Nat Ecol Evol. 2024 Aug;8(8):1505-1521. doi:10.1038/s41559-024-02456-y

Elise Parey, Olga Ortega-Martinez, Jérôme Delroisse, Laura Piovani, Anna Czarkwiani, David Dylus, Srishti Arya, Samuel Dupont, Michael Thorndyke, Tomas Larsson, Kerstin Johannesson, Katherine M. Buckley, Pedro Martinez, Paola Oliveri, Ferdinand Marlétaz

The brittle star genome illuminates the genetic basis of animal appendage regeneration

“We showed that the ‘Eleutherozoa Linkage Groups’ descend from a single fusion of ancestral bilaterian linkages (B2+C2).” “Interestingly, sea cucumbers have the lowest rate of inter-chromosomal rearrangements, yet the most derived echinoderm body plan (Rahman et al. 2019), which highlights the uncoupling of global genomic rearrangements from morphological evolution.” “In contrast with its sea star sister-group, the A. filiformis genome is highly rearranged: our analyses identified 26 inter-chromosomal rearrangements since the Eleutherozoa ancestor.”

Thomas D. Lewin, Isabel Jiah-Yih Liao, Yi-Jyun Luo

bioRxiv 2024.05.15.594353 doi:10.1101/2024.05.15.594353

Annelid comparative genomics and the evolution of massive lineage-specific genome rearrangement in bilaterians

“the last annelid common ancestor retained the ancestral lophotrochozoan karyotype with 20 chromosomes“ “The genomes of all sampled species have at least three ALG fusions compared to the ancestral annelid genome.” “almost all the chromosome fusion events in annelids can be categorized as fusion-with-mixing” “we found no correlation between the ALG fusion rate and the length of chromosomes” “In contrast to fusions, the splitting of ALGs is relatively rare, with only three cases in this dataset of 16 annelid species.” “in both leeches and earthworms, there is complete shuffling of the ancient bilaterian genome [...] there has also been massive genome shuffling between these two groups.“ “within the Clitellata, M. vulgaris has a lineage-specific tetraploidization that is not shared by other earthworms or leeches” “we developed a macrosynteny rearrangement index [...] to quantify both ALG fusion and fission into a single value between 0 (no rearrangement) and 1 (maximum rearrangement).” “dramatic genome rearrangement in clitellates correlates with the evolution of a new ecological niche, alongside divergent genomic location and altered expression of key developmental genes”

Wright CJ, Stevens L, Mackintosh A, Lawniczak M, Blaxter M.

Comparative genomics reveals the dynamics of chromosome evolution in Lepidoptera.

Nat Ecol Evol. 2024 Feb 21. doi:10.1038/s41559-024-02329-4

“We assigned 4,112 orthologues (78%) to 32 ALGs: 31 autosomes and Z, the sex chromosome. Hereafter, we refer to these ALGs as Merian elements, named after the seventeenth-century lepidopterist and botanical artist, Maria Sibylla Merian” ”Merian elements have remained intact in most species” “Lepidopteran chromosomes arising from fusions retain syntenic domains that reflect the original elements. Remarkably, this includes the M17 + M20 fusion, which occurred ~200 million years ago”

Thomas D. Lewin, Isabel Jiah-Yih Liao, Mu-En Chen, John D. D. Bishop, Peter W. H. Holland, Yi-Jyun Luo

bioRxiv 2024.02.15.580425; doi:10.1101/2024.02.15.580425

Fusion, fission, and scrambling of the bilaterian genome in Bryozoa.

Defines a “microsynteny mixing score” as 1 minus the absolute value of the spearman correlation coefficient of the ranked positions of orthologous genes on orthologous chromosome pairs.

Jia SL, Zhang M, Liu GL, Chi ZM, Chi Z.

Funct Integr Genomics. 2023 Jun 19;23(3):206. doi:10.1007/s10142-023-01127-8

Novel chromosomes and genomes provide new insights into evolution and adaptation of the whole genome duplicated yeast-like fungus TN3-1 isolated from natural honey.

A new Aureobasidium melanogenum strain that has two subgenomes that diverged ~10 million years ago.

Chromosome-level genome assemblies of Cutaneotrichosporon spp. (Trichosporonales, Basidiomycota) reveal imbalanced evolution between nucleotide sequences and chromosome synteny.

BMC Genomics. 2023 Oct 11;24(1):609. doi:10.1186/s12864-023-09718-2.

Kobayashi Y, Kayamori A, Aoki K, Shiwa Y, Matsutani M, Fujita N, Sugita T, Iwasaki W, Tanaka N, Takashima M.

