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Y chromosomes originate from ordinary autosomes and degenerate by accumulating deleterious mutations. This accumulation results from a lack of recombination on the Y and is driven by interference among deleterious mutations (Muller's ratchet and background selection) and the fixation of beneficial alleles (genetic hitchhiking). Here I show that the relative importance of these processes is expected to vary over the course of Y chromosome evolution due to changes in the number of active genes. The dominant mode of degeneration on a newly formed gene-rich Y chromosome is expected to be Muller's ratchet and/or background selection due to the large numbers of deleterious mutations arising in active genes. However, the relative importance of these modes of degeneration declines rapidly as active genes are lost. In contrast, the rate of degeneration due to hitchhiking is predicted to be highest on Y chromosomes containing an intermediate number of active genes. The temporal dynamics of these processes imply that a gradual restriction of recombination, as inferred in mammals, will increase the importance of genetic hitchhiking relative to Muller's ratchet and background selection.

Many species groups, including mammals and many insects, determine sex using heteromorphic sex chromosomes. Diptera flies, which include the model Drosophila melanogaster, generally have XY sex chromosomes and a conserved karyotype consisting of six chromosomal arms (five large rods and a small dot), but superficially similar karyotypes may conceal the true extent of sex chromosome variation. Here, we use whole-genome analysis in 37 fly species belonging to 22 different families of Diptera and uncover tremendous hidden diversity in sex chromosome karyotypes among flies. We identify over a dozen different sex chromosome configurations, and the small dot chromosome is repeatedly used as the sex chromosome, which presumably reflects the ancestral karyotype of higher Diptera. However, we identify species with undifferentiated sex chromosomes, others in which a different chromosome replaced the dot as a sex chromosome or in which up to three chromosomal elements became incorporated into the sex chromosomes, and others yet with female heterogamety (ZW sex chromosomes). Transcriptome analysis shows that dosage compensation has evolved multiple times in flies, consistently through up-regulation of the single X in males. However, X chromosomes generally show a deficiency of genes with male-biased expression, possibly reflecting sex-specific selective pressures. These species thus provide a rich resource to study sex chromosome biology in a comparative manner and show that similar selective forces have shaped the unique evolution of sex chromosomes in diverse fly taxa.

Gene duplication is a key source of genetic innovation that plays a role in the evolution of phenotypic complexity. Although several evolutionary processes can result in the long-term retention of duplicate genes, their relative contributions in nature are unknown. Here we develop a phylogenetic approach for comparing genome-wide expression profiles of closely related species to quantify the roles of conservation, neofunctionalization, subfunctionalization, and specialization in the preservation of duplicate genes. Application of our method to pairs of young duplicates in Drosophila shows that neofunctionalization, the gain of a novel function in one copy, accounts for the retention of almost two-thirds of duplicate genes. Surprisingly, novel functions nearly always originate in younger (child) copies, whereas older (parent) copies possess functions similar to those of ancestral genes. Further examination of such pairs reveals a strong bias toward RNA-mediated duplication events, implicating asymmetric duplication and positive selection in the evolution of new functions. Moreover, we show that young duplicate genes are expressed primarily in testes and that their expression breadth increases over evolutionary time. This finding supports the “out-of-testes” hypothesis, which posits that testes are a catalyst for the emergence of new genes that ultimately evolve functions in other tissues. Thus, our study highlights the importance of neofunctionalization and positive selection in the retention of young duplicates in Drosophila and illustrates how duplicates become incorporated into novel functional networks over evolutionary time.

