How chromosomal inversions reorient the evolutionary process

Journal of Evolutionary Biology, Journal Year: 2023, Volume and Issue: 36(12), P. 1761 - 1782

Published: Nov. 9, 2023

Abstract Inversions are structural mutations that reverse the sequence of a chromosome segment and reduce effective rate recombination in heterozygous state. They play major role adaptation, as well other evolutionary processes such speciation. Although inversions have been studied since 1920s, they remain difficult to investigate because reduced conferred by them strengthens effects drift hitchhiking, which turn can obscure signatures selection. Nonetheless, numerous found be under Given recent advances population genetic theory empirical study, here we review how different mechanisms selection affect evolution inversions. A key difference between mutations, single nucleotide variants, is fitness an inversion may affected larger number frequently interacting processes. This considerably complicates analysis causes underlying We discuss extent these disentangled, approach. often roles adaptation speciation, but direct their obscured characteristic makes so unique (reduced arrangements). In this review, examine impact evolution, weaving together both theoretical studies. emphasize most patterns overdetermined (i.e. caused multiple processes), highlight new technologies provide path forward towards disentangling mechanisms.

Language: Английский

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Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci

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

Published: June 13, 2022

Supergenes are genetic architectures associated with discrete and concerted variation in multiple traits. It has long been suggested that supergenes control these complex polymorphisms by suppressing recombination between sets of coadapted genes. However, because suppression hinders the dissociation individual effects genes within supergenes, there is still little evidence evolve tightening linkage Here, combining a landmark-free phenotyping algorithm multivariate genome-wide association studies, we dissected basis wing pattern butterfly Heliconius numata . We show supergene controlling striking polymorphism displayed this species contains several independent loci different features patterns. The three chromosomal inversions suppress loci, supporting hypothesis they may have evolved captured beneficial combinations alleles. Some are, however, colour variations only subset morphs where phenotype controlled derived inversion forms, indicating were recruited after formation inversions. Our study shows clusters adaptive general form via evolution rearrangements co-adapted but also subsequent recruitment linked mutations. This article part theme issue ‘Genomic architecture supergenes: causes evolutionary consequences’.

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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A micro-RNA is the effector gene of a classic evolutionary hotspot locus

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

Published: Feb. 12, 2024

In Lepidoptera (butterflies and moths), a genomic region around the gene cortex is hotspot locus, repeatedly used to generate intraspecific melanic wing color polymorphisms across 100-million-years of evolution. However, identity effector regulating within this locus remains unknown. Here, we show that none four candidate protein-coding genes including cortex, serve as major effectors. Instead, micro-RNA (miRNA), mir-193, serves three deeply diverged lineages butterflies, its function conserved in Drosophila. Lepidoptera, mir-193 derived from gigantic long non-coding RNA, ivory, it functions by directly repressing multiple pigmentation genes. We miRNA can drive repeated instances adaptive evolution animals.

Language: Английский

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A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies

Proceedings of the National Academy of Sciences, Journal Year: 2024, Volume and Issue: 121(36)

Published: Aug. 30, 2024

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples adaptation by crypsis mimicry. The

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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The emergence of supergenes from inversions in Atlantic salmon

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

Published: June 13, 2022

Supergenes link allelic combinations into non-recombining units known to play an essential role in maintaining adaptive genetic variation. However, because supergenes can be maintained over millions of years by balancing selection and typically exhibit strong recombination suppression, both the underlying functional variants how are formed largely unknown. Particularly, questions remain importance inversion breakpoint sequences whether capture pre-existing variation or accumulate this following suppression. To investigate process supergene formation, we identified polymorphisms Atlantic salmon assembling eleven genomes with nanopore long-read sequencing technology. A genome assembly from sister species, brown trout, was used determine standard state inversions. We found evidence for through genotype–environment associations, but not accumulation deleterious mutations. One young 3 Mb segregating North American populations has captured that is still within arrangement inversion, while some accumulated after inversion. This two others had breakpoints disrupting genes. Three multigene inversions matched repeat structures at did show any signatures, suggesting shared repeats may obstruct formation. article part theme issue ‘Genomic architecture supergenes: causes evolutionary consequences’.

Language: Английский

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Genomic architecture of supergenes: connecting form and function

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

Published: June 13, 2022

Supergenes are tightly linked sets of loci that inherited together and control complex phenotypes. While classical supergenes-governing traits such as wing patterns in Heliconius butterflies or heterostyly Primula-have been studied since the Modern Synthesis, we still understand very little about how they evolve persist nature. The genetic architecture supergenes is a critical factor affecting their evolutionary fate, it can change key parameters recombination rate effective population size, potentially redirecting molecular evolution supergene addition to surrounding genomic region. To evolution, must link with processes. This now becoming possible recent advances sequencing technology powerful forward computer simulations. present theme issue brings theoretical empirical papers, well opinion synthesis which showcase architectural diversity connect this processes polymorphism maintenance mutation accumulation. Here, summarize those insights highlight new ideas methods illuminate path for study article part 'Genomic supergenes: causes consequences'.

Language: Английский

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Genomic architecture and functional effects of potential human inversion supergenes

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

Published: June 13, 2022

Supergenes are involved in adaptation multiple organisms, but they little known humans. Genomic inversions the most common mechanism of supergene generation and maintenance. Here, we review information about two large that best examples potential human supergenes. In addition, do an integrative analysis newest data to understand better their functional effects underlying genetic changes. We have found highly divergent haplotypes 17q21.31 inversion approximately 1.5 Mb phenotypic associations, with consistent brain-related traits, red white blood cells, lung function, male female characteristics disease risk. By combining gene expression nucleotide variation data, also analysed molecular differences between haplotypes, including duplications, amino acid substitutions regulatory changes, identify CRHR1, KANLS1 MAPT as good candidates be responsible for these phenotypes. The situation is more complex 8p23.1 inversion, where there no clear differentiation. However, associated several related phenotypes could linked specific one orientation. Our work, therefore, contributes characterization both exceptional variants illustrates important role inversions. This article part theme issue 'Genomic architecture supergenes: causes evolutionary consequences'.

Language: Английский

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A long non-coding RNA at thecortexlocus controls adaptive colouration in butterflies

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

Published: Feb. 12, 2024

Abstract Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples adaptation by crypsis mimicry. The cortex locus has been independently mapped as controlling colour polymorphisms 14 lepidopteran species, suggesting it acts a genomic hotspot for diversification patterns, but functional validation through protein-coding knockouts proven difficult to obtain. Our study unveils role novel long non-coding RNA (lncRNA) which we name ivory , transcribed from locus, modulating patterning butterflies. Strikingly, expression prefigures most melanic patterns during pupal development, an early developmental specifying scale identity. To test this, generated CRISPR mosaic knock-outs five nymphalid butterfly species show that mutagenesis yields transformations dark pigmented scales into white or light-coloured scales. Genotyping Vanessa cardui germline mutants associates these phenotypes small on-target deletions at conserved first exon . In contrast, mutant with confirmed null alleles lack any phenotype, exclude this adjacent gene. Overall, results lncRNA master switch pattern specification, played key roles adaptive Significance statement Deciphering genetic underpinnings is fundamental comprehensive understanding evolutionary processes. Long RNAs (lncRNAs) represent emerging category modulators within genome, yet they have overlooked source phenotypic diversity. study, unveil pivotal orchestrating transitions between light development. Remarkably, gene nested region known control multiple cases moths, including iconic natural selection. These findings highlight significant influence lncRNAs regulation, also underscore their potential players process itself.

Language: Английский

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