Cutaneotrichosporon cavernicola sister species with same karyotype, ITS sequence similarity above the usual threshold for species boundaries, but scrambling of large-width regions. “If [mating infertility caused by genome rearrangement] is universal, chromosome synteny should be considered the determinant of biological species”

Yin Y, Fan H, Zhou B, Hu Y, Fan G, Wang J, Zhou F, Nie W, Zhang C, Liu L, Zhong Z, Zhu W, Liu G, Lin Z, Liu C, Zhou J, Huang G, Li Z, Yu J, Zhang Y, Yang Y, Zhuo B, Zhang B, Chang J, Qian H, Peng Y, Chen X, Chen L, Li Z, Zhou Q, Wang W, Wei F.

Nat Commun. 2021 Nov 25;12(1):6858. doi:10.1038/s41467-021-27091-0

Molecular mechanisms and topological consequences of drastic chromosomal rearrangements of muntjac deer

“we identified the rapidly evolving genes (REGs) and positively selected genes (PSGs) in the M. crinifrons, M. gongshanensis, and M. muntjak vaginalis with large fused chromosomes, as well in their common ancestor node. The results showed that the PSGs and REGs in these lineages are enriched in GOs and pathways related to the maintenance of genomic stability.” “the occurrence/frequency of genomic rearrangements (>10 kb) of M. crinifrons and M. gongshanensis (3.06~3.89 events/Mb) are not significantly higher than those in M. reevesi, E. davidianus, and C. albirostris (3.11~4.56 events/Mb)”

Schultz DT, Haddock SHD, Bredeson JV, Green RE, Simakov O, Rokhsar DS.

Nature. 2023 May 17. doi:10.1038/s41586-023-05936-6

Ancient gene linkages support ctenophores as sister to other animals.

Gene linkages found in all metazoans and single-celled outgroups are irreversibly merged (fusion followed by mixing) in Porifera, Cnidaria and Bilateria, supporting the idea that Ctenophora are sister to them.

Damas J, Corbo M, Kim J, Turner-Maier J, Farré M, Larkin DM, Ryder OA, Steiner C, Houck ML, Hall S, Shiue L, Thomas S, Swale T, Daly M, Korlach J, Uliano-Silva M, Mazzoni CJ, Birren BW, Genereux DP, Johnson J, Lindblad-Toh K, Karlsson EK, Nweeia MT, Johnson RN; Zoonomia Consortium; Lewin HA.

Proc Natl Acad Sci U S A. 2022 Oct 4;119(40):e2209139119. doi: 10.1073/pnas.2209139119

Evolution of the ancestral mammalian karyotype and syntenic regions.

Analyses the number of breakpoints between nodes of the phylogenetic tree, thanks to ancestral genome reconstruction. “2 extant mammals (Dataset S1), representing all 19 eutherian, 3 marsupial, and the monotreme orders, were used to reconstruct ancestral karyotypes at 16 nodes of the mammalian phylogeny” “We used DESCHRAMBLER to generate reconstructed ancestral chromosome fragments (RACFs) for each of 16 mammalian ancestors at 300-kbp syntenic fragment (SF) resolution” “The reconstructed mammalian ancestor karyotype has 19 autosomes plus X, except for the cattle genome-based reconstruction, which has two fewer chromosomes and the lowest total reconstruction length” “The differences between the mammalian and therian (n = 17 + X) ancestors’ chromosomes resulted from 96 chromosomal rearrangements over 18 My.” “The eutherian ancestor (n = 19 + X) is the most recent common ancestor of the three lineages represented by the reference genomes. Its karyotype evolved from that of the therian ancestor as a result of 124 chromosomal rearrangements over 53 My.” “We identified 323, 262, and 257 EBRs that occurred along the lineage from the mammalian ancestor to the human, sloth, and cattle genomes, respectively” “Inversions were most frequent, accounting for 76 to 85% of all rearrangements identified for each lineage” “The highest number of interchromosomal rearrangements (i.e., fissions and fusions) was observed on the branch from the therian to the eutherian ancestor (n = 30)” “We observed that 9 of 14 small MAMs have 1:1 orthology to chicken chromosomes (GGA) and reconstructed chromosomes of the avian and amniote ancestors” “EBRs were found to have a significantly higher density of repeats”

Li Y, Liu H, Steenwyk JL, LaBella AL, Harrison MC, Groenewald M, Zhou X, Shen XX, Zhao T, Hittinger CT, Rokas A.

Curr Biol. 2022 Dec 19;32(24):5335-5343.e4. doi:10.1016/j.cub.2022.10.025

Contrasting modes of macro and microsynteny evolution in a eukaryotic subphylum.

