A Genomic Update on the Evolutionary Impact of Chromosomal Rearrangements

Molecular Ecology, Journal Year: 2024, Volume and Issue: 33(24)

Published: Nov. 25, 2024

The field of evolutionary and speciation genomics has been revolutionised by the ubiquity availability genomic data even for non-model organisms. capability to sequence long-fragment DNA particularly spurred trans-national initiatives generate publicly available chromosome-resolved reference genomes across Tree Life. Initiatives such as Darwin Life (The Project Consortium et al. 2022) or European Genome Atlas (ERGA; Mazzoni, Ciofi, Waterhouse 2023) enable researchers around globe address unresolved questions pursue novel lines research. role chromosomal rearrangements (CRs) in driving evolution a long-standing question biology (Berdan 2023; Dobzhansky Sturtevant 1938; King 1995; Robertson 1916; Wellenreuther Bernatchez 2018; White 1978). CRs comprise an array that reorganise linear genome, ranging from local structural variants (SVs) inversions duplications, large-scale karyological changes, including fusions fissions Lucek 2023). Current have already highlighted are much more common diverse taxa than previously thought (e.g., Damas 2022; Weissensteiner 2020). While can now easily be mapped within taxa, their potential species diversification often remained enigmatic, theoretical explorations exist only few types CR At dawn broad genome model organisms alike, our special issue aims provide update on impact various CRs. Specifically, asks what causes establishment whether these differ among taxa? Are randomly distributed do they cause other rearrangements? How promote how potentially lead speciation? Is same different CRs? Finally, depending autosomes sex chromosomes involved? Whether directly indirectly involved adaptation diversification, detecting them understanding factors influencing appearance first place key start shedding light processes linked Traditionally, were detected either directly, with cytogenetic screenings (Krimbas Powell 1992; Stebbins 1971; 1973), indirectly, looking at consequences 1938). However, resolution techniques and/or limitation cross-species comparisons restricted study evolution. In this issue, several contributions successfully used chromosome-level assemblies long-read sequencing analyse range systems scales. Focusing holocentric sedges genus Carex, Escudero (2023) estimated overall high rate genus. Using dual approach, authors then combined linkage maps identify between species, later refine using Carex outgroup define conserved rearranged regions. Interestingly, despite rates chromosome fission fusion, longer expected syntenic blocks species. Comparing distribution transposable elements (TEs) genes two regions, further showed regions correlate gene dense areas, while TEs, pointing hotspots reshuffling. Going one step further, Cornet compared repetitive independently evolved clades - Erebia butterflies relation result karyotype changes clades. First, low-coverage short-read characterised species-specific repeat landscape, highlighting classes occur four collected information populations landscapes populations, scale degree genetic differentiation, suggesting similar may affect rest genome. macroevolutionary scale, clustering based differences landscape general concordance gene-based phylogeny, although was stronger Carex. Moreover, number proxy inter-chromosome rearrangements, found certain repeats likely associated changes. Overall, results fusion events but relative specific karyotypic differs groups. By analysing three medaka fishes representing major karyotypes, is, metacentric acrocentric larger smaller arm numbers, respectively well large chromosomes, Ansai tested caused centric fissions, pericentric inversions, centromere repositioning, tandem fusions. They identified putative centromeric continuous long reads polished short reads, assessed unassembled phylogenetic analyses compare centromere-associated study, not multiple enriched pericentromeric also some sequences all centromeres landscapes. mechanism played fishes, allowing shape without altering numbers. Arias-Sardá, Quigley, Farré aligned 26 ruminant reconstructed five ancestral ancestor most recent bovids. doing so, CRs, breakpoint (EBRs) blocks. maintaining synteny 50 million years, others rearrangement. Similarly (2023), Arias-Sardá colleagues looked into TEs showing depleted expression least nine tissues orthologous housekeeping genes. breaks genes, tend located These results, previous publications carnivores rodents (Álvarez-González Corbo highlight co-localise boundaries topologically domains, suggest might regulatory disrupting functional essential become fixed But happens when occur? Wang hotspot Neurospora fungi telomeres where duplication relocation led lineage-specific 78% telomeric through regional rebirth. To investigate functions assembled 68 experiments 14 transcriptomic studies, covering morphological stages distinct culturing conditions N. crassa. Although non-essential partners aspects crassa biology, knocked down mas-1 increased resistance toxins, contribute new phenotypes under conditions. All all, highlights source novelty speciation. Chromosome formation structures, neo-sex autosome chromosome. tribe Danaini, Mora (2024) investigated chromosomes. stand out containing prominent examples fused chromosomes: recently neo-W another older neo-Z Oxford Nanopore Illumina RNA-Seq libraries assemble annotate Danaini levels both autosomes, identifying sex-biased strong association presence likelihood turnover, affecting W clusters significantly biased towards males females, roles This accumulation influenced mechanisms sexual antagonism, emerges critical factor contributing observed over time macro-evolutionary perspective, geographic isolation drivers biodiversity. Márquez-Corro conducted integrative combining phylogeography, ecological requirements plant complex, Western Euro-Mediterranean region. RADseq 152 samples, constructed phylogeny studied Combined molecular evidence points southern Iberia–north Africa cradle group. addition, 74 loci correlated variables related adaptation, temperature precipitation. climatic variables. Therefore, supports hypothesis variation, could selected optima