338 coleopteran genomes reveal exceptional rearrangement variation compared to other insect orders

Key results

1. ShownBeetles descend from eight ancestral linkage groups (C1 to C7 plus the sex-linked CX). Early fissions on the Adephaga and Polyphaga stems mean that no extant genome in the dataset keeps the ancestral configuration.

   3,603 of 3,729 BUSCO genes (approximately 97%) were assigned to C1–C7 and CX, with co-assignment blocks recovered across 10,000 Syngraph bootstrap replicates. A stem-Polyphaga fission of C1 gives nine ALGs, still retained in 15 species. Nine fissions on the Adephaga stem produced 17 linkage groups. · Eight ancestral linkage groups reveal deep…; Ancient fissions and divergent rearrangement…; Inferring ancestral linkage groups

2. ShownThe common 10- and 11-chromosome karyotypes are convergent endpoints that arose at least 65 times, mostly via fissions of a few large ALGs. Models favour optima near n = 10–11; n = 10 arises more often than expected and persists once reached, but transitions show no universal pull toward it.

   n = 10 arose at least 36 times (101 species), 17 of them by one fission of the polyphagan configuration (C2 in 15); n = 11 arose 29 times. Moves toward vs away from n = 10: 91 vs 134 (p = 0.998). Origins: 31 vs a simulated median of 19 [11–29], p = 0.0136. Exit rate 19.0% vs 43.0%, Fisher p = 3.0 × 10^-10. · Ancient fissions and divergent rearrangement…; Phylogenetic tests of chromosome-number…

3. SuggestedRearrangement tempo differs greatly among beetle lineages. Clades with larger increases in rearrangement rate tend to show larger increases in diversification rate. Beetles also keep more persistent rearrangements than flies or moths.

   33% of species show at most three rearrangements, while at least 21 lineages (41% of species) exceed ten. Clade rate ratios span 0.08–18.17-fold, with seven strongly accelerated clades including Phytophaga and Chrysomelidae. Log rearrangement-rate ratio vs log diversification-rate ratio: PGLS β = 0.0373, t = 2.56, p = 0.0145. · Highly variable tempo of chromosome evolution…; Chromosomal rearrangement bursts coincide with…; Contrasting modes of genome structure evolution…; Testing association of rearrangement rates and…

4. ShownChromosome size, satellite repeats and centromere position predict autosomal rearrangement. Small chromosomes tend to fuse and large ones to split, and recent fissions yield acrocentric chromosomes, consistent with Robertsonian mechanisms.

   Versus non-rearranged chromosomes, fusing ones were 2.26× smaller and splitting ones 1.65× larger; splitting ones were 3.73× the size of fusion partners (mixed model F = 2947, p < 2.2 × 10^-16). Satellite enrichment near breakpoints (100-kb windows): 2.30-fold for fusions, 2.69-fold for fissions, p < 0.01. Centromere position (157 genomes): 0.126 after recent fission vs 0.326–0.420. · Chromosome size and centromere architecture…; Analysing potential constraints in chromosomal…; Analysing potential constraints in chromosomal…; Analysing potential constraints in chromosomal…

5. ShownThe ancestral beetle X (CX) is highly conserved. Its changes are mostly recent X-autosome fusions concentrated on terminal branches, and CX fuses less often than its size predicts. Partial homology with the fly sex-linked ALG D6 supports a holometabolan ancestral X.

   Of 147 species with identified sex chromosomes, 116 retain CX as the X and 31 carry 25 independent neo-X cases. There is one true turnover (Aleochara curtula). CX fusion odds ratio 0.23 [0.15–0.36], p = 3.97 × 10^-13. Only eight of 55 X-related transitions are shared by two or more species. · Sex chromosome changes in Coleoptera; Deep conservation of the ancestral holometabolan…; Identifying changes and constraints of sex…