“conservation index is calculated by counting the number of one-to-one orthologous gene pairs whose genes are in homologous chromosomes/scaffolds and dividing it by the number of one-to-one orthologs whose genes reside in non-homologous chromosomes/scaffolds” “we found a faster decay of macrosynteny conservation compared with filamentous fungi and animals, which is corroborated by findings of rapid chromosome structure evolution in budding yeasts” “at the small-scale gene-level of organization, we identified both deeply conserved and lineage-specific instances of conservation of microsynteny across budding yeast genomes.”

Housworth EA, Postlethwait J

Genetics. 2002 Sep;162(1):441-8. doi:10.1093/genetics/162.1.441

Measures of synteny conservation between species pairs.

Introduces a syntenic correlation measure, ρ, which is a scaled chi-square statistic, and an alternative measure λ with measures “the proportion of errors made in assigning a gene to a chromosome in one species that can be eliminated by knowing which chromosome the orthologue belongs to in the other species.”

“We introduce a measure of genomic conservation, which we call syntenic correlation, which corresponds to a measure of how far the orthologues are from being independently scattered in the genomes of the two species. This measure is standardized to be between zero, for completely randomized arrangements of orthologues between the genomes, and one, for two genomes with perfect synteny conservation. Further, this measure can be used to compare genomic distances (i.e., Oxford grids) between many pairs of species.”

Ranz JM, González PM, Su RN, Bedford SJ, Abreu-Goodger C, Markow T.

Proc Biol Sci. 2022 Jan 26;289(1967):20212183. doi:10.1098/rspb.2021.2183

Multiscale analysis of the randomization limits of the chromosomal gene organization between Lepidoptera and Diptera.

Uses 5 to 7000 1-to-1 orthologues to study synteny in insects that speciated ~100 My ago. Uses a definition of microsynteny with no constrains on orientation, where transposition does not interrupt synteny, and where triplets of orthologues do not need to be in the same order. A repurposed tissue-specificity index identifies ancestral relationships between chromosomes. Searched for conserved clusters (Hox etc.) by allowing a distance of 250 kbp between genes, regardless the number of interveining genes. Found that most clusters still exist, but rearranged.

Goel M, Sun H, Jiao WB, Schneeberger K.

Genome Biol. 2019 Dec 16;20(1):277. doi:10.1186/s13059-019-1911-0

SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies.

Identifies inversions, translocations, duplications, etc., but requires that the two genomes have the same number of chromosomes and that they are oriented the same direction.

Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization.

Nat Commun. 2022 Apr 21;13(1):2172. doi:10.1038/s41467-022-29694-7

Schmidbaur H, Kawaguchi A, Clarence T, Fu X, Hoang OP, Zimmermann B, Ritschard EA, Weissenbacher A, Foster JS, Nyholm SV, Bates PA, Albertin CB, Tanaka E, Simakov O.

Defines “microsyntenic blocks as at least three or more co-occurring orthologous genes with up to five intervening genes with no constraints on their collinearity”. Found 505 microsyntenies unique to cephalopods and 275 unique to metazooans. “Genes in cephalopod-specific microsyntenies do not tend to be co-expressed, despite their tight co-localization” “In contrast [to cephalopod-specific microsyntenies], conserved metazoan microsyntenies show significant (Wilcoxon test, p ≤ 0.001) co-expression when compared to simulated microsyntenies”

Albertin CB, Medina-Ruiz S, Mitros T, Schmidbaur H, Sanchez G, Wang ZY, Grimwood J, Rosenthal JJC, Ragsdale CW, Simakov O, Rokhsar DS.

Nat Commun. 2022 May 4;13(1):2427. doi:10.1038/s41467-022-29748-w

Genome and transcriptome mechanisms driving cephalopod evolution.

Most chromosomes of Doryteuthis pealeii have a direct counterpart in Euprymna scolopes and retained visible synteny with the scallop Mizuhopecten yessoensis. In both cases, the gene order in syntenic regions is considerably scrambled.

Simakov O, Bredeson J, Berkoff K, Marletaz F, Mitros T, Schultz DT, O'Connell BL, Dear P, Martinez DE, Steele RE, Green RE, David CN, Rokhsar DS.

Sci Adv. 2022 Feb 4;8(5):eabi5884. doi:10.1126/sciadv.abi5884

Deeply conserved synteny and the evolution of metazoan chromosomes.

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Bhutkar A, Schaeffer SW, Russo SM, Xu M, Smith TF, Gelbart WM.

Genetics. 2008 Jul;179(3):1657-80. doi:10.1534/genetics.107.086108

Chromosomal rearrangement inferred from comparisons of 12 Drosophila genomes.

