Evolution of novel genes in three-spined stickleback populations

Schmitz, Julia; Chain, Frédéric J. J.; Bornberg‐Bauer, Erich

doi:10.1038/s41437-020-0319-7

Cited by 35 publications

(38 citation statements)

References 87 publications

(141 reference statements)

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“…Rapid evolution of the genome, especially the intergenic regions, have been postulated to contribute to genetic diversity 1 – 5 . In Drosophila, yeasts, stickleback fishes, and even in humans some intergenic regions have been shown to evolve into ‘de novo’ or ‘orphan’ or ‘proto’ genes, and they were more often shown to be specifically expressed as transcripts in tissues associated with male reproduction 4 , 6 , 7 , suggesting sexual or gamete selection. Subsequently, de novo genes were identified in many other organisms 8 , 9 .…”

Section: Introductionmentioning

confidence: 99%

Evolutionary divergence of novel open reading frames in cichlids speciation

Puntambekar

Newhouse

San-Miguel

et al. 2020

Sci Rep

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Novel open reading frames (nORFs) with coding potential may arise from noncoding DNA. Not much is known about their emergence, functional role, fixation in a population or contribution to adaptive radiation. Cichlids fishes exhibit extensive phenotypic diversification and speciation. Encounters with new environments alone are not sufficient to explain this striking diversity of cichlid radiation because other taxa coexistent with the Cichlidae demonstrate lower species richness. Wagner et al. analyzed cichlid diversification in 46 African lakes and reported that both extrinsic environmental factors and intrinsic lineage-specific traits related to sexual selection have strongly influenced the cichlid radiation, which indicates the existence of unknown molecular mechanisms responsible for rapid phenotypic diversification, such as emergence of novel open reading frames (nORFs). In this study, we integrated transcriptomic and proteomic signatures from two tissues of two cichlids species, identified nORFs and performed evolutionary analysis on these nORF regions. Our results suggest that the time scale of speciation of the two species and evolutionary divergence of these nORF genomic regions are similar and indicate a potential role for these nORFs in speciation of the cichlid fishes.

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Section: Introductionmentioning

confidence: 99%

Evolutionary divergence of novel open reading frames in cichlids speciation

Puntambekar

Newhouse

San-Miguel

et al. 2020

Sci Rep

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“…Fine-scale analyses, using closely related taxa, have allowed for the study of the evolution of protein properties in insects ( Heames et al. 2020 ) and fish ( Schmitz et al. 2020 ) but, until now, not mammals.…”

Section: Discussionmentioning

confidence: 99%

Stochastic Gain and Loss of Novel Transcribed Open Reading Frames in the Human Lineage

Dowling

Schmitz

Bornberg‐Bauer

2020

Genome Biology and Evolution

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In addition to known genes, much of the human genome is transcribed into RNA. Chance formation of novel open reading frames (ORFs) can lead to the translation of myriad new proteins. Some of these ORFs may yield advantageous adaptive de novo proteins. However, widespread translation of non-coding DNA can also produce hazardous protein molecules, which can misfold and\or form toxic aggregates. The dynamics of how de novo proteins emerge from potentially toxic raw materials and what influences their long-term survival are unknown. Here, using transcriptomic data from human and five other primates, we generate a set of transcribed human ORFs at six conservation levels to investigate which properties influence the early emergence and long-term retention of these expressed ORFs. As these taxa diverged from each other relatively recently we present a fine scale view of the evolution of novel sequences over recent evolutionary time. We find that novel human-restricted ORFs are preferentially located on GC-rich gene-dense chromosomes, suggesting their retention is linked to pre-existing genes. Sequence properties such as intrinsic structural disorder and aggregation propensity–which have been proposed to play a role in survival of de novo genes–remain relatively unchanged over time. Even very young sequences code for proteins with low aggregation propensities, suggesting that genomic regions with many novel transcribed ORFs are concomitantly less likely to produce ORFs which code for harmful toxic proteins. Our data indicate that the survival of these novel ORFs is largely stochastic rather than shaped by selection.

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“…Rapid evolution of the genome, especially the intergenic regions, have been postulated to contribute to genetic diversity 2 3 4 5 6 . In Drosophila, yeasts, stickleback fishes, and even in humans some intergenic regions have been shown to evolve into ‘de novo’ or ‘orphan’ or ‘proto’ genes, and they were more often shown to be specifically expressed as transcripts in tissues associated with male reproduction 5,7,8 , suggesting a sexual or gamete selection. Subsequently, de novo genes were identified in many other organisms 9, 10 .…”

Section: Introductionmentioning

confidence: 99%

Evolutionary divergence of novel open reading frames in cichlids speciation

Puntambekar

Newhouse

Navas

et al. 2020

Preprint

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Cichlids fishes exhibit extensive phenotypic diversification and speciation. Encounters with new environments alone are not sufficient to explain this striking diversity of cichlid radiation because other taxa coexistent with the Cichlidae demonstrate lower species richness. Wagner et al analyzed cichlid diversification in 46 African lakes and reported that both extrinsic environmental factors and intrinsic lineage-specific traits related to sexual selection have strongly influenced the cichlid radiation 1 , which indicates the existence of molecular mechanisms responsible for rapid phenotypic diversification and events leading to reproductive isolation. However discovery of the molecular mechanisms in terms of genetic or transcriptomic or proteomic diversity responsible for the rapid speciation in a short geological time has remained elusive. In this study we integrated transcriptomic and proteomic signatures from two cichlids species, identified novel open reading frames (nORFs) and performed evolutionary analysis on these nORF regions. Our results suggest that the time scale of speciation of the two species can be better explained by the evolutionary divergence of these nORF genomic regions. Therefore this study has revealed the potential functional and evolutionary role of nORFs, which has far reaching implications for such evolutionary and speciation studies that have traditionally been focussed on known protein coding regions.

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Evolution of novel genes in three-spined stickleback populations

Cited by 35 publications

References 87 publications

Evolutionary divergence of novel open reading frames in cichlids speciation

Evolutionary divergence of novel open reading frames in cichlids speciation

Stochastic Gain and Loss of Novel Transcribed Open Reading Frames in the Human Lineage

Evolutionary divergence of novel open reading frames in cichlids speciation

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