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.

Genomic data have provided evidence of previously unknown ancient whole genome duplications (WGDs) and highlighted the role of WGDs in the evolution of many eukaryotic lineages. Ancient WGDs often are detected by examining distributions of synonymous substitutions per site (Ks) within a genome, or “Ks plots.” For example, WGDs can be detected from Ks plots by using univariate mixture models to identify peaks in Ks distributions. We performed gene family simulation experiments to evaluate the effects of different Ks estimation methods and mixture models on our ability to detect ancient WGDs from Ks plots. The simulation experiments, which accounted for variation in substitution rates and gene duplication and loss rates across gene families, tested the effects of WGD age and gene retention rates following WGD on inferring WGDs from Ks plots. Our simulations reveal limitations of Ks plot analyses. Strict interpretations of mixture model analyses often overestimate the number of WGD events, and Ks plot analyses typically fail to detect WGDs when ≤10% of the duplicated genes are retained following the WGD. However, WGDs can accurately be characterized over an intermediate range of Ks. The simulation results are supported by empirical analyses of transcriptomic data, which also suggest that biases in gene retention likely affect our ability to detect ancient WGDs. Although our results indicate mixture model results should be interpreted with great caution, using node-averaged Ks estimates and applying more appropriate mixture models can improve the accuracy of detecting WGDs.

Phylogenetic results provide confidence in relationships among Ipomoeeae lineages. Divergence time estimation results provide a temporal context for diversification of morning glories. Ancestral character reconstructions support previous findings that morning glory morphology is evolutionarily labile. Taken together, our study provides strong resolution of the morning glory phylogeny, which is broadly applicable to the evolution and ecology of these fascinating species.