The Easter Egg Weevil ( Pachyrhynchus) genome reveals syntenic patterns in Coleoptera across 200 million years of evolution

Abstract

Patterns of genomic architecture across insects remain largely undocumented or decoupled from a broader phylogenetic context. For instance, it is unknown whether translocation rates differ between insect orders. We address broad scale patterns of genome architecture across Insecta by examining synteny in a phylogenetic framework from open-source insect genomes. To accomplish this, we add a chromosome level genome to a crucial lineage, Coleoptera. Our assembly of the Pachyrhynchus sulphureomaculatus genome is the first chromosome scale genome for the hyperdiverse Phytophaga lineage and currently the largest insect genome assembled to this scale. The genome is significantly larger than those of other weevils, and this increase in size is caused by repetitive elements. Our results also indicate that, among beetles, there are instances of long-lasting (>200 Ma) localization of genes to a particular chromosome with few translocation events. While some chromosomes have a paucity of translocations, intra-chromosomal synteny was almost absent, with gene order thoroughly shuffled along a chromosome. This large amount of reshuffling within chromosomes with few inter-chromosomal events contrasts with patterns seen in mammals in which the chromosomes tend to exchange larger blocks of material more readily. To place our findings in an evolutionary context, we compared syntenic patterns across Insecta in a phylogenetic framework. For the first time, we find that synteny decays at an exponential rate relative to phylogenetic distance. Additionally, there are significant differences in decay rates between insect orders, this pattern was not driven by Lepidoptera alone which has a substantially different rate.

Author summary

Patterns of genomic architecture across insects remain largely undocumented or decoupled from a broader evolutionary context. For instance, it is unknown whether rates of gene order decay differ between insect orders. We address broad scale patterns of genome architecture across Insecta by examining synteny (shared gene order) in a phylogenetic framework from open-source insect genomes (143 complete chromosome assemblies in total). To accomplish this, we add a chromosome level genome to a crucial lineage, Coleoptera (beetles). Our assembly of the Easter Egg Weevil Pachyrhynchus sulphureomaculatus genome is the first chromosome scale genome for the hyperdiverse Phytophaga lineage and currently the largest insect genome assembled to this scale. We are the first to identify in beetles that genes stay localized on chromosomes for hundreds of millions of years, while their order along chromosomes gets completely shuffled over time. We are also the first to empirically demonstrate that synteny decay rates different significantly between insect orders and that this pattern in not driven solely by Lepidoptera (moths and butterflies), which has a substantially different rate.