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

Abstract

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.

Inferring putative ancient whole genome duplications in the 1000 Plants (1KP) initiative: access to gene family phylogenies and age distributions

“…To place inferred WGDs from Ks plots onto the species phylogeny, we compared the median paralog divergence ( Ks ) of putative WGD peaks to the divergence of orthologs among species across the phylogeny [4] . We also employed phylogenomic analyses and simulations of WGDs using MultitAxon Paleopolyploidy Search(MAPS) [5,6] to corroborate the inferences and phylogenetic placements of the putative ancient WGDs.…”

“…We used MAPS, a gene tree topology sorting algorithm [5,6] , to confirm the placement of ancient WGDs that may be shared by at least three species. MAPS uses a given species tree to filter collections of nuclear gene trees for subtrees consistent with relationships at each node in the species tree.…”

“…For this reason, we aimed to place the focal WGD test node in the middle of the phylogeny being examined. Secondly, we implemented an option in MAPS to increase taxon occupancy in the gene trees by requiring a minimum number of ingroup taxa be present in each subtree [5] . Based on previous work [27] and balancing the number of trees retained in our analyses, we used a minimum 45% ingroup taxa requirement in our MAPS analyses.…”

The causes and consequences of subgenome dominance in hybrids and recent polyploids

“…Additionally, biased subgenome patterns in polyploid lineages are ideal for probing mechanisms of convergent evolution potentially caused by constraint, drift, selection, or a dynamic combination of the three (Washburn et al, 2016). Such questions can be tested by comparing molecular mechanisms of subgenome dominance in diverse lineages, including animals (Braasch & Postlethwait, 2012;Session et al, 2016;McElroy et al, 2017;Li et al, 2018). A fascinating question that remains to be answered is whether a parallel mechanism of subgenome dominance operates in animal systems.…”

Universal trends of post-duplication evolution revealed by the genomes of 13Parameciumspecies sharing an ancestral whole-genome duplication

“…In its most extreme form, duplication can encompass the entire genome, creating a new copy of each gene. Such Whole-Genome Duplication (WGD) events are not uncommon, with evidence of ancient WGDs in the lineages of many eukaryotes including the budding yeast (Kellis, et al 2004), insects (Li, et al 2018), the African clawed frog (Session, et al 2016), the rainbow trout (Berthelot, et al 2014) and Paramecium (Aury, et al 2006). It is also now widely accepted that two successive rounds of WGDs occurred in the ancestor of vertebrates (Hokamp, et al 2003;Dehal and Boore 2005;Holland and Ocampo Daza 2018) and an additional round of genome duplication in the lineage leading to all teleost fish (Meyer and Schartl 1999;Jaillon, et al 2004;Howe, et al 2013;Glasauer and Neuhauss 2014).…”