An autosomal chromosome pair in Drosophila , the dot chromosome, is shown to have evolved from an ancestral X chromosome: these findings explain several previously puzzling aspects of dot chromosome biology and challenge the view that differentiated sex chromosomes represent a terminal evolutionary stage. A former sex chromosome unmasked Sex-determination mechanisms are known to evolve frequently in species with identical sex chromosomes, but distinct sex chromosomes (such as X and Y) are seen as a terminal evolutionary stage resulting from chromosome-specific adaptations such as dosage compensation or an accumulation of sex-specific mutations. Using whole-genome sequencing and comparative genomics, Beatriz Vicoso and Doris Bachtrog show that an autosomal pair in Drosophila , the dot chromosome, evolved from an X chromosome. Their results explain several previously puzzling aspects of the biology of the Drosophila dot chromosome as remnants of its former life as a sex chromosome. Although transitions of sex-determination mechanisms are frequent in species with homomorphic sex chromosomes 1 , 2 , 3 , heteromorphic sex chromosomes are thought to represent a terminal evolutionary stage owing to chromosome-specific adaptations such as dosage compensation or an accumulation of sex-specific mutations 1 , 4 . Here we show that an autosome of Drosophila , the dot chromosome, was ancestrally a differentiated X chromosome. We analyse the whole genome of true fruitflies (Tephritidae), flesh flies (Sarcophagidae) and soldier flies (Stratiomyidae) to show that genes located on the dot chromosome of Drosophila are X-linked in outgroup species, whereas Drosophila X-linked genes are autosomal. We date this chromosomal transition to early drosophilid evolution by sequencing the genome of other Drosophilidae. Our results reveal several puzzling aspects of Drosophila dot chromosome biology to be possible remnants of its former life as a sex chromosome, such as its minor feminizing role in sex determination 5 or its targeting by a chromosome-specific regulatory mechanism 6 . We also show that patterns of biased gene expression of the dot chromosome during early embryogenesis, oogenesis and spermatogenesis resemble that of the current X chromosome. Thus, although sex chromosomes are not necessarily evolutionary end points and can revert back to an autosomal inheritance, the highly specialized genome architecture of this former X chromosome suggests that severe fitness costs must be overcome for such a turnover to occur.

Sex-chromosomes have formed repeatedly across Diptera from ordinary autosomes, and X-chromosomes mostly conserve their ancestral genes. Y-chromosomes are characterized by abundant gene-loss and an accumulation of repetitive DNA, yet the nature of the gene repertoire of fly Y-chromosomes is largely unknown. Here we trace gene-content evolution of Y-chromosomes across 22 Diptera species, using a subtraction pipeline that infers Y genes from male and female genome, and transcriptome data. Few genes remain on old Y-chromosomes, but the number of inferred Y-genes varies substantially between species. Young Y-chromosomes still show clear evidence of their autosomal origins, but most genes on old Y-chromosomes are not simply remnants of genes originally present on the proto-sex-chromosome that escaped degeneration, but instead were recruited secondarily from autosomes. Despite almost no overlap in Y-linked gene content in different species with independently formed sex-chromosomes, we find that Y-linked genes have evolved convergent gene functions associated with testis expression. Thus, male-specific selection appears as a dominant force shaping gene-content evolution of Y-chromosomes across fly species. While X-chromosome gene content tends to be conserved, Y-chromosome evolution is dynamic and difficult to reconstruct. Here, Mahajan and Bachtrog use a subtraction pipeline to identify Y-linked genes in 22 Diptera species, revealing patterns of Y-chromosome gene-content evolution.

Y chromosomes often contain amplified genes which can increase dosage of male fertility genes and counteract degeneration via gene conversion. Here we identify genes with increased copy number on both X and Y chromosomes in various species of Drosophila, a pattern that has previously been associated with sex chromosome drive involving the Slx and Sly gene families in mice. We show that recurrent X/Y co-amplification appears to be an important evolutionary force that has shaped gene content evolution of sex chromosomes in Drosophila. We demonstrate that convergent acquisition and amplification of testis expressed gene families are common on Drosophila sex chromosomes, and especially on recently formed ones, and we carefully characterize one putative novel X/Y co-amplification system. We find that co-amplification of the S-Lap1/GAPsec gene pair on both the X and the Y chromosome occurred independently several times in members of the D. obscura group, where this normally autosomal gene pair is sex-linked due to a sex chromosome-autosome fusion. We explore several evolutionary scenarios that would explain this pattern of co-amplification. Investigation of gene expression and short RNA profiles at the S-Lap1/GAPsec system suggest that, like Slx/Sly in mice, these genes may be remnants of a cryptic sex chromosome drive system, however additional transgenic experiments will be necessary to validate this model. Regardless of whether sex chromosome drive is responsible for this co-amplification, our findings suggest that recurrent gene duplications between X and Y sex chromosomes could have a widespread effect on genomic and evolutionary patterns, including the epigenetic regulation of sex chromosomes, the distribution of sex-biased genes, and the evolution of hybrid sterility.

Centromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high-quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric and the creation of metacentric chromosomes in some species was driven by de novo seeding of new centromeres at ancestrally gene-rich regions, independently of chromosomal rearrangements. The emergence of centromeres resulted in a drastic size increase due to repeat accumulation, and dozens of genes previously located in euchromatin are now embedded in pericentromeric heterochromatin. Metacentric chromosomes secondarily became telocentric in the pseudoobscura subgroup through centromere repositioning and a pericentric inversion. The former (peri)centric sequences left behind shrunk dramatically in size after their inactivation, yet contain remnants of their evolutionary past, including increased repeat-content and heterochromatic environment. Centromere movements are accompanied by rapid turnover of the major satellite DNA detected in (peri)centromeric regions.

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.

Key Points Recently developed genomic technologies have shed light on the genomic composition of the ancient Y chromosomes of some primates and Drosophila melanogaster and have shown that Y chromosomes in these species largely conform to the previously held view of being degenerate. The presence of evolutionary strata confirmed by genome sequencing of the sex chromosomes supports that Y-chromosome degeneration occurred through successive arrest of recombination over time. In addition, the enrichment of Y chromosomes for genes of male-beneficial functions suggests that sexually antagonistic mutations may have a role in Y-chromosome evolution. Genome sequencing of young Y chromosomes in plants and neo-Y chromosomes in Drosophila spp. have provided insight into the molecular processes that trigger initiation of Y-chromosome degeneration. Empirical evidence suggests that gene silencing occurs before pseudogenization. Empirical observations in Drosophila neo-sex chromosomes, primate Y chromosomes and theoretical models and computer simulations show that degeneration is not a linear process, and so Y chromosomes in these species will probably not completely degenerate in the future. The Y chromosomes of many species, including humans, are gene-poor and degenerate. The recent application of genome-wide technologies to evolutionarily old and young Y chromosomes has provided insight into the processes that have shaped them and their future. The human Y chromosome is intriguing not only because it harbours the master-switch gene that determines gender but also because of its unusual evolutionary history. The Y chromosome evolved from an autosome, and its evolution has been characterized by massive gene decay. Recent whole-genome and transcriptome analyses of Y chromosomes in humans and other primates, in Drosophila species and in plants have shed light on the current gene content of the Y chromosome, its origins and its long-term fate. Furthermore, comparative analysis of young and old Y chromosomes has given further insights into the evolutionary and molecular forces triggering Y-chromosome degeneration and into the evolutionary destiny of the Y chromosome.

Transposable elements (TEs) may contribute to evolutionary innovations through the rewiring of networks by supplying ready-to-use eis regulatory elements. Genes on the Drosophila X chromosome are coordinately regulated by the male specific lethal (MSL) complex to achieve dosage compensation in males. We show that the acquisition of dozens of MSL binding sites on evolutionarily new X chromosomes was facilitated by the independent co-option of a mutant helitron TE that attracts the MSL complex (TE domestication). The recently formed neo-X recruits helitrons that provide dozens of functional, but suboptimal, MSL binding sites, whereas the older XR chromosome has ceased acquisition and appears to have fine-tuned the binding affinities of more ancient elements for the MSL complex. Thus, TE-mediated rewiring of regulatory networks through domestication and amplification may be followed by fine-tuning of the cis-regulatory element supplied by the TE and erosion of nonfunctional regions.