Abstract

BackgroundThe ancestral arthropod is believed to have had a clustered arrangement of ten Hox genes. Within arthropods, Hox gene mutations result in transformation of segment identities. Despite the fact that variation in segment number/character was common in the diversification of arthropods, few examples of Hox gene gains/losses have been correlated with morphological evolution. Furthermore, a full appreciation of the variation in the genomic arrangement of Hox genes in extant arthropods has not been recognized, as genome sequences from each major arthropod clade have not been reported until recently. Initial genomic analysis of the chelicerate Tetranychusurticae suggested that loss of Hox genes and Hox gene clustering might be more common than previously assumed. To further characterize the genomic evolution of arthropod Hox genes, we compared the genomic arrangement and general characteristics of Hox genes from representative taxa from each arthropod subphylum.ResultsIn agreement with others, we find arthropods generally contain ten Hox genes arranged in a common orientation in the genome, with an increasing number of sampled species missing either Hox3 or abdominal-A orthologs. The genomic clustering of Hox genes in species we surveyed varies significantly, ranging from 0.3 to 13.6 Mb. In all species sampled, arthropod Hox genes are dispersed in the genome relative to the vertebrate Mus musculus. Differences in Hox cluster size arise from variation in the number of intervening genes, intergenic spacing, and the size of introns and UTRs. In the arthropods surveyed, Hox gene duplications are rare and four microRNAs are, in general, conserved in similar genomic positions relative to the Hox genes.ConclusionsThe tightly clustered Hox complexes found in the vertebrates are not evident within arthropods, and differential patterns of Hox gene dispersion are found throughout the arthropods. The comparative genomic data continue to support an ancestral arthropod Hox cluster of ten genes with a shared orientation, with four Hox gene-associated miRNAs, although the degree of dispersion between genes in an ancestral cluster remains uncertain. Hox3 and abdominal-A orthologs have been lost in multiple, independent lineages, and current data support a model in which inversions of the Abdominal-B locus that result in the loss of abdominal-A correlate with reduced trunk segmentation.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-016-0048-4) contains supplementary material, which is available to authorized users.

Highlights

  • The ancestral arthropod is believed to have had a clustered arrangement of ten Hox genes

  • The increase in the spatial arrangement of the Ixodes Hox cluster is correlated with its large genome (1.7 gigabase pairs (Gb)) [57] relative to other arthropods with sequenced genomes, which range from 91 megabase pairs (Mb) in Tetranychus [24] to 1.3 Gb in Aedes aegypti [69]

  • Excluding arthropods with Hox genes organized into distinct genomic complexes (e.g., Drosophila, Bombyx, and Tetranychus), the variation in clustering of Hox genes is mainly attributed to the amount of intervening space between Hox genes, not to a lack of Hox gene coding sequence, intron, and untranslated region (UTR) lengths

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Summary

Introduction

The ancestral arthropod is believed to have had a clustered arrangement of ten Hox genes. The Hox genes are a highly conserved set of homeodomain transcription factors that function in fundamental developmental processes in metazoans This conservation extends to their genomic arrangement [1,2,3]. Inversions that disrupt the transcriptional orientation of Hox genes are found in several taxa, including Drosophila and Anopheles gambiae [13, 14, 17, 18, 21, 22] (Fig. 1). These fragmented and inverted organizations appear unusual among insects

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