Mechanisms and dynamics of orphan gene emergence in insect genomes

Lothar Wissler, Juergen Gadau, Daniel F. Simola, Martin Helmkampf, Erich Bornberg-Bauer

Research output: Contribution to journalArticle

70 Citations (Scopus)

Abstract

Orphan genes are defined as genes that lack detectable similarity to genes in other species and therefore no clear signals of common descent (i.e., homology) can be inferred. Orphans are an enigmatic portion of the genome because their origin and function are mostly unknown and they typically make up 10% to 30% of all genes in a genome. Several case studies demonstrated that orphans can contribute to lineage-specific adaptation. Here, we study orphan genes by comparing 30 arthropod genomes, focusing in particular on seven recently sequenced ant genomes. This setup allows analyzing a major metazoan taxon and a comparison between social Hymenoptera (ants and bees) and nonsocial Diptera (flies and mosquitoes). First, we find that recently split lineages undergo accelerated genomic reorganization, including the rapid gain of many orphan genes. Second, between the two insect orders Hymenoptera and Diptera, orphan genes aremore abundant and emerge more rapidly in Hymenoptera, in particular, in leaf-cutter ants. With respect to intragenomic localization, we find that ant orphan genes show little clustering, which suggests that orphan genes in ants are scattered uniformly over the genome and between nonorphan genes. Finally, our results indicate that the genetic mechanisms creating orphan genes-such as gene duplication, frame-shift fixation, creation of overlapping genes, horizontal gene transfer, and exaptation of transposable elements-act at different rates in insects, primates, and plants. In Formicidae, the majority of orphan genes has their origin in intergenic regions, pointing to a high rate of de novo gene formation or generalized gene loss, and support a recently proposed dynamic model of frequent gene birth and death.

Original languageEnglish (US)
Pages (from-to)439-445
Number of pages7
JournalGenome Biology and Evolution
Volume5
Issue number2
DOIs
StatePublished - 2013

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Insect Genome
orphan
eclosion
genome
insect
insects
gene
Genes
Ants
genes
Formicidae
ant
Hymenoptera
Genome
Diptera
Insects
Overlapping Genes
Horizontal Gene Transfer

Keywords

  • Ants (Formicidae)
  • Genome evolution
  • Insects
  • Orphan genes

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Mechanisms and dynamics of orphan gene emergence in insect genomes. / Wissler, Lothar; Gadau, Juergen; Simola, Daniel F.; Helmkampf, Martin; Bornberg-Bauer, Erich.

In: Genome Biology and Evolution, Vol. 5, No. 2, 2013, p. 439-445.

Research output: Contribution to journalArticle

Wissler, L, Gadau, J, Simola, DF, Helmkampf, M & Bornberg-Bauer, E 2013, 'Mechanisms and dynamics of orphan gene emergence in insect genomes', Genome Biology and Evolution, vol. 5, no. 2, pp. 439-445. https://doi.org/10.1093/gbe/evt009
Wissler, Lothar ; Gadau, Juergen ; Simola, Daniel F. ; Helmkampf, Martin ; Bornberg-Bauer, Erich. / Mechanisms and dynamics of orphan gene emergence in insect genomes. In: Genome Biology and Evolution. 2013 ; Vol. 5, No. 2. pp. 439-445.
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