Ancient Expansion of the Hox Cluster in Lepidoptera Generated Four Homeobox Genes Implicated in Extra-Embryonic Tissue Formation

Ferguson, Laura; Marlétaz, Ferdinand; Carter, Jean-Michel; Taylor, William R.; Gibbs, Melanie; Breuker, Casper J.; Holland, Peter W.H.

doi:10.1371/journal.pgen.1004698

Cited by 57 publications

(77 citation statements)

References 56 publications

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“…Our results raise the possibility that gene and genome duplications could be associated with major transitions in insect evolution. The route to such profound transitions might involve the introduction of novelty via duplication, as has been shown in the expanding Hox genes of some Lepidoptera (Ferguson et al 2014) . Our results lend support to long-standing hypotheses that gene and genome duplications are important forces in animal evolution (Ohno and Susumu 1970;Van de Peer et al 2009) .…”

Section: Discussionmentioning

confidence: 99%

Multiple large-scale gene and genome duplications during the evolution of hexapods

Tiley

Galuska

et al. 2018

Preprint

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Polyploidy or whole genome duplication (WGD) is a major contributor to genome evolution and diversity. Although polyploidy is recognized as an important component of plant evolution, it is generally considered to play a relatively minor role in animal evolution. Ancient polyploidy is found in the ancestry of some animals, especially fishes, but there is little evidence for ancient WGDs in other metazoan lineages. Here we use recently published transcriptomes and genomes from more than 150 species across the insect phylogeny to investigate whether ancient WGDs occurred during the evolution of Hexapoda, the most diverse clade of animals. Using gene age distributions and phylogenomics, we found evidence for 18 ancient WGDs and six other large-scale bursts of gene duplication during insect evolution. These bursts of gene duplication occurred in the history of lineages such as the Lepidoptera, Trichoptera, and Odonata. To further corroborate the nature of these duplications, we evaluated the pattern of gene retention from putative WGDs observed in the gene age distributions. We found a relatively strong signal of convergent gene retention across many of the putative insect WGDs.Considering the phylogenetic breadth and depth of the insect phylogeny, this observation is consistent with polyploidy as we expect dosage-balance to drive the parallel retention of genes. Together with recent research on plant evolution, our hexapod results suggest that genome duplications contributed to the evolution of two of the most diverse lineages of eukaryotes on Earth.

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Section: Discussionmentioning

confidence: 99%

Multiple large-scale gene and genome duplications during the evolution of hexapods

Tiley

Galuska

et al. 2018

Preprint

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“…To investigate the origin of Shx genes, we determined low-coverage genome sequences for five additional lepidopteran species chosen for phylogenetic position, plus a caddisfly outgroup [52,54]. Assembly and analysis revealed that the Bombyx situation is unusual, whereas possession of four distinct Shx genes (ShxA, ShxB, ShxC, ShxD) is typical for a large clade within Lepidoptera, encompassing butterflies (Heliconius, Polygonium, Pararge), tiger moth (Callimorpha) and Gracillariidae (Cameraria).…”

Section: Extra Hox Genes and The Evolutionary Success Of Lepidopteramentioning

confidence: 99%

“…The basal Orange swift moth also has zen duplicates, but without extensive divergence. (b) Localized ShxC RNA marks the presumptive serosa in developing oocytes of the speckled wood butterfly Pararge aegeria [52]. All four Shx genes are expressed in serosa as it develops.…”

Section: Glyphotaelius Pellucidus Caddisfly 4x 4xmentioning

confidence: 99%

New genes from old: asymmetric divergence of gene duplicates and the evolution of development

Holland

Marlétaz

Maeso

et al. 2017

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Evodevo in the genomics era, and the origins of morphological diversity'. Gene duplications and gene losses have been frequent events in the evolution of animal genomes, with the balance between these two dynamic processes contributing to major differences in gene number between species. After gene duplication, it is common for both daughter genes to accumulate sequence change at approximately equal rates. In some cases, however, the accumulation of sequence change is highly uneven with one copy radically diverging from its paralogue. Such 'asymmetric evolution' seems commoner after tandem gene duplication than after whole-genome duplication, and can generate substantially novel genes. We describe examples of asymmetric evolution in duplicated homeobox genes of moths, molluscs and mammals, in each case generating new homeobox genes that were recruited to novel developmental roles. The prevalence of asymmetric divergence of gene duplicates has been underappreciated, in part, because the origin of highly divergent genes can be difficult to resolve using standard phylogenetic methods.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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“…However, many bilateral animals have a disorganized HOX cluster with no obvious impact on their body plan (Duboule ). Hox gene number and order is highly flexible within some genera (e.g., Drosophila ) and phyla (e.g., Nematoda, Mollusca, Urochordata, Arthropoda) (Aboobaker and Blaxter ; Seo et al ; Negre and Ruiz ; Ferguson et al ). Therefore, Hox genes do not need to be organized in an intact cluster for proper development of the A‐P axis (Monteiro and Ferrier ; Negre and Ruiz ).…”

Section: Introductionmentioning

confidence: 99%

Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited

Byrne

Martinez

Morris

2016

Evolution and Development

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Echinodermata is a large phylum of marine invertebrates characterized by an adult, pentameral body plan. This morphology is clearly derived as all members of Deuterostomia (the superphylum to which they belong) have a bilateral body plan. The origin of the pentameral plan has been the subject of intense debate. It is clear that the ancestor of Echinodermata had a bilateral plan but how this ancestor transformed its body "architecture" in such a drastic manner is not clear. Data from the fossil record and ontogeny are sparse and, so far, not very informative. The sequencing of the sea urchin genome a decade ago opened the possibility that the pentameral body plan was a consequence of a broken Hox cluster and a series of papers dwelt on the putative relationship between Hox gene arrangements in the chromosomes and the origin of pentamery. This relationship, sound as it was, is challenged by the revelation that the sea star HOX cluster is, in fact, intact, thus falsifying the hypothesis of a direct relationship between HOX cluster arrangement and the origin of the pentameral body plan. Here, we explore the relationship between Hox gene arrangements and echinoderm body "architecture," the expression of Hox genes in development and alternative scenarios for the origin of pentamery, with putative roles for signaling centers in generating multiple axes.

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Ancient Expansion of the Hox Cluster in Lepidoptera Generated Four Homeobox Genes Implicated in Extra-Embryonic Tissue Formation

Cited by 57 publications

References 56 publications

Multiple large-scale gene and genome duplications during the evolution of hexapods

Multiple large-scale gene and genome duplications during the evolution of hexapods

New genes from old: asymmetric divergence of gene duplicates and the evolution of development

Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited

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