An Ancestral Balanced Inversion Polymorphism Confers Global Adaptation

Molecular Biology and Evolution, Journal Year: 2023, Volume and Issue: 40(6)

Published: May 23, 2023

Abstract Since the pioneering work of Dobzhansky in 1930s and 1940s, many chromosomal inversions have been identified, but how they contribute to adaptation remains poorly understood. In Drosophila melanogaster, widespread inversion polymorphism In(3R)Payne underpins latitudinal clines fitness traits on multiple continents. Here, we use single-individual whole-genome sequencing, transcriptomics, published sequencing data study population genomics this four continents: its ancestral African range derived populations Europe, North America, Australia. Our results confirm that originated sub-Saharan Africa subsequently became cosmopolitan; observe marked monophyletic divergence inverted noninverted karyotypes, with some substructure among chromosomes between Despite divergent evolution since out-of-Africa migration, non-African exhibit similar patterns long-range linkage disequilibrium breakpoints major peaks center, consistent balancing selection suggesting harbors alleles are maintained by several Using RNA-sequencing, identify overlap inversion-linked single-nucleotide polymorphisms loci differentially expressed chromosomes. Expression levels higher for at low temperature, loss buffering or compensatory plasticity frequency warm climates. suggest ancestrally tropical balanced spread around world latitudinally assorted along independent climatic gradients, always being frequent subtropical/tropical areas rare absent temperate

Language: Английский

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Why do sex chromosomes progressively lose recombination?

Trends in Genetics, Journal Year: 2024, Volume and Issue: 40(7), P. 564 - 579

Published: April 27, 2024

Language: Английский

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Divergence and gene flow history at two large chromosomal inversions underlying ecotype differentiation in the long‐snouted seahorse

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

Published: Jan. 27, 2024

Abstract Chromosomal inversions can play an important role in divergence and reproductive isolation by building maintaining distinct allelic combinations between evolutionary lineages. Alternatively, they take the form of balanced polymorphisms that segregate within populations until one arrangement becomes fixed. Many questions remain about how inversion arise, are maintained over long term, ultimately, whether contribute to speciation. The long‐snouted seahorse ( Hippocampus guttulatus ) is genetically subdivided into geographic lineages marine‐lagoon ecotypes, with shared structural variation underlying lineage ecotype divergence. Here, we aim characterize variants reconstruct their history suspected formation. We generated a near chromosome‐level genome assembly described genome‐wide patterns diversity through analysis 112 whole‐genome sequences from Atlantic, Mediterranean, Black Sea populations. By also analysing linked‐read sequencing data, found evidence for two chromosomal were several megabases length showed contrasting allele frequency ecotypes across species range. reveal these represent ancient intraspecific polymorphisms, likely being divergent selection other pseudo‐overdominance. A possible selective coupling was further supported absence specific haplotype putative functional interaction reproduction. Lastly, detected gene flux eroding inverted alleles at varying levels inversions, impact on dynamics contribution

Language: Английский

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A supergene underlies linked variation in color and morphology in a Holarctic songbird

Nature Communications, Journal Year: 2021, Volume and Issue: 12(1)

Published: Nov. 25, 2021

Abstract The genetic architecture of a phenotype can have considerable effects on the evolution trait or species. Characterizing provides insight into complexity given and, potentially, role in evolutionary processes like speciation. We use genome sequences to investigate basis phenotypic variation redpoll finches ( Acanthis spp.). demonstrate that is broadly controlled by ~55-Mb chromosomal inversion. Within this inversion, we find multiple candidate genes related melanogenesis, carotenoid coloration, and bill shape, suggesting inversion acts as supergene controlling linked traits. A latitudinal gradient ecotype distribution suggests driven color morphology are likely under environmental selection, maintaining haplotypes balanced polymorphism. Our results provide mechanism for maintenance redpolls despite largely homogenized gene flow.

Language: Английский

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Natural selection and the distribution of chromosomal inversion lengths

Molecular Ecology, Journal Year: 2021, Volume and Issue: 31(13), P. 3627 - 3641

Published: July 23, 2021

Chromosomal inversions contribute substantially to genome evolution, yet the processes governing their evolutionary dynamics remain poorly understood. Theory suggests that a readily measurable property of inversions-their length-can potentially affect fates. Emerging data on lengths polymorphic and fixed may therefore provide clues promoting inversion establishment. However, formal predictions for distribution incomplete, making empirical patterns difficult interpret. We model relation between length establishment probability four types: (1) neutral, (2) underdominant, (3) directly beneficial, (4) indirectly with selection favouring latter because they capture locally adapted alleles at migration-selection balance suppress recombination them. also consider how deleterious mutations established inversions. show distributions common systematically differ among types. Small rearrangements most evolution under neutral underdominant scenarios selection, substitutions increasing, those decreasing, effective population size. Among beneficial inversions, small are preferentially fixed, whereas intermediate-to-large maintained as balanced polymorphisms via associative overdominance. Finally, local adaptation scenario predominantly intermediate-to-large. Such or approach fixation within populations where favoured. Our models clarify relate establishment, providing platform testing natural shapes structure.