“This analysis reveals between 42 (D. sechellia) and 1430 (D. willistoni) syntenic blocks across various species on the basis of the D. melanogaster gene order.” “Comparison of syntenic blocks across this large genomic data set confirms that genetic elements are largely (95%) localized to the same Muller element across genus Drosophila species and paracentric inversions serve as the dominant mechanism for shuffling the order of genes along a chromosome.” “When we infer that a breakpoint is reused we mean that two or more breakage events occurred within the nucleotide interval between blocks, but the events are not necessarily coincident within the breakpoint”

Kent WJ, Baertsch R, Hinrichs A, Miller W, Haussler D.

Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11484-9. doi:10.1073/pnas.1932072100

Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes.

Primary paper for chains and nets, built with the BLASTZ and AXTCHAIN programs. Chains are one-to-many alignments and allow skipping over local inversions. In human/mouse comparisons, 2.0 inversion per Mbp, median length 814. Double gaps ≥ 100 per Mbp: 398.6, median length 411. Chains are called “short” when their span is <100,000 bases (span distribution of short chains apparently bimodal). 579 “long” chains (average length 983 kb) cover 32.9% of the bases in the human genome. Collectively all chains span 96.3% of the human genome and align to 34.6% of it. The authors note that the observed distribution of gap lengths violate the usual affine model of aligners.

“A chained alignment [is] an ordered sequence of traditional pairwise nucleotide alignments (“blocks”) separated by larger gaps, some of which may be simultaneous gaps in both species. [...] intervening DNA in one species that does not align with the other because it is locally inverted or has been inserted in by lineage-specific translocation or duplication is skipped”

“The chains are then put into a list sorted with the highest-scoring chain first. [...] each iteration taking the next chain off of the list, throwing out the parts of the chain that intersect with bases already covered by previously taken chains, and then marking the bases that are left in the chain as covered. [...] If a chain covers bases that are in a gap in a previously taken chain, it is marked as a child of the previous chain. In this way, a hierarchy of chains is formed that we call a net.”

“To be considered syntenic, a chain has to either have a very high score itself or be embedded in a larger chain, on the same chromosome, and come from the same region as the larger chain. Thus, inversions and tandem duplications are considered syntenic.”

“We define the (human) span of a chain to be the distance in bases in the human genome from the first to the last human base in the chain, including gaps, and we define the size of the chain as the number of aligning bases in it, not including gaps.”

Hane JK, Rouxel T, Howlett BJ, Kema GH, Goodwin SB, Oliver RP.

Genome Biol. 2011;12(5):R45. doi:10.1186/gb-2011-12-5-r45

A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi.

Defines “mesosynteny” as the phenomonon seen when gene order varies at the scale of whole chromosomes, but gene content of homologous chromosomes does not vary much. Reports that in fungi, mesosynteny is found in filamentous Ascomycetes but not in other clades such as yeast. Concludes on the possibility that inversions play a role in mesosynteny.

Drillon G, Fischer G.

C R Biol. 2011 Aug-Sep;334(8-9):629-38. doi:10.1016/j.crvi.2011.05.011

Comparative study on synteny between yeasts and vertebrates.

“Synteny blocks were defined as series of neighboring pairs of orthologs separated by less than 5 nonneighboring reciprocal best-hits in the two compared genomes.” “In vertebrates, the number of synteny blocks increases exponentially with increasing divergence time, varying from a very small number of blocks, 43 between human and chimpanzee, to more than 1900 blocks between dog and zebrafish.” “In yeasts, the number of synteny blocks is more restrained, varying from 26 between Candida albicans and C. dubliniensis up to 744 between Debaryomyces hansenii and Pichia pastoris. The number of blocks also exponentially increases along with protein divergence but only between 8 and 36% of divergence. At increasing phylogenetic distances, the number of synteny blocks decreases.” “For both yeast and vertebrate, the average number of shared orthologs per synteny block decreases exponentially with increasing evolutionary distance”

Rocha, Eduardo P C.

Trends Genet. 2003 Nov;19(11):600-3. doi:10.1016/j.tig.2003.09.011

DNA repeats lead to the accelerated loss of gene order in bacteria.

Defines a Gene Order Conservation (GOC) number as: “the average number of orthologues for which the consecutive orthologue co-occurs close by in the other genome. It varies between 0 (no co-occurrence) and 1 (complete gene order conservation)”.

Mudd AB, Bredeson JV, Baum R, Hockemeyer D, Rokhsar DS

Commun Biol. 2020 Sep 1;3(1):480. doi:10.1038/s42003-020-1096-9

Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution.

