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

---

A cosmopolitan inversion facilitates seasonal adaptation in overwintering Drosophila

Genetics, Journal Year: 2023, Volume and Issue: 226(2)

Published: Dec. 5, 2023

Abstract Fluctuations in the strength and direction of natural selection through time are a ubiquitous feature life on Earth. One evolutionary outcome such fluctuations is adaptive tracking, wherein populations rapidly adapt from standing genetic variation. In certain circumstances, tracking can lead to long-term maintenance functional polymorphism despite allele frequency change due selection. Although likely common process, we still have limited understanding aspects its architecture relative other forces as drift. Drosophila melanogaster living temperate regions evolve track seasonal an excellent system tackle these gaps knowledge. By sequencing orchard collected across multiple years, characterized genomic signal demography identified that cosmopolitan inversion In(2L)t facilitates shows molecular footprints A meta-analysis phenotypic studies loci within associated with behavior, history, physiology, morphological traits. We identify candidate experimentally link them phenotype. Our work contributes our general fluctuating highlights dynamics contemporary inversions.

Language: Английский

---

The evolutionary dynamics of locally adaptive chromosome inversions inMimulus guttatus

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: Dec. 8, 2023

Abstract Chromosomal inversion polymorphisms are ubiquitous across the diversity of diploid organisms and play a significant role in evolution adaptations those species. Inversions thought to operate as supergenes by trapping adaptive alleles at multiple linked loci through suppression recombination. While there is now considerable support for supergene mechanism evolution, extent which inversions trap pre-existing genetic variation versus accumulate new variants over time remains unclear. In this study, we report insights into evolutionary dynamics locally chromosomal polymorphism (inv_chr8A), contributes divergence between coastal perennial inland annual ecotypes yellow monkeyflower, Mimulus guttatus . This research was enabled sequencing, assembly, annotation genomes M. using Oxford Nanopore long-read sequencing technology. addition inv_chr8A inversion, identified three other large polymorphisms, including previously unknown (inv_chr8B) nested within inv_chr8A. Through population genomic analyses comparative genomics, determined that inv_chr8B significantly older than larger it resides. We also evaluated key candidate genes involved gibberellin biosynthesis anthocyanin regulation, hypothesize underlie phenotypic effects inversion. Although little evidence found suggest breakpoint mutations drive effects, our findings dynamic continuous process.

Language: Английский

---

Inversions Can Accumulate Balanced Sexual Antagonism: Evidence from Simulations and Drosophila Experiments

Published: Jan. 23, 2025

Chromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for maintenance polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one has negative frequency-dependent fitness. These conditions yield form disruptive selection, favoring predominant haplotypes segregating alleles favor opposing antagonistic phenotypes. An associated with haplotype reduce fitness load incurred by generating recombinant offspring, reinforcing its linkage and enabling both accumulate more than expected otherwise. develop apply forward simulator examine these dynamics under tradeoff between survival male display. simulations indeed generate inversion-associated sex-specific effects. Antagonism strengthens time, ultimately karyotypes at surprisingly predictable frequencies, striking genotype frequency differences sexes developmental stages. To test whether this may well-studied yet enigmatic in Drosophila melanogaster , we track frequencies laboratory crosses they influence reproductive success or survival. find four tested inversions show significant evidence examined, In(3R)K In(3L)Ok reproduction. In line apparent effects implied those inversions, was also found less costly viability and/or longevity males females, whereas beneficial female Based on work, expect balancing selection pleiotropic traits provide underappreciated contribution natural polymorphism.

Language: Английский

---

Incomplete recombination suppression fuels extensive haplotype diversity in a butterfly colour pattern supergene

PLoS Biology, Journal Year: 2025, Volume and Issue: 23(2), P. e3003043 - e3003043

Published: Feb. 28, 2025

Supergenes can evolve when recombination-suppressing mechanisms like inversions promote co-inheritance of alleles at two or more polymorphic loci that affect a complex trait. Theory shows such genetic architectures be favoured under balancing selection local adaptation in the face gene flow, but they also bring costs associated with reduced opportunities for recombination. These may turn offset by rare ‘gene flux’ between inverted and ancestral haplotypes, range possible outcomes. We aimed to shed light on these processes investigating BC supergene, large genomic region comprising multiple rearrangements three distinct wing colour morphs Danaus chrysippus , butterfly known as African monarch, queen plain tiger. Using whole-genome resequencing data from 174 individuals, we first confirm effects pattern: background melanism is SNPs promoter yellow within an subregion while forewing tip pattern most likely copy-number variation separate supergene. then show haplotype diversity supergene surprisingly extensive: there are least six divergent groups experience suppressed recombination respect each other. Despite high divergence groups, identify unexpectedly number natural recombinant haplotypes. Several inferred crossovers occurred adjacent inversion ‘modules’, others inversions. Furthermore, new have arisen through pre-existing ones. Specifically, allele dark colouration has recombined into backgrounds occasions. Overall, our findings paint picture dynamic evolution fuelled incomplete suppression.

