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.

Keywords: genome duplication; genomics; hexapods; insects; polyploidy.

Fig. 1.

Inferring ancient WGDs and large-scale genome duplications. Histograms of the age distribution of gene duplications (Ks plots) with mixture models of inferred WGDs for (A) Baetis sp. (Ephemeroptera), inferred WGD peak median Ks = 0.83. (B) Menopon gallinae (Psocodea), inferred WGD peak median Ks = 0.80. (C) Gynaikothrips ficorum (Thysanoptera), inferred WGD peak median Ks = 1.73. (D) T. saltator (Diptera), inferred WGD peak median Ks = 0.59. The mixture model distributions consistent with inferred ancient WGDs are highlighted in yellow. (E) MAPS results from observed data, null and positive simulations on the associated phylogeny. Percentage of subtrees that contain a gene duplication shared by descendant species at each node, results from observed data (red line), 100 resampled sets of null simulations (multiple black lines), and positive simulations (multiple gray lines). The red oval corresponds to the location of an inferred large-scale genome duplication event in Lepidoptera.

Fig. 2.

Placement of inferred ancient genome duplications on the phylogeny of Hexapoda. Red circles indicate WGDs in hexapods inferred from Ks plots; orange circles, WGDs in outgroups inferred from KS plots; blue diamonds, large-scale genome duplications inferred by MAPS analyses; empty squares, episodic bursts of gene duplication with varying levels of significance across different MAPS analyses. Hexapod phylogeny adapted from Misof et al. (26). The Solenopsis invicta (Hymenoptera) WGD inferred by Ks plot is not included in this phylogeny. Images of Raphidioptera, Coleoptera, and Neuroptera are credited to artists Tang Liang, Zichen Wang, and Zheng Li. Other images are in the public domain and credit information for each can be found in SI Appendix, Table S6.

Fig. 3.

Principal component analysis of the GO category composition of all genes in each genome/transcriptome and WGD paralogs. Red circles indicate number of genes annotated to each GO category in the whole genome or transcriptomes; black circles, number of WGD paralogs annotated to each GO category. Ellipses represent the 95% confidence interval of SD of point scores.