Long-read based assembly and synteny analysis of a reference Drosophila subobscura genome reveals signatures of structural evolution driven by inversions recombination-suppression effects

Abstract

BackgroundDrosophila subobscura has long been a central model in evolutionary genetics. Presently, its use is hindered by the lack of a reference genome. To bridge this gap, here we used PacBio long-read technology, together with the available wealth of genetic marker information, to assemble and annotate a high-quality nuclear and complete mitochondrial genome for the species. With the obtained assembly, we performed the first synteny analysis of genome structure evolution in the subobscura subgroup.ResultsWe generated a highly-contiguous ~ 129 Mb-long nuclear genome, consisting of six pseudochromosomes corresponding to the six chromosomes of a female haploid set, and a complete 15,764 bp-long mitogenome, and provide an account of their numbers and distributions of codifying and repetitive content. All 12 identified paracentric inversion differences in the subobscura subgroup would have originated by chromosomal breakage and repair, with some associated duplications, but no evidence of direct gene disruptions by the breakpoints. Between lineages, inversion fixation rates were 10 times higher in continental D. subobscura than in the two small oceanic-island endemics D. guanche and D. madeirensis. Within D. subobscura, we found contrasting ratios of chromosomal divergence to polymorphism between the A sex chromosome and the autosomes.ConclusionsWe present the first high-quality, long-read sequencing of a D. subobscura genome. Our findings generally support genome structure evolution in this species being driven indirectly, through the inversions’ recombination-suppression effects in maintaining sets of adaptive alleles together in the face of gene flow. The resources developed will serve to further establish the subobscura subgroup as model for comparative genomics and evolutionary indicator of global change.Electronic supplementary materialThe online version of this article (10.1186/s12864-019-5590-8) contains supplementary material, which is available to authorized users.

Dynamic turnover of centromeres drives karyotype evolution in Drosophila

“…2). Genome--wide alignments between our D. subobscura assembly and a recently published high-quality genome confirm our inference of pericentromeric DNA (Puerma et al 2018;Karageorgiou et al 2019) and verify the orientation of the chromosomes (Fig. S4).…”

“…Our annotations identified 12,714 protein--coding genes in D. subobscura, 13,665 in D. athabasca, 14,547 in D. lowei, and 14,334 in D. pseudoobscura. The number of annotated genes in D. subobscura is very similar to the 13,317 protein--coding genes in another assembly of D. subobscura (Karageorgiou et al 2019) and the 13,453 genes of its close relative D. guanche (Puerma et al 2018). Further, the number of annotated genes in D. pseudoobscura and D. lowei (Table S4) are similar to the number in the current version of D. pseudoobscura (14,574 genes in Dpse_3.0).…”

“…S3). BUSCO (Benchmarking Universal Single--Copy Orthologs) scores reveal that our genomes are highly complete (Table S3) and match or exceed other recently published high quality Drosophila genomes (Mahajan et al 2018;Puerma et al 2018;Miller et al 2018;Karageorgiou et al 2019). Identification of D. melanogaster orthologs in our genome assemblies allowed us to unambiguously assign each chromosome to a Muller element ( Fig.…”

“…2). A lower cut--off was used for D. subobscura, as this species has a very small, compact and repeat--poor genome (see also Karageorgiou et al 2019). The sizes of (peri)centromere regions recovered for each chromosome and species vary considerably ( Table 1).…”

Basal hsp70 expression levels do not explain adaptive variation of the warm- and cold-climate O3 + 4 + 7 and OST gene arrangements of Drosophila subobscura

“…Using the recently assembled genome of D. subobscura [41] we have estimated that the hsp70 loci are around 0.8 Mb from the closest O 4 distal breakpoint and likely too far away as to be directly affected by this breakpoint, an inference that is in agreement with the similar RNA amounts found in the two chromosomal arrangements analysed here. Four genes (Pxd, Set 8, CG5225 and Acf) are located near O 4 inversion breakpoints [42], but at present we do not know whether potential position effects affecting these genes play any role in the in the adaptive value of this inversion.…”