Language: Английский

---

The Evolution of Locally Adaptive Chromosome Inversions in Mimulus guttatus

Molecular Ecology, Journal Year: 2025, Volume and Issue: unknown

Published: March 5, 2025

Chromosomal inversion polymorphisms are ubiquitous across the diversity of diploid organisms and play a significant role in evolution adaptations those species. Inversions thought to operate as supergenes by trapping adaptive alleles at multiple linked loci through suppression recombination. While there is now considerable support for supergene mechanism evolution, extent which inversions trap pre-existing genetic variation versus accumulate new variants over time remains unclear. In this study, we report insights into locally chromosomal polymorphism (inv_chr8A), contributes divergence between coastal perennial inland annual ecotypes yellow monkeyflower, Mimulus guttatus. This research was enabled sequencing, assembly annotation genomes M. guttatus using Oxford Nanopore long-read sequencing technology. addition inv_chr8A inversion, identified three other large polymorphisms, including previously unknown (inv_chr8B) nested within inv_chr8A. Through population genomic analyses, determined that inv_chr8B significantly older than larger it resides. We also evaluated potential key candidate genes underlying phenotypic effects These involved gibberellin biosynthesis anthocyanin regulation. Although little evidence found suggest breakpoint mutations drive effects, our findings do adaptation may sometimes involve evolve different times.

Language: Английский

---

(Limited) Predictability of thermal adaptation in invertebrates

Journal of Experimental Biology, Journal Year: 2025, Volume and Issue: 228(5)

Published: March 1, 2025

Evolutionary genomic approaches provide powerful tools to understand variation in and evolution of physiological processes. Untargeted or transcriptomic screens can identify functionally annotated candidate genes linked specific processes, turn suggesting evolutionary roles for these Such studies often aim inform modeling the potential natural populations adapt climate change, but models are most accurate when responses repeatable, thus predictable. Here, we synthesize genetic comparative literature on terrestrial marine invertebrates assess whether temperature repeatable within populations, across species. There is compelling evidence repeatability, sometimes even However, laboratory selection geographic thermal gradients appear be highly idiosyncratic. We also survey genetic/transcriptomic repeatedly three functional groups previously associated with response stress: heat shock protein (Hsp) genes, proteolysis immunity genes. Multiple species candidates included gene sets. Yet, each sets identified only a minority studies. Together, patterns suggest that there limited predictability selection, including discuss sets, implications predictive modeling, other applications genetics elucidating physiology function. Finally, limitations inferences from available directions future research.

Language: Английский

---

The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments

eLife, Journal Year: 2025, Volume and Issue: 12

Published: April 16, 2025

Chromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for maintenance polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one has negative frequency-dependent fitness. These conditions yield form disruptive selection, favoring predominant haplotypes segregating alleles favor opposing antagonistic phenotypes. An associated with haplotype reduce fitness load incurred by generating recombinant offspring, reinforcing its linkage and enabling both accumulate more than expected otherwise. develop apply forward simulator examine these dynamics under tradeoff between survival male display. simulations indeed generate inversion-associated sex-specific effects. Antagonism strengthens time, ultimately karyotypes at surprisingly predictable frequencies, striking genotype frequency differences sexes developmental stages. To test whether this may well-studied yet enigmatic in Drosophila melanogaster , we track frequencies laboratory crosses they influence reproductive success or survival. find four tested inversions show significant evidence examined, In(3 R)K L)Ok reproduction. In line apparent effects implied those inversions, was also found less costly viability and/or longevity males females, whereas beneficial female Based on work, expect balancing selection pleiotropic traits provide underappreciated contribution natural polymorphism.

Language: Английский

---

The effects of inversion polymorphisms on patterns of neutral genetic diversity

Genetics, Journal Year: 2023, Volume and Issue: 224(4)

Published: June 22, 2023

The strong reduction in the frequency of recombination heterozygotes for an inversion and a standard gene arrangement causes arrangements to become partially isolated genetically, resulting sequence divergence between them changes levels neutral variability at nucleotide sites within each class. Previous theoretical studies on effects inversions have assumed either that population is panmictic or it divided into 2 populations subject divergent selection. Here, theory extended model arbitrary number demes connected by migration, using finite island with present same all demes. Recursion relations mean pairwise coalescent times are used obtain simple approximate expressions diversity statistics polymorphism equilibrium under drift, approach following sweep stable intermediate frequency. patterns linkage disequilibrium also examined. effective rate caused subdivision can significant these statistics. results discussed relation genomic data polymorphisms, emphasis Drosophila melanogaster. Methods proposed testing whether not close recombination-drift equilibrium, estimating recombinational exchange inversions; difficulties involved ages discussed.

Language: Английский

---

The fitness consequences of genetic divergence between polymorphic gene arrangements

Genetics, Journal Year: 2023, Volume and Issue: 226(3)

Published: Dec. 26, 2023

Inversions restrict recombination when heterozygous with standard arrangements, but often have few noticeable phenotypic effects. Nevertheless, there are several examples of inversions that can be maintained polymorphic by strong selection under laboratory conditions. A long-standing model for the source such is divergence between arrangements respect to recessive or partially deleterious mutations, resulting in a selective advantage heterokaryotypic individuals over homokaryotypes. This paper uses combination analytical and numerical methods investigate this model, simple case an autosomal inversion multiple independent nucleotide sites subject mildly mutations. complete lack heterokaryotypes assumed, as well constancy frequency space time. It shown significantly higher mutational load will develop less frequent arrangement. only expected two alternative nearly equal frequency, so their loads very similar size. The effects some Drosophila pseudoobscura on fitness traits seem too large explained process, although it may contribute observed Several population genomic statistics provide evidence signatures reduced efficacy associated rarer currently little published data relevant theoretical predictions.

Language: Английский

---