Satellite DNAs Unveil Clues about the Ancestry and Composition of B Chromosomes in Three Grasshopper Species

Abstract

Supernumerary (B) chromosomes are dispensable genomic elements occurring frequently among grasshoppers. Most B chromosomes are enriched with repetitive DNAs, including satellite DNAs (satDNAs) that could be implicated in their evolution. Although studied in some species, the specific ancestry of B chromosomes is difficult to ascertain and it was determined in only a few examples. Here we used bioinformatics and cytogenetics to characterize the composition and putative ancestry of B chromosomes in three grasshopper species, Rhammatocerus brasiliensis, Schistocerca rubiginosa, and Xyleus discoideus angulatus. Using the RepeatExplorer pipeline we searched for the most abundant satDNAs in Illumina sequenced reads, and then we generated probes used in fluorescent in situ hybridization (FISH) to determine chromosomal position. We used this information to infer ancestry and the events that likely occurred at the origin of B chromosomes. We found twelve, nine, and eighteen satDNA families in the genomes of R. brasiliensis, S. rubiginosa, and X. d. angulatus, respectively. Some satDNAs revealed clustered organization on A and B chromosomes varying in number of sites and position along chromosomes. We did not find specific satDNA occurring in the B chromosome. The satDNAs shared among A and B chromosomes support the idea of putative intraspecific ancestry from small autosomes in the three species, i.e., pair S11 in R. brasiliensis, pair S9 in S. rubiginosa, and pair S10 in X. d. angulatus. The possibility of involvement of other chromosomal pairs in B chromosome origin is also hypothesized. Finally, we discussed particular aspects in composition, origin, and evolution of the B chromosome for each species.

Satellitome Analysis in the Ladybird Beetle Hippodamia variegata (Coleoptera, Coccinellidae)

“…Nevertheless, the satDNA of M. macrocephalus only represented 13.47% (female) and 11.99% (male) of the genome [61]. Therefore, the existence of multiple satDNA families seems to be a common characteristic of eukaryotic genomes as they have also been found in plants and vertebrates [61][62][63].…”

Too much too many: comparative analysis of morabine grasshopper genomes reveals highly abundant transposable elements and rapidly proliferating satellite DNA repeats

“…The non-coding satDNAs have been traditionally viewed as mostly useless material capable of accumulating primarily in heterochromatin [11][12][13]27,29] until they become a too heavy load for the host genome (reviewed in [45]). It will be interesting to test whether the differential amplification of satDNAs is correlated with the amount of heterochromatin.…”

“…Another type of repetitive element widely distributed in eukaryotic genomes is satDNA. It consists of non-coding repetitive DNA that is tandemly arranged and largely represented in the centromeric and pericentromeric heterochromatin of most eukaryotic genomes [11][12][13]. satDNA evolution is influenced by several mechanisms of non-reciprocal genetic exchange such as unequal crossing-over, intra-strand homologous recombination, gene conversion, rolling-circle replication and transposition [11,[14][15][16][17].…”

“…Sequence divergence as the outcome of reproductive isolation might then lead to a formation of species-specific profiles of satDNA sequence variants [25,26]. For grasshoppers and crickets (Orthoptera), high-throughput sequencing analyses detected 316 satDNA families in ~20 species [12,21,[27][28][29][30][31][32]. Because of the large divergence time between these Orthopteran species (73-224 millions years, Myr) [33], none of these 316 satDNA families showed interspecific homology, except for partial sequence homology within satDNAs of Gryllus cricket species [27] (unknown divergence time) and within Schistocerca grasshopper species [21] with divergence time < 8 Myr [34].…”

Evolution, Composition and Regulation of Supernumerary B Chromosomes

“…[2] use a combination of cytogenetics and bioinformatics to investigate Bs in three other grasshopper species from North and South America. Their data show the recurrent involvement of small A chromosomes, that are poor in genes and enriched in repetitive DNA, in the B chromosome origin.…”