Dataset Information

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish.

ABSTRACT: Comparative studies of developmental processes suggest that novel traits usually evolve through the cooption of preexisting genes and proteins, mainly via gene duplication and functional specialization of paralogs. However, an alternative hypothesis is that novel protein function can evolve without gene duplication, through changes in the spatiotemporal patterns of gene expression (e.g., via cis-regulatory elements), or functional modifications (e.g., addition of functional domains) of the proteins they encode, or both. Here we present an astacin metalloprotease, dubbed patristacin, which has been coopted without duplication, via alteration in the expression of a preexisting gene from the kidney and liver of bony fishes, for a novel role in the brood pouch of pregnant male pipefish. We examined the molecular evolution of patristacin and found conservation of astacin-specific motifs but also several positively selected amino acids that may represent functional modifications for male pregnancy. Overall, our results pinpoint a clear case in which gene cooption occurred without gene duplication during the genesis of an evolutionarily significant novel structure, the male brood pouch. These findings contribute to a growing understanding of morphological innovation, a critically important but poorly understood process in evolutionary biology.

SUBMITTER: Harlin-Cognato A

PROVIDER: S-EPMC1748239 | biostudies-literature | 2006 Dec

REPOSITORIES: biostudies-literature

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Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish.

Harlin-Cognato April A Hoffman Eric A EA Jones Adam G AG

Proceedings of the National Academy of Sciences of the United States of America 20061208 51

Comparative studies of developmental processes suggest that novel traits usually evolve through the cooption of preexisting genes and proteins, mainly via gene duplication and functional specialization of paralogs. However, an alternative hypothesis is that novel protein function can evolve without gene duplication, through changes in the spatiotemporal patterns of gene expression (e.g., via cis-regulatory elements), or functional modifications (e.g., addition of functional domains) of the prote ...[more]

PMID: 17158805

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Project description:BackgroundConvergent and parallel evolution provide unique insights into the mechanisms of natural selection. Some of the most striking convergent and parallel (collectively recurrent) amino acid substitutions in proteins are adaptive, but there are also many that are selectively neutral. Accordingly, genome-wide assessment has shown that recurrent sequence evolution in orthologs is chiefly explained by nearly neutral evolution. For paralogs, more frequent functional change is expected because additional copies are generally not retained if they do not acquire their own niche. Yet, it is unknown to what extent recurrent sequence differentiation is discernible after independent gene duplications in different eukaryotic taxa.ResultsWe develop a framework that detects patterns of recurrent sequence evolution in duplicated genes. This is used to analyze the genomes of 90 diverse eukaryotes. We find a remarkable number of families with a potentially predictable functional differentiation following gene duplication. In some protein families, more than ten independent duplications show a similar sequence-level differentiation between paralogs. Based on further analysis, the sequence divergence is found to be generally asymmetric. Moreover, about 6% of the recurrent sequence evolution between paralog pairs can be attributed to recurrent differentiation of subcellular localization. Finally, we reveal the specific recurrent patterns for the gene families Hint1/Hint2, Sco1/Sco2 and vma11/vma3.ConclusionsThe presented methodology provides a means to study the biochemical underpinning of functional differentiation between paralogs. For instance, two abundantly repeated substitutions are identified between independently derived Sco1 and Sco2 paralogs. Such identified substitutions allow direct experimental testing of the biological role of these residues for the repeated functional differentiation. We also uncover a diverse set of families with recurrent sequence evolution and reveal trends in the functional and evolutionary trajectories of this hitherto understudied phenomenon.

Dataset Information

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish.

Publications

Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish.

Similar Datasets

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