The Impact of Chromosomal Rearrangements in Speciation: From Micro- to Macroevolution

Lucek, Kay; Giménez, Mabel D.; Joron, Mathieu; Rafajlović, Marina; Searle, Jeremy B.; Walden, Nora; Westram, Anja Marie; Faria, Rui

doi:10.1101/cshperspect.a041447

Cited by 19 publications

(9 citation statements)

References 127 publications

(150 reference statements)

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“…Inversions have been increasingly appreciated as key to enabling coexistence of ecologically divergent lineages in sympatry (Hooper and Price, 2017;Faria, Chaube, et al, 2019). And yet, how the inversions enabling the formation of stable morphs, divergence or speciation originate remains a consequential question (Faria, Johannesson, et al, 2019;Lucek et al, 2023). We document recent and extensive expansions of long terminal repeats, constituting over 20% of the genome in T. conura, rendering genome size in T. conura 55% bigger than that of the closely related species Rhagoletis pomonella.…”

Section: Discussionmentioning

confidence: 94%

“…In spite of mounting support for inversions having a role in speciation (Jones et al, 2012;Küpper et al, 2016;Tuttle et al, 2016;Hooper and Price, 2017;Wellenreuther and Bernatchez, 2018;Faria, Chaube, et al, 2019;Faria, Johannesson, et al, 2019;Lucek et al, 2023), studies that uncover how they contribute to coupling of genes underlying ecological and reproductively isolating traits, enabling the formation of persistent species are scarce (but see Meyer et al, 2023;Moan et al, 2023). We find compelling evidence for a large inversion enabling host race specific adaptation and progress towards speciation in T. conura.…”

Section: Discussionmentioning

confidence: 99%

“…Regions that repeatedly differ among differentially adapted taxa are likely to play a role in speciation (Johannesson et al, 2010;Meier et al, 2018;Rivas et al, 2018;Bohutínská et al, 2021;Koch et al, 2022). Extensive theoretical and empirical evidence has shown that genomic architecture coupling coadapted loci, including inversions, is particularly important for persistence of differential adaptation in the face of gene flow Kirkpatrick and Barton, 2006;Wellenreuther and Bernatchez, 2018;Faria, Johannesson, et al, 2019;Berdan et al, 2022;Schaal et al, 2022;Lucek et al, 2023). Yet, the extent to which linkage of ecological adaptation and reproductive isolation loci is facilitated by pleiotropic effects of the same genes, coupling of genes through structural variation, or co-inheritance of uncoupled genomic regions upheld by correlational selection remains an empirical challenge for speciation researchers.…”

Section: Introductionmentioning

confidence: 99%

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The genomic landscape of adaptation to a new host plant

Nilsson

Steward

Gimenez

et al. 2023

Preprint

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Adaptation to novel ecological niches is known to be rapid. However, how ecological divergence translates into reproductive isolation remains a consequential question in speciation research. It is still unclear how coupling of ecological divergence loci and reproductive isolation loci occurs at the genomic level, ultimately enabling the formation of persistent species. Here, we investigate the genomic underpinning colonization of a new niche and formation of two host races in Tephritis conura peacock flies that persist in sympatry. To uncover the genomic differences underlying host plant adaptation, we take advantage of two independent sympatric zones, where host plant specialists using the thistle species Cirsium heterophyllum and C. oleraceum co-occur, and address what regions of the genome that diverge between the host races in a parallel fashion. Using Population Branch Statistics, dxy and BayPass we identify 2996 and 3107 outlier regions associated with host use among western and eastern Baltic populations, respectively, with 82% overlap. The majority of outliers are located within putative inversions, adding to the growing body of evidence that structural changes to the genome are important for adaptations to persist in face of gene flow. Potentially, the high contents of repetitive elements could have given rise to the inversions, but this remains to be tested. The outlier regions were enriched for genes involved in e.g. metabolism and morphogenesis, potentially due to the selection for processing different metabolites, and changes in size and ovipositor length respectively. In conclusion, this study suggests that structural changes in the genome, and divergence in independent ecological functions may facilitate the formation of persistent host races in face of gene flow.