“Comparative Hi-C analysis showed that the chromosome fusions on the M. muntjak lineage altered long-range, three-dimensional chromosome organization relative to M. reevesi in interphase nuclei including A/B compartment structure. This reshaping of multi-megabase contacts occurred without notable change in local chromatin compaction, even near fusion sites.”

“During the ~4.9 million years since the divergence of M. muntjak and M. reevesi, the M. muntjak lineage experienced 26 fusions for a rate of ~5.3 changes per million years.” “M. muntjak and M. reevesi [...] genomes are locally very similar, with 98.5% identity in aligned regions and a nucleotide divergence of 0.0130 substitutions per site, based on fourfold degenerate positions.” “The pairwise alignment of the muntjac genomes contains 2.45 Gb of contig sequence [...] average sequence identity of 98.5%, excluding indels [...] In comparison, alignments of red deer, reindeer, and muntjacs to B. taurus contain 1.80–2.21 Gb of contig sequences with 92.7–93.2% average identity.” “The nucleotide and temporal divergence between the two muntjac species is comparable to the divergence between humans and chimpanzees. The observed chromosome dynamism in muntjacs, however, far exceeds the rate in the chimpanzee and human lineages” “we noted the maintenance of distinct Hi-C boundaries in several examples, such as the junction between the X and autosomal segments on MMU3_X circa 133 Mb. Other fusion sites, however, show no notable difference compared with the rest of the genome in M. muntjak. As expected, M. reevesi shows a clear distinction between intra- and inter-chromosome contacts, including across fusion sites in M. muntjak.”

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Nature. 2007 Nov 8;450(7167):203-18. doi:10.1038/nature06341

Evolution of genes and genomes on the Drosophila phylogeny.

The result of pairwise comparisons between the species ranges between a few tens or hundreds of synteny blocks of up to ~1000 genes, to ~1000 synteny blocks with a few (tens of) genes.

Chakraborty M, Chang CH, Khost DE, Vedanayagam J, Adrion JR, Liao Y, Montooth KL, Meiklejohn CD, Larracuente AM, Emerson JJ.

Genome Res. 2021 Feb 9. doi:10.1101/gr.263442.120

Evolution of genome structure in the Drosophila simulans species complex.

“de novo reference genomes for the Drosophila simulans species complex (D. simulans, D. mauritiana, and D. sechellia), which speciated ∼250,000 yr ago.” “Genome-wide, ∼15% of sim-complex genome content fails to align uniquely to D. melanogaster.” “Within aligned sequence blocks, the sim-complex species show ∼7% divergence from D. melanogaster” “535–542 rearrangements between D. melanogaster and the sim-complex (approximately 90 mutations per million years), and 113–177 rearrangements within the sim-complex (226–354 mutations per million years)”

Zhou Y, Shearwin-Whyatt L, Li J, Song Z, Hayakawa T, Stevens D, Fenelon JC, Peel E, Cheng Y, Pajpach F, Bradley N, Suzuki H, Nikaido M, Damas J, Daish T, Perry T, Zhu Z, Geng Y, Rhie A, Sims Y, Wood J, Haase B, Mountcastle J, Fedrigo O, Li Q, Yang H, Wang J, Johnston SD, Phillippy AM, Howe K, Jarvis ED, Ryder OA, Kaessmann H, Donnelly P, Korlach J, Lewin HA, Graves J, Belov K, Renfree MB, Grutzner F, Zhou Q, Zhang G.

Nature. 2021 Jan 6. doi:10.1038/s41586-020-03039-0

Platypus and echidna genomes reveal mammalian biology and evolution.

The ancestral mammalian genome had 30 pairs of chromosomes.

José M. Martín-Durán, Bruno C. Vellutini, Ferdinand Marlétaz, Viviana Cetrangolo, Nevena Cvetesic, Daniel Thiel, Simon Henriet, Xavier Grau-Bové, Allan M. Carrillo-Baltodano, Wenjia Gu, Alexandra Kerbl, Yamile Marquez, Nicolas Bekkouche, Daniel Chourrout, Jose Luis Gómez-Skarmeta, Manuel Irimia, Boris Lenhard, Katrine Worsaae, Andreas Hejnol

bioRxiv 2020.05.07.078311; doi:10.1101/2020.05.07.078311

Conservative route to genome compaction in a miniature annelid

Genome assembly (PacBio, 73.8 Mb, 95.8% BUSCO genes, 2.24 Mb N50, 4.87% transposable elements, 14,203 protein-coding genes) for the annelid Dimorphilus gyrociliatus, a meiobenthic segmented worm. Synteny with the scallop genome is visible. The Hox cluster is present and lacks only one gene, post1. However, in situ hybridisation suggests lack of temporal colinearity. The Myc pathway “lacks the regulators mad (in D. gyrociliatus) and mnt (in all Dinophilidae), a condition also shared with the appendicularian O. dioica”. “Open chromatin regions [ATAC-seq peaks] are short and mostly found in promoters.” “Promoters [CAGE] are narrow (<150 bp) and use pyrimidine-purine dinucleotides as preferred initiators.”

