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Janine A. Clayton and Francis S. Collins unveil policies to ensure that preclinical research funded by the US National Institutes of Health considers females and males.

Chromosome rearrangements are arguably the most dramatic type of mutations, often leading to rapid evolution and speciation. However, chromosome dynamics have only been studied at the sequence level in a small number of model systems. In insects, Diptera and Lepidoptera have conserved genome structure at the scale of whole chromosomes or chromosome arms. Whether this reflects the diversity of insect genome evolution is questionable given that many species exhibit rapid karyotype evolution. Here, we investigate chromosome evolution in aphids—an important group of hemipteran plant pests—using newly generated chromosome-scale genome assemblies of the green peach aphid (Myzus persicae) and the pea aphid (Acyrthosiphon pisum), and a previously published assembly of the corn-leaf aphid (Rhopalosiphum maidis). We find that aphid autosomes have undergone dramatic reorganization over the last 30 My, to the extent that chromosome homology cannot be determined between aphids from the tribes Macrosiphini (Myzus persicae and Acyrthosiphon pisum) and Aphidini (Rhopalosiphum maidis). In contrast, gene content of the aphid sex (X) chromosome remained unchanged despite rapid sequence evolution, low gene expression, and high transposable element load. To test whether rapid evolution of genome structure is a hallmark of Hemiptera, we compared our aphid assemblies with chromosome-scale assemblies of two blood-feeding Hemiptera (Rhodnius prolixus and Triatoma rubrofasciata). Despite being more diverged, the blood-feeding hemipterans have conserved synteny. The exceptional rate of structural evolution of aphid autosomes renders them an important emerging model system for studying the role of large-scale genome rearrangements in evolution.

Major changes in chromosome number and structure are linked to a series of evolutionary phenomena, including intrinsic barriers to gene flow or suppression of recombination due to chromosomal rearrangements. However, chromosome rearrangements can also affect the fundamental dynamics of molecular evolution within populations by changing relationships between linked loci and altering rates of recombination. Here, we build chromosome-level assembly Eueides isabella and, together with a recent chromosome-level assembly of Dryas iulia, examine the evolutionary consequences of multiple chromosome fusions in Heliconius butterflies. These assemblies pinpoint fusion points on 10 of the 20 autosomal chromosomes and reveal striking differences in the characteristics of fused and unfused chromosomes. The ten smallest autosomes in D. iulia and E. isabella, which have each fused to a longer chromosome in Heliconius, have higher repeat and GC content, and longer introns than predicted by their chromosome length. When fused, these characteristics change to become more in line with chromosome length. The fusions also led to reduced diversity, which likely reflects increased background selection and selection against introgression between diverging populations, following a reduction in per-base recombination rate. We further show that chromosome size and fusion impact turnover rates of functional loci at a macroevolutionary scale. Together these results provide further evidence that chromosome fusion in Heliconius likely had dramatic effects on population level processes shaping rates of neutral and adaptive divergence. These effects may have impacted patterns of diversification in Heliconius, a classic example of an adaptive radiation.

Heteromorphic sex chromosomes are usually thought to have originated from a pair of autosomes that acquired a sex-determining locus and subsequently stopped recombining, leading to degeneration of the sex-limited chromosome. The majority of nematode species lack heteromorphic sex chromosomes and determine sex using an X-chromosome counting mechanism, with males being hemizygous for one or more X chromosomes (XX/X0). Some filarial nematode species, including important parasites of humans, have heteromorphic XX/XY karyotypes. It has been assumed that sex is determined by a Y-linked locus in these species. However, karyotypic analyses suggested that filarial Y chromosomes are derived from the unfused homologue of an autosome involved in an X-autosome fusion event. Here, we generated a chromosome-level reference genome for Litomosoides sigmodontis , a filarial nematode with the ancestral filarial karyotype and sex determination mechanism (XX/X0). By mapping the assembled chromosomes to the rhabditid nematode ancestral linkage (or Nigon) elements, we infer that the ancestral filarial X chromosome was the product of a fusion between NigonX (the ancestrally X-linked element) and NigonD (ancestrally autosomal). In the two filarial lineages with XY systems, there have been two independent X-autosome chromosome fusion events involving different autosomal Nigon elements. In both lineages, the region shared by the neo-X and neo-Y chromosomes is within the ancestrally autosomal portion of the X, confirming that the filarial Y chromosomes are derived from the unfused homologue of the autosome. Sex determination in XY filarial nematodes therefore likely continues to operate via the ancestral X-chromosome counting mechanism, rather than via a Y-linked sex-determining locus.

Abstract The relatively young and repeated evolutionary origins of dioecy (separate sexes) in flowering plants enables the investigation of molecular dynamics occurring at the earliest stages of sex chromosome evolution. With two independently young origins of dioecy, Asparagus is a model genus for studying the genetics of sex-determination and sex chromosome evolution. Dioecy first evolved in Asparagus ∼3 to 4 million years ago (Ma) in the ancestor of a now widespread Eurasian clade including garden asparagus (Asparagus officinalis). A second origin occurred in a smaller, geographically restricted, Mediterranean Basin clade, including Asparagus horridus. New haplotype-resolved reference genomes for garden asparagus and A. horridus, elucidate contrasting first steps in the origin of the sex chromosomes of the Eurasian and Mediterranean Basin clade ancestors. Analysis of the A. horridus genome revealed an XY system derived from a different ancestral pair of autosomes with different sex-determining genes than have been characterized for garden asparagus. We estimate that proto-XY chromosomes evolved 1 to 2 Ma in the Mediterranean Basin clade, following a ∼2.1-megabase inversion that now distinguishes the X and Y chromosomes. Recombination suppression and LTR retrotransposon accumulation drove the expansion of the male-specific region on the Y (MSY) that reaches ∼9.6-megabases in A. horridus. The garden asparagus genome revealed an MSY spanning ∼1.9-megabases. A segmental duplication and neofunctionalization of one duplicated gene (SOFF) drove the origin of dioecy in the Eurasian clade. These findings support previous inference based on phylogeographic analysis revealing two recent origins of dioecy in Asparagus and establish the genus as a model for investigating sex chromosome evolution.

