Genomic evidence of paternal genome elimination in the globular springtailAllacma fusca

Abstract

Paternal genome elimination (PGE) - a type of reproduction in which males inherit but fail to pass on their father’s genome - evolved independently in six to eight arthropod clades. Thousands of species, including several important for agriculture, reproduce via this mode of reproduction. While PGE is well established in some of the clades, the evidence in globular springtails (Symphypleona) remains elusive, even though they represent the oldest and most species rich clade putatively reproducing via PGE. We sequenced genomic DNA from whole bodies of Allacma fusca males with high fractions (>27.5%) of sperm to conclusively confirm that all the sperm carry one parental haplotype only. Although it is suggestive that the single haplotype present in sperm is maternally inherited, definitive genetic proof of the parent of origin is still needed. The genomic approach we developed allows for detection of genotypic differences between germline and soma in all species with sufficiently high fraction of germline in their bodies. This opens new opportunities for scans of reproductive modes in small organisms.

The X chromosome of insects predates the origin of Class Insecta

“…We then downloaded RNA-seq reads for both species, as neither genome had gene annotations, and constructed transcriptome assemblies to use in downstream analyses. The A. fusca annotation has two X chromosomes, X1 and X2 (Jaron et al 2022). In contrast, no information is available as to what chromosome is the X in S. curviseta.…”

“…Additionally, we downloaded chromosome-level assemblies of the common yellow sally (Insecta: Plecoptera), Isoperla grammatica (McSwan et al 2023), and two springtails (Entognatha: Collembola), Sinella curviseta (Zhang et al 2019) and Allacma fusca (Jaron et al 2022), all of which lack accompanying gene annotations. We therefore downloaded RNAsequencing reads from the SRA (Sequence Read Archive) on NCBI (Table S1) in order to construct gene annotations for these species.…”

The genome sequence of the springtail Allacma fusca (Linnaeus, 1758)

“…The cell with two missing chromosomes will immediately degenerate, while the cell with the complete haploid set will undergo the rest of meiosis and form two spermatozoa ( Dallai et al , 2000 ). The sperm contains one parental haplotype only ( Jaron et al , 2022 ). It is hypothesised that the retained genome is of maternal origin, therefore A. fusca more likely reproduces via so-called paternal genome elimination ( Jaron et al , 2022 ).…”

“…The sperm contains one parental haplotype only ( Jaron et al , 2022 ). It is hypothesised that the retained genome is of maternal origin, therefore A. fusca more likely reproduces via so-called paternal genome elimination ( Jaron et al , 2022 ). A similar type of spermatogenesis is found across at least five globular springtail families ( Dallai et al , 1999 ; Dallai et al , 2000 ; Dallai et al , 2001 ; Dallai et al , 2004 ), and therefore paternal genome elimination is thought to be ancestral to all globular springtails (Symphypleona).…”