New genes as drivers of phenotypic evolution

Chen, Sidi; Krinsky, Benjamin H.; Long, Manyuan

doi:10.1038/nrg3521

Cited by 355 publications

(298 citation statements)

References 131 publications

(181 reference statements)

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“…There is a debate over the relative roles for core sets of conserved genes (42-48) and taxon-restricted genes (TRGs) (5,44,47,49,50) in the evolution of convergent phenotypes (7,44,46). We found evidence that both types of gene classes play peripheral roles in the molecular networks associated with phenotypic differentiation in our study species.…”

Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 56%

“…in the evolution of phenotypic diversity (5,44,(47)(48)(49)(50)(51). Our analyses add to this hypothesis by identifying roles for both conserved genes and TRGs in highly plastic phenotypes.…”

Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 56%

“…S8) and at similar levels to TRGs across the whole genome [ant (11.6% TRGs): χ 2 = 0.11, P = 0.74; wasp (9.1% TRGs): χ 2 = 0.52, P = 0.47; Dataset S5]. Taxon-restricted DEGs are likely to be new genes (short in length relative to annotated/known genes) (49) (Fig. S8) with unknown/novel functions ("guilt-by-association" network analysis) (41), because their nearest neighbors were also taxon-restricted (unknown function) (mean = 2.3 of the 10 most connected genes had BLAST hits; Fig.…”

Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 99%

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Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

202

278

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Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

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Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 56%

Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 56%

Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 99%

See 1 more Smart Citation

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

202

278

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“…Old genes originated in an evolutionary-distant common ancestor and orthologous copies are found across many distant taxa, whereas new genes originated recently and are found only in specific taxonomic groups. Taxonomically restricted genes (TRGs) have been the subject of recent attention because they are predicted to be drivers of phenotypic evolution (30). The genomes of social insects harbor many TRGs, which are hypothesized to play an important role in the elaboration of sociality (31).…”

Section: Resultsmentioning

confidence: 99%

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Harpur¹,

Kent²,

Molodtsova³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

195

271

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Most theories used to explain the evolution of eusociality rest upon two key assumptions: mutations affecting the phenotype of sterile workers evolve by positive selection if the resulting traits benefit fertile kin, and that worker traits provide the primary mechanism allowing social insects to adapt to their environment. Despite the common view that positive selection drives phenotypic evolution of workers, we know very little about the prevalence of positive selection acting on the genomes of eusocial insects. We mapped the footprints of positive selection in Apis mellifera through analysis of 40 individual genomes, allowing us to identify thousands of genes and regulatory sequences with signatures of adaptive evolution over multiple timescales. We found Apoidea-and Apis-specific genes to be enriched for signatures of positive selection, indicating that novel genes play a disproportionately large role in adaptive evolution of eusocial insects. Worker-biased proteins have higher signatures of adaptive evolution relative to queen-biased proteins, supporting the view that worker traits are key to adaptation. We also found genes regulating worker division of labor to be enriched for signs of positive selection. Finally, genes associated with worker behavior based on analysis of brain gene expression were highly enriched for adaptive protein and cis-regulatory evolution. Our study highlights the significant contribution of worker phenotypes to adaptive evolution in social insects, and provides a wealth of knowledge on the loci that influence fitness in honey bees.natural selection | kin selection | social evolution | taxonomically restricted genes E usocial behavior evolved multiple times in insects and is characterized in part by extreme asymmetries in the reproductive potential of individuals (1). This asymmetry is most pronounced in advanced eusocial insects, with their fertile queen and sterile worker castes. Darwin first recognized that natural selection cannot directly optimize worker phenotypes because workers are usually sterile (2). Hamilton (3, 4) developed kinselection theory to describe the conditions that allow natural selection to indirectly optimize worker phenotypes if such phenotypes benefit their fertile kin. It is commonly believed that worker traits, such as sib-care, foraging, and colony defense, play important roles in allowing colonies to adapt to their environment (5-7). However, despite the central role of kin-selection and inclusive fitness theory in the field of Sociobiology (8, 9), we lack knowledge on the pattern and prevalence of positive selection acting on the genomes of eusocial insects.Population genomic studies provide unprecedented opportunities to detect signatures of selection on DNA sequences over different timescales (10). There are several tests of selection that can be applied to genome-wide datasets. The McDonald-Kreitman (MK) test is arguably the best method for detecting selection on protein coding sequences because of its robustness to changes in a species' demography,...

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“…Gene duplication as a means of generating novel genes has been realized for a long time (Haldane 1933;Muller 1935;Bridges 1936;Lewis 1951;Stephens 1951;Nei 1969). Gradual change from a duplicated gene, via those encoding isoforms, up to the acquisition of novel functions including subfunctionalization (Lynch and Force 2000) is now well documented (Roth et al 2007;Kaessmann 2010;Chen et al 2013). Gene amplification can occur via segmental duplication (Bailey and Eichler 2006) or retroposition (Brosius 1999a;Babushok et al 2007) with a lower "success rate" for the latter.…”

Section: Yesterday's Junk Could Become Tomorrow's Novel Gene Module mentioning

confidence: 99%

The Persistent Contributions of RNA to Eukaryotic Gen(om)e Architecture and Cellular Function

Brosius

2014

Cold Spring Harbor Perspectives in Biology

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New genes as drivers of phenotypic evolution

Cited by 355 publications

References 131 publications

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

The Persistent Contributions of RNA to Eukaryotic Gen(om)e Architecture and Cellular Function

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