Language: Английский

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Mutation Load in Sunflower Inversions Is Negatively Correlated with Inversion Heterozygosity

Molecular Biology and Evolution, Journal Year: 2022, Volume and Issue: 39(5)

Published: May 1, 2022

Abstract Recombination is critical both for accelerating adaptation and purging deleterious mutations. Chromosomal inversions can act as recombination modifiers that suppress local in heterozygotes thus, under some conditions, are predicted to accumulate such In this study, we investigated patterns of recombination, transposable element abundance, coding sequence evolution across the genomes 1,445 individuals from three sunflower species, well within nine segregating species. We also analyzed effects inversion genotypes on 87 phenotypic traits test overdominance. found significant negative correlations long terminal repeat retrotransposon abundance mutations with rates genome all However, failed detect an increase these features inversions, except a modest proportion stop codon several very large or rare inversions. Consistent finding, there was little evidence overdominance phenotypes may relate fitness. On other hand, significantly greater load observed populations polymorphic given compared monomorphic one arrangements, suggesting state polymorphism affects load. These seemingly contradictory results be explained by low frequency wild populations, apparently due divergent selection associated geographic structure. Inversions contributing represent ideal modifiers, acting facilitate adaptive divergence gene flow, while largely escaping accumulation

Language: Английский

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Inversions and parallel evolution

Philosophical Transactions of the Royal Society B Biological Sciences, Journal Year: 2022, Volume and Issue: 377(1856)

Published: June 13, 2022

Local adaptation leads to differences between populations within a species. In many systems, similar environmental contrasts occur repeatedly, sometimes driving parallel phenotypic evolution. Understanding the genomic basis of local and evolution is major goal evolutionary genomics. It now known that by preventing break-up favourable combinations alleles across multiple loci, genetic architectures reduce recombination, like chromosomal inversions, can make an important contribution adaptation. However, little about whether inversions also contribute disproportionately Our aim here highlight this knowledge gap, showcase existing studies, illustrate with without using simple models. We predict generating stronger effective selection, speed up adaptive process or enable where it would be impossible otherwise, but highly dependent on spatial setting. further empirical work needed, in particular cover broader taxonomic range understand relative importance compared regions inversions. This article part theme issue ‘Genomic architecture supergenes: causes consequences’.

Language: Английский

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Structural Variants and Speciation: Multiple Processes at Play

Cold Spring Harbor Perspectives in Biology, Journal Year: 2023, Volume and Issue: 16(3), P. a041446 - a041446

Published: Dec. 5, 2023

Emma L. Berdan1,2, Thomas G. Aubier3,4, Salvatore Cozzolino5, Rui Faria6,7, Jeffrey Feder8, Mabel D. Giménez9,10, Mathieu Joron11, Jeremy B. Searle12 and Claire Mérot13 1Department of Marine Sciences, Gothenburg University, 40530, Sweden 2Bioinformatics Core, Department Biostatistics, Harvard T.H. Chan School Public Health, Medical School, Boston, Massachusetts 02115, USA 3Laboratoire Évolution & Diversité Biologique, Université Paul Sabatier Toulouse III, UMR 5174, CNRS/IRD, 31077 Toulouse, France 4Department Biology, University North Carolina at Chapel Hill, 27599, 5Department Naples Federico II, Complesso Universitario di Monte S. Angelo, 80126 Napoli, Italia 6CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO, Laboratório Associado, Universidade do Porto, Vairão, Portugal 7BIOPOLIS Program in Genomics, Biodiversity Land Planning, CIBIO, 4485-661 8Department Biological Notre Dame, Indiana 46556, 9Consejo Nacional Investigaciones Científicas y Técnicas (CONICET), Instituto Genética Humana Misiones (IGeHM), Parque la Salud Provincia "Dr. Ramón Madariaga," N3300KAZ Posadas, Misiones, Argentina 10Facultad Ciencias Exactas, Químicas Naturales, Universidad N3300LQH 11Centre d'Ecologie Fonctionnelle et Evolutive, Montpellier, CNRS, EPHE, IRD, 12Department Ecology Evolutionary Cornell Ithaca, New York 14853, 13CNRS, 6553 Ecobio, OSUR, Rennes, 35000 Correspondence: claire.merot{at}gmail.com; emma.berdan{at}gmail.com

Language: Английский

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Introgression dynamics of sex-linked chromosomal inversions shape the Malawi cichlid adaptive radiation

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: July 29, 2024

Abstract Chromosomal inversions contribute to adaptive speciation by linking co-adapted alleles. Querying 1,375 genomes of the species-rich Malawi cichlid fish radiation, we discovered five large segregating in benthic subradiation that each suppress recombination over more than half a chromosome. Two were transferred from deepwater pelagic Diplotaxodon via admixture, while others established early deep clade. Introgression haplotypes lineages inside and outside radiation coincided with bursts species diversification. Inversions show evidence for transient sex linkage striking excess protein changing substitutions points towards selection on neuro-sensory, physiological reproductive genes. We conclude repeated interplay between depth adaptation sex-specific has been central evolution this iconic system.

Language: Английский

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The interplay of local adaptation and gene flow may lead to the formation of supergenes

Molecular Ecology, Journal Year: 2024, Volume and Issue: unknown

Published: Feb. 28, 2024

Supergenes are genetic architectures resulting in the segregation of alternative combinations alleles underlying complex phenotypes. The co-segregation at linked loci is often facilitated by polymorphic chromosomal rearrangements suppressing recombination locally. involved many polymorphisms, including sexual, colour or behavioural polymorphisms numerous plants, fungi, mammals, fish, and insects. Despite a long history empirical theoretical research, formation supergenes remains poorly understood. Here, using two-island population model, we explore how gene flow evolution overdominant inversions may jointly lead to supergenes. We show that differentiated populations, both under disruptive selection, leads an increase frequency adapted, immigrant haplotypes. Indeed, rare allelic combinations, such as haplotypes, more frequently reshuffled than common therefore benefit from suppression generated inversions. When inversion capturing locally adapted haplotype spreads but associated with fitness cost hampering its fixation (e.g. recessive mutation load), maintenance non-inverted enhanced; certain conditions, persists alongside inverted local haplotype, while standard disappears. This establishes stable, polymorphism two non-recombining haplotypes encoding adaptive strategies, is, supergene. These results bring new light importance adaptation, overdominance, general.

Language: Английский

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