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Section: Discussionmentioning

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The genomic landscape of adaptation to a new host plant

Nilsson

Steward

Gimenez

et al. 2023

Preprint

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“…18 Mya (de Vos et al, 2014a). Despite the importance of chromosomal rearrangements in adaptation and speciation, little is known on how frequently they occur in different species (Lucek et al, 2023; Mérot et al, 2020), thus it is impossible to compare the rate of rearrangements observed in Primula with other plant groups. However, we previously discovered a high frequency of intra-species structural rearrangements in P. veris and postulated that this phenomenon may be linked to the dynamic nature of Primula genomes, potentially influenced by transposable elements (TEs), which constitute a significant portion of primrose genomes (see below; Potente et al, 2022a).…”

Section: Resultsmentioning

confidence: 99%

ThePrimula edelbergii S-locus is an example of a jumping supergene

Potente,

Yousefi,

Keller

et al. 2024

Preprint

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Research on supergenes, non-recombining genomic regions housing tightly linked genes that control complex phenotypes, has gained prominence in genomics, with supergenes having been described in most eukaryotic lineages. Heterostyly, a floral heteromorphism promoting outcrossing in several angiosperm families, is controlled by the S-locus supergene. Historically, the S-locus has been studied primarily in closely related Primula species and, more recently, in other groups that independently evolved heterostyly. However, it remains unknown whether genetic architecture and composition of the S-locus are maintained among species that share a common origin of heterostyly and subsequently diverged across larger time scales. To address this research gap, we present a chromosome-scale genome assembly of Primula edelbergii, a species that shares the same origin of heterostyly with Primula veris (whose S-locus has been characterized) but diverged from it ca. 18 million years ago. Comparative genomic analyses between P. edelbergii and P. veris allowed us to show, for the first time, that the S-locus can 'jump' (i.e. translocate) between chromosomes. Additionally, we found that four S-locus genes were maintained across time but were reshuffled within the supergene, seemingly without affecting their expression. Furthermore, we confirmed that S-locus hemizygosity counteracts genetic degeneration, otherwise expected in supergenes. Finally, we investigated P. edelbergii evolutionary history within Ericales in terms of whole genome duplications and transposable element accumulation. In summary, our work provides a valuable resource for comparative analyses aimed at investigating the genetics of heterostyly and the pivotal role of supergenes in shaping the evolution of complex phenotypes.

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“…In oaks, research has revealed the importance of natural hybridization and introgression in promoting genetic diversity and the generation of new species [ 53 , 54 ]. Identical chromosomal rearrangements among oaks are associated with the evolution of Quercus ’ common ancestor, and these rearrangements may have been preserved in frequent hybridization and have the effect of inhibiting recombination [ 55 , 56 ]. Species-specific chromosomal variation enriched the lineage-specific diversity of chromosomal structure and contributed to the species reproductive isolation, speciation, and adaptive evolution [ 3 , 9 ].…”

Section: Discussionmentioning

confidence: 99%

Karyotype and LTR-RTs analysis provide insights into oak genomic evolution

Cao,

Chen,

Liao

et al. 2024

BMC Genomics

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Background Whole-genome duplication and long terminal repeat retrotransposons (LTR-RTs) amplification in organisms are essential factors that affect speciation, local adaptation, and diversification of organisms. Understanding the karyotype projection and LTR-RTs amplification could contribute to untangling evolutionary history. This study compared the karyotype and LTR-RTs evolution in the genomes of eight oaks, a dominant lineage in Northern Hemisphere forests. Results Karyotype projections showed that chromosomal evolution was relatively conservative in oaks, especially on chromosomes 1 and 7. Modern oak chromosomes formed through multiple fusions, fissions, and rearrangements after an ancestral triplication event. Species-specific chromosomal rearrangements revealed fragments preserved through natural selection and adaptive evolution. A total of 441,449 full-length LTR-RTs were identified from eight oak genomes, and the number of LTR-RTs for oaks from section Cyclobalanopsis was larger than in other sections. Recent amplification of the species-specific LTR-RTs lineages resulted in significant variation in the abundance and composition of LTR-RTs among oaks. The LTR-RTs insertion suppresses gene expression, and the suppressed intensity in gene regions was larger than in promoter regions. Some centromere and rearrangement regions indicated high-density peaks of LTR/Copia and LTR/Gypsy. Different centromeric regional repeat units (32, 78, 79 bp) were detected on different Q. glauca chromosomes. Conclusion Chromosome fusions and arm exchanges contribute to the formation of oak karyotypes. The composition and abundance of LTR-RTs are affected by its recent amplification. LTR-RTs random retrotransposition suppresses gene expression and is enriched in centromere and chromosomal rearrangement regions. This study provides novel insights into the evolutionary history of oak karyotypes and the organization, amplification, and function of LTR-RTs.

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The Impact of Chromosomal Rearrangements in Speciation: From Micro- to Macroevolution

Cited by 19 publications

References 127 publications

The genomic landscape of adaptation to a new host plant

The genomic landscape of adaptation to a new host plant

ThePrimula edelbergii S-locus is an example of a jumping supergene

Karyotype and LTR-RTs analysis provide insights into oak genomic evolution

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