Wang S, Zhang J, Jiao W, Li J, Xun X, Sun Y, Guo X, Huan P, Dong B, Zhang L, Hu X, Sun X, Wang J, Zhao C, Wang Y, Wang D, Huang X, Wang R, Lv J, Li Y, Zhang Z, Liu B, Lu W, Hui Y, Liang J, Zhou Z, Hou R, Li X, Liu Y, Li H, Ning X, Lin Y, Zhao L, Xing Q, Dou J, Li Y, Mao J, Guo H, Dou H, Li T, Mu C, Jiang W, Fu Q, Fu X, Miao Y, Liu J, Yu Q, Li R, Liao H, Li X, Kong Y, Jiang Z, Chourrout D, Li R, Bao Z.

Nat Ecol Evol. 2017 Apr 3;1(5):120. doi:10.1038/s41559-017-0120

Scallop genome provides insights into evolution of bilaterian karyotype and development.

“The final [SOAPdenovo] assembly is 988 Mb, with a contig N50 size of 38 kb and a scaffold N50 size of 804 kb.” “With the aid of a high-density linkage map (7,489 markers) constructed by using the 2b-RAD methodology, 1,419 scaffolds (covering ~81% of the assembly) are assigned to the 19 haploid chromosomes.” “The scallop genome encodes 26,415 protein-coding genes.” “Phylogenetic analysis with 482 highly conserved, single-copy genes show that the scallop lineage diverged around ~425 Ma from the lineage leading to Pacific oyster and pearl oyster. Based on the sister taxon relationship between Bivalvia and Gastropoda, our phylogenetic analysis gives an estimation of 504 Ma for the appearance of the bivalve lineage or its divergence from the gastropod lineage.” “Chromosome-based macrosynteny analysis reveals a near-perfect correspondence between the 19 scallop chromosomes and the 17 presumed bilaterian ancestral linkage groups.” “ParaHox and Hox clusters are well-preserved and remain intact in the scallop genome.”

Ranz JM, Casals F, Ruiz A.

Genome Res. 2001 Feb;11(2):230-9. doi:10.1101/gr.162901

How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila.

186 DNA probes on Muller element E (density: 1 / 175 kbp in D. mel and 1 / 219 in D. rep) for comparing gene order in D. repleta and D. melanogaster. Random distribution of breakpoints. “177.07 (±28.88) breakpoints or 89 (±14) paracentric inversions fixed in this chromosomal element between D. melanogaster and D. repleta.” “Application of [a] ML method [...] yielded an estimate of 228 (±28) fixed breakpoints, that is, 114 ± 14 fixed inversions.” “We estimate an evolution rate of 0.9–1.4 chromosomal inversions fixed per million years.” “A significant correlation of gene order was found.” “If large inversions have a low probability of fixation because of their fertility effects (Navarro et al. 1997), which seems to be the case (Cáceres et al. 1997), then the randomization of gene order would proceed at a slower rate than is implied in Figure 2.”

Shah N, Dorer DR, Moriyama EN, Christensen AC.

G3 (Bethesda). 2012 Feb;2(2):313-9. doi:10.1534/g3.111.001412

Evolution of a large, conserved, and syntenic gene family in insects.

The Osiris gene family, specific to insects, shows strong conservation of synteny over ~400 million years

Simakov O, Marlétaz F, Yue JX, O'Connell B, Jenkins J, Brandt A, Calef R, Tung CH, Huang TK, Schmutz J, Satoh N, Yu JK, Putnam NH, Green RE, Rokhsar DS.

Nat Ecol Evol. 2020 Jun;4(6):820-830. doi:10.1038/s41559-020-1156-z

Deeply conserved synteny resolves early events in vertebrate evolution.

Most of the 19 amphioxus (lancelet) chromosomes directly correspond to one of the 17 ancestral chordate linkage groups. Pattern of paralogue elimination show that autotetraploidy was followed by allotetraploidy in bony vertebrates. Vertebrate and amphioxus mini-chromosomes descend from the ancestral linkage groups too.

Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutiérrez EL, Dubchak I, Garcia-Fernàndez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin-I T, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS.

Nature. 2008 Jun 19;453(7198):1064-71. doi:10.1038/nature06967

The amphioxus genome and the evolution of the chordate karyotype.

17 ancestral chordate chromosomes.