regimes. Ranging fungi, mammals monocentric clear picture emerges, genomes; instead, paired elements. moreover traits. If selectively advantageous reproductive isolation, eventually (Faria Navarro 2010; Kirkpatrick Barton 2006). empirical observations taxonomic groups 2023), fixation is easy point view: meiotic defects heterozygotes, would hybrid dysfunction sterility underdominant, especially low frequency (Navarro 2003). Consequently, strongly underdominant thus unlikely spread fixation. weak underdominance make likely, weaker less 2019; Faria Rieseberg 2001). ambiguous consequently referred 'underdominance paradox' (Spirito 1998). Fixation if selective advantage, instance overdominance, via inbreeding drift, which counteract negative selection facilitate novel, yet (Guerrero 2014; Hedrick 1981; still elusive addressed issue. contribution Jay, Aubier, Joron implements two-island population explore flow overdominant act supergenes. Supergenes represent particular type polymorphism group elements, segregate single Mendelian locus (Thompson Jiggins 2014) inversions. Modelling evolving disruptive resulted poorly adapted immigrant inversion haplotypes. model, supergenes evolve maintained balancing because maintenance alternative haplotypes bear unequal benefits adaptation. case recombination load balances fitness load, loss existing locally haplotype, turn differentially non-recombining extends idea environmental (Schwander, Libbrecht, Keller 2014), intrinsic features themselves. forward-in-time simulation framework, Banse outcome substitutions, insertion-deletions (InDels) Their models duplications reduce epistasis, together support long-term Here, higher benefit simulations started far off optimum, adaptive Within simulated small InDels size differently. allow de novo instead allowed evolve, introduce random material, leading fewer Together, evolution, therefore speciation, conditions, stress need develop frameworks go beyond widespread Life, it remains unclear established chance, example, drift selection. level assemblies, Mackintosh Brenthis butterflies. Based inferred demographic history focal show neutral very weakly system. enough fix considerably there positive natural drive. Indeed, event sweep, though distant past excluded. framework combines whole-genome scale. Chromosomal suppression (Noor 2001; 2001) inducing heterozygote disadvantage (White operate Yoshida Inversions (Kirkpatrick 2006) recombination, thereby capturing linking alleles, divergence face flow. comparatively 2018), studies focused (but see Augustijnen 2024; 2024), translocations (see Guerrero (2014)), Several expand polymorphisms. For instance, Ravagni characterise absence acts supergene quail Coturnix coturnix Azores. quails Europe Africa, Macaronesian archipelagos, migratory behaviour (Sanchez-Donoso 2022). Azores, find inverted standard configuration minimal, arrangements coexisted relatively populations. selection, rather divergent maintains frequencies migration absent Azorean present not, vary geographical those underlying repeated ecotype formation, polymorphic species' explored Reeve (2023). rough periwinkle Littorina saxatilis, closely arcana, polymorphisms common, tied parallel ecotypes vast nonetheless location-dependent patterns, indicating contain sets alleles pressures. Altogether, suggests complex ecotypes, given basis always same. complementary approach detect spl heterozygosity, useful cases fully resolved, rare. Mediterranean long-snouted seahorses Hippocampus guttulatus Meyer (2024), similarly large, ancient inversions: alternatively marine lagoon environments, play second Sea governed combination pseudo-overdominance possible breakdown link marine-lagoon environment polymorphic, epistatic interactions bring up interesting concerning interplay segregating many seem involve sections (Meyer Schaal, Haller, Lotterhos does case. extensive, sockeye salmon Oncorhynchus nerka, Euclide islands spawning ground. Most consistently everywhere. Only seems hitchhiking. radiation multitude mosaic unique allele combinations divergence. require importance. architecture strength pressures influence Sex disproportionately (Payseur, Presgraves, Filatov 2018) (Mora Wright 2016). Viitaniemi effects Z-chromosome zebra finch Taeniopygia guttata sperm morphology. As disrupt regulation tissue-specific manner Kraft 2019), analysed testes liver development. impacts liver, heterokaryotypes intermediate resembling homokaryotype gene-specific manner. Taken together, pleiotropic tissues. Technical limitations CR. Recent developments, overcome obstacle international democratising access resources. brings diversity, micro- level, explorations, nature classic detection methods data, use current state-of-the-art comparative approaches Contrasting predictions homology (Nadeau Sankoff 1998), as, undergo (Arias-Sardá, (2023); (2023)). generality investigation. (Cornet (Wang diversity genomes. nevertheless profound structure, repositioning (Ansai Despite ease genome-wide quantified, fixation, enigmatic. Overcoming dominance paradox, context dependent (Ravagni Sanchez-Donoso Other establish adaptive, promoting Macroevolutionary investigations additional extrinsic agents promoted (Lucek precipitation (Potter 2017). intraspecific variation (Euclide 2018). Given having eukaryotic becoming reality next decade, inferences will possible, map genera families test Combining intra- interspecific pan-genome hold bridge Identifying target allows experimental CRISPR/CAS9 (Cheng nanosurgery (Blázquez-Castro, Fernández-Piqueras, Santos 2020) correlational associations. Understanding requires so 2019) numbers InDels. primarily along latter folded three-dimensional structure altered technical advances organisms, assess (Mohan 2024). contributed writing manuscript. We like thank who articles Special Issue, reviewers evaluated manuscripts. executive editor Ben Sibbett his help throughout. K.L. supported Swiss National Science Foundation (SNSF) Eccellenza 'The barriers completion speciation' (Grant ID 202869) H.A. SNSF grant 184934 'Genomic origin awarded Burckhardt-Bürgin foundation 219283 Thomas Flatt. C.A.-S. funded GTA fellowship programme University Kent. M.F. Royal Society RGS/R1/211047. declare no conflicts interest. editorial any data.

