Evolution of the Spider Homeobox Gene Repertoire by Tandem and Whole Genome Duplication

Abstract

Gene duplication generates new genetic material that can contribute to the evolution of gene regulatory networks and phenotypes. Duplicated genes can undergo subfunctionalization to partition ancestral functions and/or neofunctionalization to assume a new function. We previously found there had been a whole genome duplication (WGD) in an ancestor of arachnopulmonates, the lineage including spiders and scorpions but excluding other arachnids like mites, ticks, and harvestmen. This WGD was evidenced by many duplicated homeobox genes, including two Hox clusters, in spiders. However, it was unclear which homeobox paralogues originated by WGD versus smaller-scale events such as tandem duplications. Understanding this is a key to determining the contribution of the WGD to arachnopulmonate genome evolution. Here we characterized the distribution of duplicated homeobox genes across eight chromosome-level spider genomes. We found that most duplicated homeobox genes in spiders are consistent with an origin by WGD. We also found two copies of conserved homeobox gene clusters, including the Hox, NK, HRO, Irx, and SINE clusters, in all eight species. Consistently, we observed one copy of each cluster was degenerated in terms of gene content and organization while the other remained more intact. Focussing on the NK cluster, we found evidence for regulatory subfunctionalization between the duplicated NK genes in the spider Parasteatoda tepidariorum compared to their single-copy orthologues in the harvestman Phalangium opilio. Our study provides new insights into the relative contributions of multiple modes of duplication to the homeobox gene repertoire during the evolution of spiders and the function of NK genes.

A comprehensive examination of Chelicerate genomes reveals no evidence for a whole genome duplication among spiders and scorpions

“…Here, we used several of these methods to investigate the existence of ancient WGDs in the Chelicerates (Nossa, et al 2014; Kenny, et al 2016; Shingate, Ravi, Prasad, Tay, et al 2020; Shingate, Ravi, Prasad, Tay and Venkatesh 2020). Several rounds of WGD have been proposed in the history of horseshoe crab evolution, and a single WGD has been proposed in the ancestor of spiders and scorpions (Sharma, et al 2014; Clarke, et al 2015; Schwager, et al 2017; Leite, et al 2018; Fan, et al 2021; Harper, et al 2021; Aase-Remedios, et al 2023). The evidence for these events usually starts with the observation of the duplication of a well-conserved gene family cluster, the Hox genes.…”

“…Examination of the Hox gene cluster has also been used to suggest that there have been anywhere between one and three WGDs during the course of horseshoe crab evolution (Kenny, et al 2016; Shingate, Ravi, Prasad, Tay, et al 2020; Shingate, Ravi, Prasad, Tay and Venkatesh 2020). Similar approaches also form the basis for the claim that a WGD has occurred in the lineage ancestral to extant spiders and scorpions (Sharma, et al 2014; Clarke, et al 2015; Schwager, et al 2017; Leite, et al 2018; Fan, et al 2021; Harper, et al 2021; Aase-Remedios, et al 2023). In both cases, the number of genes or genomes used for analysis has been limited.…”

Genome sequences of fourIxodesspecies expands understanding of tick evolution

“…Gene duplication can result from different mechanisms, with both small-scale events, such as tandem duplications and retropositions, and larger-scale events, such as segmental duplications or whole genome duplication (WGD) (Wolfe & Shields 1997; Kuzmin et al 2022). In the Chelicerata, previous studies have shown that WGD has occurred independently in the Xiphosura (horseshoe crabs) (Kenny et al 2016) and in the common ancestor of scorpions and spiders (Schwager et al 2017; Aase-Remedios et al 2023), whereas there is currently no evidence of WGD in ticks. A previous study based on the genetic distances between paralogs (Van Zee et al 2016) suggested that large-scale duplications may have occurred in ancestral ticks.…”