“We estimate that the haploid amphioxus genome contains 21,900 protein-coding loci. [...] The observed heterozygosity shows correlations at short distances that decay on scales greater than ∼1 kb, indicating extensive recombination in the population. [...] Wwe reconstructed the gene complements of 17 linkage groups (that is, proto-chromosomes) of the last common chordate ancestor. [...] This analysis shows that most of the human genome (112 segments spanning 2.68 Gb, or 95% of the euchromatic genome) was affected by large-scale duplication events on the vertebrate stem before the bony vertebrate radiation (that is, the teleost/tetrapod split), and that nearly all of the ancient chordate chromosomes were quadruplicated. [...] Allowing for a range of nearly parsimonious reconstructions of 2R, we estimate that the bony vertebrate ancestor had between 37 and 49 chromosomes.”

Berthelot C, Muffato M, Abecassis J, Roest Crollius H.

Cell Rep. 2015 Mar 24;10(11):1913-24. doi: 10.1016/j.celrep.2015.02.046

The 3D organization of chromatin explains evolutionary fragile genomic regions.

Explains the power law distribution of breakpoints in mammals and yeast with chromosome contacts (Hi-C) and open chromatin (ENCODE).

“We [...] reconstruct the ancestral gene order in the 95-million-year-old ancestral genome of Boreoeutheria, the last common ancestor of primates, rodents, and laurasiatherians. [...] This reconstructed genome was further annotated with respect to its intergenic regions [...] their lengths, GC content and their proportion of conserved non-coding sequence as defined by GERP. [...] We then identified evolutionary rearrangement breakpoints that have occurred in the human, mouse, dog, cow, and horse lineages. [...] We identified a total of 751 breakpoints, 20 of which correspond to independent breakpoint reuse. [...] The identified breakpoints show the typical characteristics of rearrangement breakpoints; i.e., they occur in GC-rich, gene-dense regions possessing lower proportions of conserved non-coding sequence. [...] Breakpoint events per intergene increase as a power law of intergene length rather than a proportionality law. [...] Ancestral intergenes with high CNE content have been disrupted by significantly fewer breakpoints than intergenes of similar length with lower CNE content. [...] Rpeated elements and recombination frequencies are distributed radically differently from breakpoints, eliminating them as potential candidates to explain the breakpoint pattern. [...] The density of open chromatin is similar to the pattern of breakpoints with the proportion of DNA in an open state decreasing as intergene size increases. [...] Simulating inversions in the human genome according to contact probability [...] rearrangements were allowed to occur only between open chromatin regions, using chromatin state profiles for different cell types published by the ENCODE consortium. Under this model, the simulated average number of breakpoints per intergene closely reproduces the relationship with intergene length observed in real data.”

Sacerdot C, Louis A, Bon C, Berthelot C, Roest Crollius H.

Genome Biol. 2018 Oct 17;19(1):166. doi:10.1186/s13059-018-1559-1

Chromosome evolution at the origin of the ancestral vertebrate genome.

“The pre-1R karyotype comprised 17 chromosomes, duplicated into 34 chromosomes after the first WGD and followed by seven fusions. The resulting 27 chromosomes were duplicated in the second WGD leading to 54 Vertebrata chromosomes, at the origin of the approximately 60,000 extant species of vertebrates.” “The 54 chromosomes in the post-2R Vertebrata led to a Euteleostomi karyotype of 50 chromosomes (4 fusions) and to an Amniota karyotype of 49 chromosomes.” “The structure of the 17 pre-1R chromosomes is still strikingly apparent in the human genome, with some chromosomes almost entirely composed of genes from a single pre-1R chromosome (e.g., chromosomes 14 and 15).“ “We note that although all chromosome tetrads corresponding to pre-1R chromosomes are complete (i.e., are composed of 4 CARs), the 49 reconstructed Amniota chromosomes display large differences in gene numbers: the largest contains 862 genes (chromosome 37) and the smallest only 16 genes (chromosome 49). This could reflect either a more intense process of gene inactivation and loss on chromosomes with fewer genes, or a more intense rate of rearrangement on those chromosomes, leading to greater difficulties in reconstructing them.“

Meisel RP, Delclos PJ, Wexler JR.

BMC Biol. 2019 Dec 5;17(1):100. doi:10.1186/s12915-019-0721-x

The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence.

“We provide two lines of evidence that the X chromosome of the German cockroach, B. germanica, is homologous to Muller element F, which is X-linked in most flies. First, there is a reduced sequencing coverage of nearly half of the Muller element F homologs in male cockroach, consistent with a haploid dose of the X chromosome in males (Fig. 2). Second, there is a decreased heterozygosity of element F homologs in male cockroach, including those with reduced male sequencing coverage (Fig. 3). We therefore hypothesize that element F is an ancient X chromosome that was present in the most recent common ancestor (MRCA) of flies and cockroaches, and it has been conserved as an X chromosome in the German cockroach and many fly species.”

