The B chromosome of Pseudococcus viburni: a selfish chromosome that exploits whole-genome meiotic drive

Abstract

Meiosis, the key process underlying sexual reproduction, is generally a fair process: each chromosome has a 50% chance of being included into each gamete. However in some organisms meiosis has become highly aberrant with some chromosomes having a higher chance of making it into gametes than others. Yet why and how such systems evolve remains unclear. Here we study the unusual reproductive genetics of mealybugs, in which only maternal-origin chromosomes are included into the gametes during male meiosis, while paternally-derived chromosomes degrade. This whole genome meiotic drive occurs in all males and is evolutionarily conserved. However one species - the obscure mealybug Pseudococcus viburni - has a segregating B chromosome that increases in frequency by escaping paternal genome elimination. Here we present whole-genome and gene expression data from laboratory lines with and without B chromosomes. These data allow us to identify B-linked sequences including >70 protein-coding genes as well as a B-specific satellite repeat that makes up a significant proportion of the chromosome. We also used these data to investigate the evolutionary origin of the B chromosome. The few paralogs between the B and the core genome are distributed throughout the genome, showing that it is unlikely that the B originated through a simple duplication of one of the autosomes. We also find that while many of the B-linked genes do not have paralogs within the P.viburni genome, but they do show orthology with genes in other hemipteran insects suggesting that the B might have originated from fission of one of the autosomes, possibly followed by further translocations of individual genes. Finally in order to understand the mechanisms by which the B is able to escape elimination when paternally-derived we generated gene expression data for males and females with and without B chromosomes. We find that at the developmental stage when meiosis is taking place only a small number of B-linked genes show significant expression. Only one gene was significantly over-expressed during male meiosis, which is when the drive occurs: a acetyltransferase involved in H3K56Ac, which has a putative role in meiosis and is therefore a promising candidate for further studies. Together, these results form a promising foundation for studying the mechanisms of meiotic drive in a system that is uniquely suited for this approach.

Retention of an endosymbiont for the production of a single molecule

“…We used mealybugs from a colony reared to study the transmission of a selfish B chromosome (Vea et al, 2021). In brief, we initially obtained mealybugs from a glass house in the Royal Botanic Gardens of Edinburgh in Scotland; from these insects, we established a laboratory colony fed on sprouting potatoes at 25C on a 16hr light/8 hr dark cycle.…”

“…Illumina and PacBio sequence reads were obtained from and processed as described in Vea et al, 2021. Illumina reads were quality trimmed using Trimmomatic v0.36 (minimum length=36 bp, sliding window=4 bp, minimum quality score=15 [ILLUMINACLIP:TruSeq3-PE:2:30:10 LEADING:3 TRAILING:3 SLID-INGWINDOW:4:15 MINLEN:36]) (Bolger et al, 2014). PacBio and Illumina reads were then assembled using Canu v1.6 (default parameters; Koren et al, 2017), resulting in 2,787 contigs and 440,161,839 bases.…”

Did the creeping vole sex chromosomes evolve through a cascade of adaptive responses to a selfish x chromosome?

“…In general, the possibility that atypical genetic systems could arise due to countermeasures to the action of selfish alleles is deserving of more detailed attention and building of explicit stepwise models. [11,[22][23][64][65][66]…”

B Chromosomes in Psalidodon scabripinnis (Characiformes, Characidae) Species Complex

“…In recent years, knowledge of B chromosomes has increased significantly with the application of powerful high-resolution technologies, such as third- and fourth-generation DNA and RNA sequencing. The recently discovered fascinating aspects of B chromosomes include the presence of an epistatically Y-dominant female sex determinant gene in cichlids [ 28 ]; the elimination of B chromosomes only in the roots of Aegilops speltoides during the embryonic stage [ 29 ]; the presence of a gene acquired by interspecific hybridization called haploidizer in Nasonia vitripennis , which causes the sexual conversion of females into males by expelling the entire genome coming from the sperm [ 26 ]; the paternal inheritance and escape of the B chromosome from elimination in male meiosis in mealybugs, in which the entire paternal genome is eliminated during gamete formation [ 30 ].…”