Chromosomal inversions have the potential to play an important role in evolution by reducing recombination between favorable combinations of alleles. Until recently, however, most evidence for their likely importance derived from dipteran flies, whose giant larval salivary chromosomes aided early cytogenetic studies. The widespread application of new genomic technologies has revealed that inversions are ubiquitous across much of the plant and animal kingdoms. Here we review the rapidly accumulating literature on inversions in the plant kingdom and discuss what we have learned about their establishment and likely evolutionary role. We show that inversions are prevalent across a wide range of plant groups. We find that inversions are often associated with locally favored traits, as well as with traits that contribute to assortative mating, suggesting that they may be key to adaptation and speciation in the face of gene flow. We also discuss the role of inversions in sex chromosome formation, and explore possible parallels with inversion establishment on autosomes. The identification of inversion origins, as well as the causal variants within them, will advance our understanding of chromosomal evolution in plants.

Genome structural variations, including duplications, deletions, insertions, and inversions, are central in the evolution of eukaryotic genomes. However, structural variations present challenges for high-quality genome assembly, hampering efforts to understand the evolution of gene families and genome architecture. An example is the genome of the pea aphid (Acyrthosiphon pisum) for which the current assembly is composed of thousands of short scaffolds, many of which are known to be misassembled. Here, we present an improved version of the A. pisum genome based on the use of two long-range proximity ligation methods. The new assembly contains four long scaffolds (40–170 Mb), corresponding to the three autosomes and the X chromosome of A. pisum, and encompassing 86% of the new assembly. Assembly accuracy is supported by several quality assessments. Using this assembly, we identify the chromosomal locations and relative ages of duplication events, and the locations of horizontally acquired genes. The improved assembly illuminates the mode of gene family evolution by providing proximity information between paralogs. By estimating nucleotide polymorphism and coverage depth from resequencing data, we determined that many short scaffolds not assembling to chromosomes represent hemizygous regions, which are especially frequent on the highly repetitive X chromosome. Aligning the X-linked aphicarus region, responsible for male wing dimorphism, to the new assembly revealed a 50-kb deletion that cosegregates with the winged male phenotype in some clones. These results show that long-range scaffolding methods can substantially improve assemblies of repetitive genomes and facilitate study of gene family evolution and structural variation.

Abstract How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (My) of divergence and degeneration obscure their evolutionary history. The Sylvioidea group of songbirds is interesting for understanding avian sex chromosome evolution because a chromosome fusion event ∼24 Ma formed “neo-sex chromosomes” consisting of an added (new) and an ancestral (old) part. Here, we report the complete female genome (ZW) of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). Our long-read assembly shows that the added region has been translocated to both Z and W, and whereas the added-Z has retained its gene order the added-W part has been heavily rearranged. Phylogenetic analyses show that recombination between the homologous added-Z and -W regions continued after the fusion event, and that recombination suppression across this region took several million years to be completed. Moreover, recombination suppression was initiated across multiple positions over the added-Z, which is not consistent with a simple linear progression starting from the fusion point. As expected following recombination suppression, the added-W show signs of degeneration including repeat accumulation and gene loss. Finally, we present evidence for nonrandom maintenance of slowly evolving and dosage-sensitive genes on both ancestral- and added-W, a process causing correlated evolution among orthologous genes across broad taxonomic groups, regardless of sex linkage.

Beetles are the most species-rich group of animals and harbor diverse karyotypes. Most species have XY sex chromosomes, but X0 sex determination mechanisms are also common in some groups. We generated a whole-chromosome assembly of Tribolium confusum , which has a neo-sex chromosome, and utilize eleven additional beetle genomes to reconstruct karyotype evolution across Coleoptera. We identify ancestral linkage groups, termed Stevens elements, that share a conserved set of genes across beetles. While the ancestral X chromosome is maintained across beetles, we find independent additions of autosomes to the ancestral sex chromosomes. These neo-sex chromosomes evolve the stereotypical properties of sex chromosomes, including the evolution of dosage compensation and a non-random distribution of genes with sex-biased expression. Beetles thus provide a novel model to gain a better understanding of the diverse forces driving sex chromosome evolution.

Current phylogenomic approaches implicitly assume that the predominant phylogenetic signal within a genome reflects the true evolutionary history of organisms, without assessing the confounding effects of postspeciation gene flow that can produce a mosaic of phylogenetic signals that interact with recombinational variation. Here, we tested the validity of this assumption with a phylogenomic analysis of 27 species of the cat family, assessing local effects of recombination rate on species tree inference and divergence time estimation across their genomes. We found that the prevailing phylogenetic signal within the autosomes is not always representative of the most probable speciation history, due to ancient hybridization throughout felid evolution. Instead, phylogenetic signal was concentrated within regions of low recombination, and notably enriched within large X chromosome recombination cold spots that exhibited recurrent patterns of strong genetic differentiation and selective sweeps across mammalian orders. By contrast, regions of high recombination were enriched for signatures of ancient gene flow, and these sequences inflated crown-lineage divergence times by ∼40%. We conclude that existing phylogenomic approaches to infer the Tree of Life may be highly misleading without considering the genomic architecture of phylogenetic signal relative to recombination rate and its interplay with historical hybridization.