Carbone L, Harris RA, Gnerre S, Veeramah KR, Lorente-Galdos B, Huddleston J, Meyer TJ, Herrero J, Roos C, Aken B, Anaclerio F, Archidiacono N, Baker C, Barrell D, Batzer MA, Beal K, Blancher A, Bohrson CL, Brameier M, Campbell MS, Capozzi O, Casola C, Chiatante G, Cree A, Damert A, de Jong PJ, Dumas L, Fernandez-Callejo M, Flicek P, Fuchs NV, Gut I, Gut M, Hahn MW, Hernandez-Rodriguez J, Hillier LW, Hubley R, Ianc B, Izsvák Z, Jablonski NG, Johnstone LM, Karimpour-Fard A, Konkel MK, Kostka D, Lazar NH, Lee SL, Lewis LR, Liu Y, Locke DP, Mallick S, Mendez FL, Muffato M, Nazareth LV, Nevonen KA, O'Bleness M, Ochis C, Odom DT, Pollard KS, Quilez J, Reich D, Rocchi M, Schumann GG, Searle S, Sikela JM, Skollar G, Smit A, Sonmez K, ten Hallers B, Terhune E, Thomas GW, Ullmer B, Ventura M, Walker JA, Wall JD, Walter L, Ward MC, Wheelan SJ, Whelan CW, White S, Wilhelm LJ, Woerner AE, Yandell M, Zhu B, Hammer MF, Marques-Bonet T, Eichler EE, Fulton L, Fronick C, Muzny DM, Warren WC, Worley KC, Rogers J, Wilson RK, Gibbs RA.

Nature. 2014 Sep 11;513(7517):195-201. doi:10.1038/nature13679

Gibbon genome and the fast karyotype evolution of small apes.

“We identified 96 gibbon–human synteny breakpoints in Nleu1.0.” “Segmental duplication enrichment was the best predictor of gibbon–human synteny breakpoints,[...] however, breakpoints were also enriched for Alu elements.” “ The majority of gibbon chromosomal breakpoints bore signatures of non-homology based mechanisms.” “We observed an enrichment of gibbon–human breakpoints in CTCF-binding events.” Insertion of LAVA (3'-L1-AluS-VNTR-Alu-like-5') elements in genes related to cell division might have caused the accelerated evolution of the karyotype in gibbons.

Lazar NH, Nevonen KA, O'Connell B, McCann C, O'Neill RJ, Green RE, Meyer TJ, Okhovat M, Carbone L.

Genome Res. 2018 Jul;28(7):983-997. doi:10.1101/gr.233874.117

Epigenetic maintenance of topological domains in the highly rearranged gibbon genome.

to read

Renschler G, Richard G, Valsecchi CIK, Toscano S, Arrigoni L, Ramírez F, Akhtar A.

Genes Dev. 2019 Oct 10. doi: 10.1101/gad.328971.119

Hi-C guided assemblies reveal conserved regulatory topologies on X and autosomes despite extensive genome shuffling.

Found 20 synteny breakpoints (SB) per Mb on average. “Approximately 75% of SBs stay within the A or B compartment” “Overlaps of TAD boundaries and SB breakpoints in all comparisons are highly significant”

“Hi-C data of D. melanogaster, D. virilis, and D. busckii embryos”

“D. virilis and D. busckii [...] cover ∼40 million years of evolution and multiple subgenera (Russo et al. 2013).”

“conserved sequences mostly reside on the same chromosomal arms”

“we defined synteny blocks (SBs), which are chains of conserved collinear regions that are used to identify and compare homologous regions between different species. On average, we find 20 synteny breakpoints per megabase (3726 and 3252 breakpoints in the D. melanogaster vs. D. virilis comparison, respectively, and 3340 and 2776 breakpoints in the D. melanogaster vs. D. busckii comparison, respectively), corresponding to about one breakpoint every six genes.”

“Approximately 75% of SBs stay within the A or B compartment and 25% switch between compartments. In general, about double the number of SBs lie within the A compartment than the B compartment.”

“many SB breakpoints overlap with TAD boundaries”

“To identify synteny blocks (SBs) we use LASTZ (Harris 2007) with the following parameters: “–gfextend –nochain –gapped,” which identifies local alignment blocks. We then chained blocks that are within 10-kb distance, have the same orientation, and contain at least four LASTZ-defined blocks. Chained results that were <4 kb or completely overlapped a bigger synteny block were removed.”