Cold Fusion: Massive Karyotype Evolution in the Antarctic Bullhead NotothenNotothenia coriiceps

Abstract

Half of all vertebrate species share a series of chromosome fusions that preceded the teleost genome duplication (TGD), but we do not understand the causative evolutionary mechanisms. The “Robertsonian-translocation hypothesis” suggests a regular fusion of each ancestral acro- or telocentric chromosome to just one other by centromere fusions, thus halving the karyotype. An alternative “genome-stirring hypothesis” posits haphazard and repeated fusions, inversions, and reciprocal and nonreciprocal translocations. To study large-scale karyotype reduction, we investigated the decrease of chromosome numbers in Antarctic notothenioid fish. Most notothenioids have 24 haploid chromosomes, but bullhead notothen (Notothenia coriiceps) has 11. To understand mechanisms, we made a RAD-tag meiotic map with ∼10,000 polymorphic markers. Comparative genomics aligned about a thousand orthologs of platyfish and stickleback genes along bullhead chromosomes. Results revealed that 9 of 11 bullhead chromosomes arose by fusion of just two ancestral chromosomes and two others by fusion of three ancestral chromosomes. All markers from each ancestral chromosome remained contiguous, implying no inversions across fusion borders. Karyotype comparisons support a history of: (1) Robertsonian fusions of 22 ancestral chromosomes in pairs to yield 11 fused plus two small unfused chromosomes, like N. angustata; (2) fusion of one of the remaining two ancestral chromosomes to a preexisting fused pair, giving 12 chromosomes like N. rossii; and (3) fusion of the remaining ancestral chromosome to another fused pair, giving 11 chromosomes in N. coriiceps. These results raise the question of what selective forces promoted the systematic fusion of chromosomes in pairs and the suppression of pericentric inversions in this lineage, and provide a model for chromosome fusions in stem teleosts.

Highly dense linkage maps from 31 full-sibling families of turbot (Scophthalmus maximus) provide insights into recombination patterns and chromosome rearrangements throughout a newly refined genome assembly

“… 76 It would be worth investigating in more detail if the high number of chromosome fusions occurring in the families with lower diploid numbers (e.g. Soleidae, Bothidae and Achiridae and some Paralichthydae) show a preferential fusion pattern, similar to what recently found in notothenioids 77 . In addition to chromosome fusions, other minor reorganizations between non-orthologous chromosomes of turbot, Japanese flounder and half-smooth tongue sole were identified in our study.…”

“…In addition to chromosome fusions, other minor reorganizations between non-orthologous chromosomes of turbot, Japanese flounder and half-smooth tongue sole were identified in our study. These chromosome rearrangements are thought to be important in karyotypic evolution and species differentiation, 77–79 and thus, further comparative mapping studies are encouraged to understand the reasons behind these rearrangements in the evolution of flatfish.…”

Chromonomer: a tool set for repairing and enhancing assembled genomes through integration of genetic maps and conserved synteny

“…While the ancestral haploid chromosome number in teleost fish is 24 or 25 (Naruse 2004), the black rockcod has just 11 chromosomes (V. P. Prirodina, A. V. Neyelov 1984). Using an outcrossed RADseq-based genetic map constructed from 244 progeny in an F1 pseudo-testcross with 9,138 mappable markers, Amores et al (2017) were able both to confirm this genome evolution occurred by end-to-end fusions and to identify which ancestral chromosomes became fused. The rockcod physical genome was also assembled using a hybrid strategy that mixed data from Illumina paired-end libraries, from 454-sequenced mate-pair libraries, and from limited PacBio RS II sequencing.…”

“…assembly (NCBI accession GCA_000735185.1, BioProject PRJNA66471) was created by (Shin et al 2014) from PacBio RSII, Illumina HiSeq, and 454 GLX II data using the Celera assembler (Myers 2000), and gaps were filled and extended using the PacBio data with PBJelly (English et al 2012). We employed the genetic map from (Amores et al 2017) of 244 F1 progeny, with markers generated by RADseq and assembled with Stacks (Catchen et al 2011). We aligned the markers against the black rockcod genome using BWA mem (Li 2013), used a custom script to translate scaffold and contig names in the NCBI GFF file to match the names in the NCBI FASTA and AGP genome description files.…”

Simulation with RADinitio Improves RADseq Experimental Design and Sheds Light on Sources of Missing Data

“…This family of protocols, referred hereafter as RADseq, while displaying individual benefits and disadvantages, have been designed for specific experimental contexts, and are a testament of the applicability of the general molecular approach. Independent of the specific molecular protocol used, RADseq has proven to be a versatile technique in a variety of genomics contexts, including the generation of linkage maps (Amores, Catchen, Ferrara, Fontenot, & Postlethwait, 2011;Amores, Wilson, Allard, Detrich, & Postlethwait, 2017;Small et al, 2016), de novo population genomics (Jeffery et al, 2017;Portnoy et al, 2015), landscape genomics (Bay et al, 2018;Dudaniec, Yong, Lancaster, Svensson, & Hansson, 2018), reference-based genome scans (Bassham, Catchen, Lescak, von Hippel, & Cresko, 2018), and phylogenomics/phylogeography (Cristofari et al, 2016;Razkin et al, 2016;Suchan et al, 2017).…”