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Molecular basis of canalization in an ascidian species complex adapted to different thermal conditions.

ABSTRACT: Canalization is a result of intrinsic developmental buffering that ensures phenotypic robustness under genetic variation and environmental perturbation. As a consequence, animal phenotypes are remarkably consistent within a species under a wide range of conditions, a property that seems contradictory to evolutionary change. Study of laboratory model species has uncovered several possible canalization mechanisms, however, we still do not understand how the level of buffering is controlled in natural populations. We exploit wild populations of the marine chordate Ciona intestinalis to show that levels of buffering are maternally inherited. Comparative transcriptomics show expression levels of genes encoding canonical chaperones such as Hsp70 and Hsp90 do not correlate with buffering. However the expression of genes encoding endoplasmic reticulum (ER) chaperones does correlate. We also show that ER chaperone genes are widely conserved amongst animals. Contrary to previous beliefs that expression level of Heat Shock Proteins (HSPs) can be used as a measurement of buffering levels, we propose that ER associated chaperones comprise a cellular basis for canalization. ER chaperones have been neglected by the fields of development, evolution and ecology, but their study will enhance understanding of both our evolutionary past and the impact of global environmental change.

SUBMITTER: Sato A

PROVIDER: S-EPMC4649386 | biostudies-literature | 2015 Nov

REPOSITORIES: biostudies-literature

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Molecular basis of canalization in an ascidian species complex adapted to different thermal conditions.

Sato Atsuko A Kawashima Takeshi T Fujie Manabu M Hughes Samantha S Satoh Noriyuki N Shimeld Sebastian M SM

Scientific reports 20151118

Canalization is a result of intrinsic developmental buffering that ensures phenotypic robustness under genetic variation and environmental perturbation. As a consequence, animal phenotypes are remarkably consistent within a species under a wide range of conditions, a property that seems contradictory to evolutionary change. Study of laboratory model species has uncovered several possible canalization mechanisms, however, we still do not understand how the level of buffering is controlled in natu ...[more]

PMID: 26577490

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Project description:BackgroundCanalization, or buffering, is defined as developmental stability in the face of genetic and/or environmental perturbations. Understanding how canalization works is important in predicting how species survive environmental change, as well as deciphering how development can be altered in the evolutionary process. However, how developmental gene expression is linked to buffering remains unclear. We addressed this by co-expression network analysis, comparing gene expression changes caused by heat stress during development at a whole-embryonic scale in reciprocal hybrid crosses of sibling species of the ascidian Ciona that are adapted to different thermal environments.ResultsSince our previous work showed that developmental buffering in this group is maternally inherited, we first identified maternal developmental buffering genes (MDBGs) in which the expression level in embryos is both correlated to the level of environmental canalization and also differentially expressed depending on the species' gender roles in hybrid crosses. We found only 15 MDBGs, all of which showed high correlation coefficient values for expression with a large number of other genes, and 14 of these belonged to a single co-expression module. We then calculated correlation coefficients of expression between MDBGs and transcription factors in the central nervous system (CNS) developmental gene network that had previously been identified experimentally. We found that, compared to the correlation coefficients between MDBGs, which had an average of 0.96, the MDBGs are loosely linked to the CNS developmental genes (average correlation coefficient 0.45). Further, we investigated the correlation of each developmental to MDBGs, showing that only four out of 62 CNS developmental genes showed correlation coefficient > 0.9, comparable to the values between MDBGs, and three of these four genes were signaling molecules: BMP2/4, Wnt7, and Delta-like.ConclusionsWe show that the developmental pathway is not centrally located within the buffering network. We found that out of 62 genes in the developmental gene network, only four genes showed correlation coefficients as high as between MDBGs. We propose that loose links to MDBGs stabilize spatiotemporally dynamic development.

Project description:Understanding the biological mechanisms of climatic adaptation is of paramount importance for the optimization of breeding programs and conservation of genetic resources. The aim of this study was to investigate genetic diversity and unravel genomic regions potentially under selection for heat and/or cold tolerance in thirty-two worldwide cattle breeds, with a focus on Chinese local cattle breeds adapted to divergent climatic conditions, Datong yak (Bos grunniens; YAK), and Bali (Bos javanicus) based on dense SNP data. In general, moderate genetic diversity levels were observed in most cattle populations. The proportion of polymorphic SNP ranged from 0.197 (YAK) to 0.992 (Mongolian cattle). Observed and expected heterozygosity ranged from 0.023 (YAK) to 0.366 (Sanhe cattle; SH), and from 0.021 (YAK) to 0.358 (SH), respectively. The overall average inbreeding (±SD) was: 0.118 ± 0.028, 0.228 ± 0.059, 0.194 ± 0.041, and 0.021 ± 0.004 based on the observed versus expected number of homozygous genotypes, excess of homozygosity, correlation between uniting gametes, and runs of homozygosity (ROH), respectively. Signatures of selection based on multiple scenarios and methods (F ST, HapFLK, and ROH) revealed important genomic regions and candidate genes. The candidate genes identified are related to various biological processes and pathways such as heat-shock proteins, oxygen transport, anatomical traits, mitochondrial DNA maintenance, metabolic activity, feed intake, carcass conformation, fertility, and reproduction. This highlights the large number of biological processes involved in thermal tolerance and thus, the polygenic nature of climatic resilience. A comprehensive description of genetic diversity measures in Chinese cattle and YAK was carried out and compared to 24 worldwide cattle breeds to avoid potential biases. Numerous genomic regions under positive selection were detected using three signature of selection methods and candidate genes potentially under positive selection were identified. Enriched function analyses pinpointed important biological pathways, molecular function and cellular components, which contribute to a better understanding of the biological mechanisms underlying thermal tolerance in cattle. Based on the large number of genomic regions identified, thermal tolerance has a complex polygenic inheritance nature, which was expected considering the various mechanisms involved in thermal stress response.

Dataset Information

Molecular basis of canalization in an ascidian species complex adapted to different thermal conditions.

Publications

Molecular basis of canalization in an ascidian species complex adapted to different thermal conditions.

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