Language: Английский

Impact of Z chromosome inversions on gene expression in testis and liver tissues in the zebra finch

Molecular Ecology, Journal Year: 2023, Volume and Issue: 33(24)

Published: Dec. 21, 2023

Chromosomal inversions have been identified in many natural populations and can be responsible for novel traits rapid adaptation. In zebra finch, a large region on the Z chromosome has subject to multiple inversions, which pleiotropic effects but especially sperm phenotypes, such as midpiece flagellum length. To understand effect, inversion these traits, we examined testis liver transcriptomes of young males at different maturation times. We compared gene expression differences among three karyotypes: AA, B*B* AB*, where B* denotes inverted regions with respect A. testis, 794 differentially expressed genes were found most them located Z. They functionally enriched sperm-related traits. also clusters co-expressed that matched inversion-related phenotypes. liver, there some functions overrepresentation similar location testis. both tissues, overrepresented near distal end middle chromosome. For heterokaryotype, observed several one allele being dominantly expressed, patterns or other homokaryotype. This was confirmed SNPs genes, interestingly gene, DMGDH, had allele-specific originating mainly from haplotype yet haplotypes equally liver. karyotype-specific difference tissue-specific suggests effect thus mechanism divergent phenotypic resulting an inversion.

Language: Английский

Repeated evolution on oceanic islands: comparative genomics reveals species-specific processes in birds

BMC Ecology and Evolution, Journal Year: 2024, Volume and Issue: 24(1)

Published: Nov. 8, 2024

Understanding the interplay between genetic drift, natural selection, gene flow, and demographic history in driving phenotypic genomic differentiation of insular populations can help us gain insight into speciation process. Comparing patterns across different taxa subjected to similar selective pressures upon colonizing oceanic islands provides opportunity study repeated evolution identify shared their landscapes differentiation. We selected four species passerine birds (Common Chaffinch Fringilla coelebs/canariensis, Red-billed Chough Pyrrhocorax pyrrhocorax, House Finch Haemorhous mexicanus Dark-eyed/island Junco hyemalis/insularis) that have both mainland populations. Changes body size island were consistent with rule. For each species, we sequenced whole genomes from individuals infer history, characterize differentiation, factors shaping them. estimated relative (F

Language: Английский