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Taxonomically Restricted Genes Are Fundamental to Biology and Evolution.

ABSTRACT: Genes limited to particular clades, taxonomically restricted genes (TRGs), are common in all sequenced genomes. TRGs have recently become associated with the evolution of novelty, as numerous studies across the tree of life have now linked expression of TRGs with novel phenotypes. However, TRGs that underlie ancient lineage specific traits have been largely omitted from discussions of the general importance of TRGs. Here it is argued that when all TRGs are considered, it is apparent that TRGs are fundamental to biology and evolution and likely play many complementary roles to the better understood toolkit genes. Genes underlying photosynthesis and skeletons, for example, are examples of commonplace fundamental TRGs. Essentially, although basic cell biology has a highly conserved genetic basis across the tree of life, most major clades also have lineage specific traits central to their biology and these traits are often based on TRGs. In short, toolkit genes underlie what is conserved across organisms, while TRGs define in many cases what is unique. An appreciation of the importance of TRGs will improve our understanding of evolution by triggering the study of neglected topics in which TRGs are of paramount importance.

SUBMITTER: Johnson BR

PROVIDER: S-EPMC6158316 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Taxonomically Restricted Genes Are Fundamental to Biology and Evolution.

Johnson Brian R BR

Frontiers in genetics 20180920

Genes limited to particular clades, taxonomically restricted genes (TRGs), are common in all sequenced genomes. TRGs have recently become associated with the evolution of novelty, as numerous studies across the tree of life have now linked expression of TRGs with novel phenotypes. However, TRGs that underlie ancient lineage specific traits have been largely omitted from discussions of the general importance of TRGs. Here it is argued that when all TRGs are considered, it is apparent that TRGs ar ...[more]

PMID: 30294344

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Project description:BackgroundStudies have shown that taxonomically restricted genes are significant in number and important for the evolution of lineage specific traits. Social insects have gained many novel morphological and behavioral traits relative to their solitary ancestors. The task repertoire of an advanced social insect, for example, can be 40-50 tasks, about twice that of a solitary wasp or bee. The genetic basis of this expansion in behavioral repertoire is still poorly understood, and a role for taxonomically restricted genes has not been explored at the whole genome level.ResultsHere we present comparative genomics results suggesting that taxonomically restricted genes may have played an important role in generating the expansion of behavioral repertoire associated with the evolution of eusociality. First, we show that the current honey bee official gene set contains about 700 taxonomically restricted genes. These are split between orphans, genes found only in the Hymenoptera, and genes found only in insects. Few of the orphans or genes restricted to the Hymenoptera have been the focus of experimental work, but several of those that have are associated with novel eusocial traits or traits thought to have changed radically as a consequence of eusociality. Second, we predicted that if taxonomically restricted genes are important for generating novel eusocial traits, then they should be expressed with greater frequency in workers relative to the queen, as the workers exhibit most of the novel behavior of the honey bee relative to their solitary ancestors. We found support for this prediction. Twice as many taxonomically restricted genes were found amongst the genes with higher expression in workers compared to those with higher expression in queens. Finally, we compiled an extensive list of candidate taxonomically restricted genes involved in eusocial evolution by analyzing several caste specific gene expression data sets.ConclusionsThis work identifies a large number of candidate taxonomically restricted genes that may have played a role in eusocial evolution. This work thus lays the foundation for future functional genomics work on the evolution of novelty in the context of social behavior. We also present preliminary evidence, based on biased patterns of gene expression, that taxonomically restricted genes may have played a role in the evolution of caste systems, a characteristic lineage specific social trait.

Dataset Information

Taxonomically Restricted Genes Are Fundamental to Biology and Evolution.

Publications

Taxonomically Restricted Genes Are Fundamental to Biology and Evolution.

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