High‐quality genomes reveal significant genetic divergence and cryptic speciation in the model organism Folsomia candida (collembola)

Abstract

The collembolan Folsomia candida Willem, 1902, is widely distributed throughout the world and has been frequently used as a test organism in soil ecology and ecotoxicology studies. However, it is questioned as an ideal “standard” because of differences in reproductive modes and cryptic genetic diversity between strains from various geographical origins. In this study, we obtained two high‐quality chromosome‐level genomes of F. candida, for a parthenogenetic strain (named FCDK, 219.08 Mb, 25,139 protein‐coding genes) and a sexual strain (named FCSH, 153.09 Mb, 21,609 protein‐coding genes), reannotated the genome of the parthenogenetic strain reported by Faddeeva‐Vakhrusheva et al. in 2017 (named FCBL, 221.7 Mb, 25,980 protein‐coding genes) and conducted comparative genomic analyses of the three strains. High genome similarities between FCDK and FCBL based on synteny, genome architecture, mitochondrial and nuclear gene sequences suggest that they are conspecific. The seven chromosomes of FCDK are each 25%–54% larger than the corresponding chromosomes of FCSH, showing obvious repetitive element expansions and large‐scale inversions and translocations but no whole‐genome duplication. The strain‐specific genes, expanded gene families and genes in nonsyntenic chromosomal regions identified in FCDK are highly related to the broader environmental adaptation of parthenogenetic strains. In addition, FCDK has fewer strain‐specific microRNAs than FCSH, and their mitochondrial and nuclear genes have diverged greatly. In conclusion, FCDK/FCBL and FCSH have accumulated independent genetic changes and evolved into distinct species after 10 million years ago. Our work provides important genomic resources for studying the mechanisms of rapidly cryptic speciation and soil arthropod adaptation to soil ecosystems.

The functional evolution of collembolan Ubx on the regulation of abdominal appendage formation

“…According to previously reported genome assemblies (Faddeeva-Vakhrusheva et al, 2017; Luan et al, 2023), the architecture of the Hox cluster in F. candida exhibits genomic rearrangement, with Scr , Antp and Ubx inserted into the anterior region of the complex. This organization showed that the Hox genes lack spatial collinearity (Figure 3A) (Faddeeva-Vakhrusheva et al, 2017).…”

Genomic insights into the chromosomal elongation in a family of Collembola

“…BRAKER trained Augustus v. 3.3.4 [46] and GeneMark-ES/ET/EP 4.68_lic [47] integrating evidence from the OrthoDB10 v.1 database [48]. GeMoMa with parameters 'GeMoMa.c = 0.3 GeMoMa.p = 12 00 utilized eight species (Daphnia magna (GCF_003990815.1) [49], Cloeon dipterum (GCA_902829235.1) [50], Zootermopsis nevadensis (GCF_000696155.1) [51], Drosophila melanogaster (GCF_000001215.4) [52], Rhopalosiphum maidis (GCF_003676215.2) [53], Tribolium castaneum (GCF_ 000002335.3) [54], Sinella curviseta (https://doi.org/10.6084/m9.figshare.24635850) and FCSH (GCA_020923455.1)) [7] as the protein homology-based reference. RNA-seq alignments were produced using HISAT2 v. 2.2.0 [55].…”

“…These studies use chromosome-banding techniques to provide important insights into chromosome number and size characteristics [3][4][5]. Previous research has revealed that chromosome numbers in collembolan species vary between 5 and 11, and this observation is also supported by publicly available genomic data [3][4][5][6][7][8]. Furthermore, Collembola exhibit significant variations in chromosome size among different species.…”

“…Furthermore, Collembola exhibit significant variations in chromosome size among different species. Most species demonstrate a relatively consistent distribution of chromosome lengths, with the longest chromosome comprising approximately one-fifth of the total genome length [7,8] (electronic supplementary material, table S1). However, the early study on collembolan karyotypes identified an exceptionally large chromosome in the species Tomocerus minor (Tomoceridae) [3].…”

“…TEs replicate and insert themselves into new locations within the chromosome, resulting in an increase in the chromosome length. Previous research published two chromosome-level genomes of Folsomia candida , a parthenogenetic strain (FCDK, 219.08 Mb) and a sexual strain (FCSH, 153.09 Mb), and found that the seven chromosomes of FCDK are 25%–54% larger than their corresponding chromosomes in FCSH due to transposable element proliferation [7].…”