantly reduced mortality during heat shock (hormesis). Lines selected for heat shock resistance rapidly evolved the capacity to withstand heat shock in the native environment without any initial exposure to high temperatures, and early exposure to high temperatures did not lead to further increases in heat resistance. This loss of plasticity would appear to have resulted from the genetic assimilation of the heat induction response in the noninducing environment. However, analyses of transcriptional variation via RNA-sequencing from the selected populations revealed no global changes in gene regulation correlated with the observed changes in heat stress resistance. Instead, assays of the phenotypic response across a broader range of temperatures revealed that the induced plasticity was not fixed across environments, but rather the threshold for the response was shifted to higher temperatures over evolutionary time. These results demonstrate that apparent genetic assimilation can result from shifting thresholds of induction across environments and that analysis of the broader environmental context is critically important for understanding the evolution of phenotypic plasticity. Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve. However, the rate and genetic basis of plasticity evolution remain largely unknown. We experimentally evolved outbred populations of the nematode Caenorhabditis remanei under an acute heat shock during early larval development. When raised in a nonstressful environment, ancestral populations were highly sensitive to a 36.8° heat shock and exhibited high mortality. However, initial exposure to a nonlethal high temperature environment resulted in significantly reduced mortality during heat shock (hormesis). Lines selected for heat shock resistance rapidly evolved the capacity to withstand heat shock in the native environment without any initial exposure to high temperatures, and early exposure to high temperatures did not lead to further increases in heat resistance. This loss of plasticity would appear to have resulted from the genetic assimilation of the heat induction response in the noninducing environment. However, analyses of transcriptional variation via RNA-sequencing from the selected populations revealed no global changes in gene regulation correlated with the observed changes in heat stress resistance. Instead, assays of the phenotypic response across a broader range of temperatures revealed that the induced plasticity was not fixed across environments, but rather the threshold for the response was shifted to higher temperatures over evolutionary time. These results demonstrate that apparent genetic assimilation can result from shifting thresholds of induction across environments and that analysis of the broader environmental context is critically important for understanding the evolution of phenotypic plasticity.Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve. However, the rate and genetic basis of plasticity evolution remain largely unknown. We experimentally evolved outbred populations of the nematode Caenorhabditis remanei under an acute heat shock during early larval development. When raised in a nonstressful environment, ancestral populations were highly sensitive to a 36.8° heat shock and exhibited high mortality. However, initial exposure to a nonlethal high temperature environment resulted in significantly reduced mortality during heat shock (hormesis). Lines selected for heat shock resistance rapidly evolved the capacity to withstand heat shock in the native environment without any initial exposure to high temperatures, and early exposure to high temperatures did not lead to further increases in heat resistance. This loss of plasticity would appear to have resulted from the genetic assimilation of the heat induction response in the noninducing environment. However, analyses of transcriptional variation via RNA-sequencing from the selected populations revealed no global changes in gene regulation correlated with the observed changes in heat stress resistance. Instead, assays of the phenotypic response across a broader range of temperatures revealed that the induced plasticity was not fixed across environments, but rather the threshold for the response was shifted to higher temperatures over evolutionary time. These results demonstrate that apparent genetic assimilation can result from shifting thresholds of induction across environments and that analysis of the broader environmental context is critically important for understanding the evolution of phenotypic plasticity. Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve. However, the rate and genetic basis of plasticity evolution remain largely unknown. We experimentally evolved outbred populations of the nematode Caenorhabditis remanei under an acute heat shock during early larval development. When raised in a nonstressful environment, ancestral populations were highly sensitive to a 36.8° heat shock and exhibited high mortality. However, initial exposure to a nonlethal high temperature environment resulted in significantly reduced mortality during heat shock (hormesis). Lines selected for heat shock resistance rapidly evolved the capacity to withstand heat shock in the native environment without any initial exposure to high temperatures, and early exposure to high temperatures did not lead to further increases in heat resistance. This loss of plasticity would appear to have resulted from the genetic assimilation of the heat induction response in the noninducing environment. However, analyses of transcriptional variation via RNA-sequencing from the selected populations revealed no global changes in gene regulation correlated with the observed changes in heat stress resistance. Instead, assays of the phenotypic response across a broader range of temperatures revealed that the induced plasticity was not fixed across environments, but rather the threshold for the response was shifted to higher temperatures over evolutionary time. These results demonstrate that apparent genetic assimilation can result from shifting thresholds of induction across environments and that analysis of the broader environmental context is critically important for understanding the evolution of phenotypic plasticity. Abstract Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve. However, the rate and genetic basis of plasticity evolution remain largely unknown. We experimentally evolved outbred populations of the nematode Caenorhabditis remanei under an acute heat shock during early larval development. When raised in a nonstressful environment, ancestral populations were highly sensitive to a 36.8° heat shock and exhibited high mortality. However, initial exposure to a nonlethal high temperature environment resulted in significantly reduced mortality during heat shock (hormesis). Lines selected for heat shock resistance rapidly evolved the capacity to withstand heat shock in the native environment without any initial exposure to high temperatures, and early exposure to high temperatures did not lead to further increases in heat resistance. This loss of plasticity would appear to have resulted from the genetic assimilation of the heat induction response in the noninducing environment. However, analyses of transcriptional variation via RNA-sequencing from the selected populations revealed no global changes in gene regulation correlated with the observed changes in heat stress resistance. Instead, assays of the phenotypic response across a broader range of temperatures revealed that the induced plasticity was not fixed across environments, but rather the threshold for the response was shifted to higher temperatures over evolutionary time. These results demonstrate that apparent genetic assimilation can result from shifting thresholds of induction across environments and that analysis of the broader environmental context is critically important for understanding the evolution of phenotypic plasticity. |
Author | Reynolds, Rose M Sikkink, Kristin L Phillips, Patrick C Ituarte, Catherine M Cresko, William A |
Author_xml | – sequence: 1 givenname: Kristin L surname: Sikkink fullname: Sikkink, Kristin L organization: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon 97403-5289 – sequence: 2 givenname: Rose M surname: Reynolds fullname: Reynolds, Rose M organization: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon 97403-5289 – sequence: 3 givenname: Catherine M surname: Ituarte fullname: Ituarte, Catherine M organization: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon 97403-5289 – sequence: 4 givenname: William A surname: Cresko fullname: Cresko, William A email: wcresko@uoregon.edu organization: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon 97403-5289 – sequence: 5 givenname: Patrick C surname: Phillips fullname: Phillips, Patrick C email: pphil@uoregon.edu organization: Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon 97403-5289 |
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Keywords | heat stress experimental evolution natural selection genetic assimilation hormesis heat shock proteins |
Language | English |
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Snippet | Abstract
Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and... Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve.... |
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SubjectTerms | Adaptation, Biological - genetics Animals Biological Evolution Caenorhabditis - genetics Environment Gene Expression Profiling Gene Expression Regulation Gene-Environment Interaction Heat resistance Heat-Shock Response Investigations Phenotype Selection, Genetic |
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Title | Rapid Evolution of Phenotypic Plasticity and Shifting Thresholds of Genetic Assimilation in the Nematode Caenorhabditis remanei |
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