Evolution of the avian sex chromosomes and their role in sex determination

Is it the female-specific W chromosome of birds that causes the avian embryo to develop a female phenotype, analogous to the dominance mode of genic sex differentiation seen in mammals? Or is it the number of Z chromosomes that triggers male development, similar to the balance mode of differentiation seen in Drosophila and Caenorhabditis elegans? Although definite answers to these questions cannot be given yet, some recent data have provided support for the latter hypothesis. Moreover, despite the potentially common features of sex determination in mammals and birds, comparative mapping shows that the avian sex chromosomes have a different autosomal origin than the mammalian X and Y chromosomes.     

Plant sex determination and sex chromosomes

Sex determination systems in plants have evolved many times from hermaphroditic ancestors (including monoecious plants with separate male and female flowers on the same individual), and sex chromosome systems have arisen several times in flowering plant evolution. Consistent with theoretical models for the evolutionary transition from hermaphroditism to monoecy, multiple sex determining genes are involved, including male-sterility and female-sterility factors. The requirement that recombination should be rare between these different loci is probably the chief reason for the genetic degeneration of Y chromosomes. Theories for Y chromosome degeneration are reviewed in the light of recent results from genes on plant sex chromosomes.     

Evolution of fungal sex chromosomes

Sexual reproduction enables organisms to shuffle two parental genomes to produce recombinant progeny, and to purge the genome of deleterious mutations. Sex is conserved in virtually all organisms, from bacteria and fungi to plants and animals, and yet the mechanisms by which sexual identity are established share both conserved general features and are remarkably diverse. In animals, sexual identity is established by dimorphic sex chromosomes, whereas in fungi a specialized region of the genome, known as the mating-type locus, governs the establishment of cell type identity and differs in DNA sequence between cells of different mating-types. Recent studies on the mating-type loci of fungi and algae reveal features shared with the mammalian X and Y chromosomes, suggesting that these represent early steps in the evolution of sex chromosomes.     

Evolution of sex chromosomes in Sauropsida

Reptiles (sauropsids) represent the sister group to mammals, and the basal members of Reptilia may provide a good model for the condition of the common ancestor of both groups. Sex-determining mechanisms (SDM) and organizations of sex chromosomes among genotypically sex-determining (GSD) species vary widely across reptiles. Birds and snakes, for example, are entirely GSD whereas other reptiles, like all crocodilians, exhibit temperature-dependent sex determination (TSD). Here we explore the evolution of sex chromosomes and SDM within reptiles, using family-level analyses of character evolution and applying parsimony, likelihood, Bayesian, and stochastic methods. We find support for the common ancestor of amphisbaenians and whiptail lizards (Laterata) possessing the XY (male heterogametic) GSD mechanism, while the ancestors of Testudines and Crocodylia, as well as the larger group Archosauromorpha (here containing turtles) are inferred to have exhibited TSD. We also find evidence consistent with the hypothesis that the XY system is more labile and evolves faster than does the ZW (female heterogametic) system. Phylogenetic-based speciation tests do not support an association between GSD and speciation, and reject the hypothesis that the presence of the XY system is associated with speciation in reptiles.     

Mammalian sex chromosomes: Evolution of organization and function

Comparisons of chromosome size, morphology and gene arrangements between mammals of different species permit us to deduce the genome characteristics of the common ancestor, and to chart the changes that have occurred during the divergence of the two lineages. The more distantly related are the species compared, the more remote the common ancestor whose characteristics can be deduced. This means that, providing there are sufficient similarities to warrant comparison, the more divergent the species compared, the more significant the contribution to our understanding of the organization of an ancestral mammalian genome and the process of mammalian genome evolution. One of the genetic surprises of the last decade was the discovery that, although gross karyotypes of distantly related orders of eutherian mammals (e.g. cat, cow, rabbit, man) have diverged extensively, gene mapping studies reveal the presence of large chromosome segments conserved across at least 60 million years (O'Brien et al. 1988). This finding makes it worthwhile to extend genetic comparisons to the two groups of mammals most distantly related to eutherian mammals--marsupials and monotremes. Here we will review comparisons of the sex chromosomes in these three major groups of extant mammals, and show how they have led us to a new view of the evolution of mammalian sex chromosome organization and function in sex determination and X chromosome inactivation.     

Cretaceous park of sex determination: sex chromosomes are conserved across iguanas

Many poikilothermic vertebrate lineages, especially among amphibians and fishes, possess a rapid turnover of sex chromosomes, while in endotherms there is a notable stability of sex chromosomes. Reptiles in general exhibit variability in sex-determining systems; as typical poikilotherms, they might be expected to have a rapid turnover of sex chromosomes. However, molecular data which would enable the testing of the stability of sex chromosomes are lacking in most lineages. Here, we provide molecular evidence that sex chromosomes are highly conserved across iguanas, one of the most species-rich clade of reptiles. We demonstrate that members of the New World families Iguanidae, Tropiduridae, Leiocephalidae, Phrynosomatidae, Dactyloidae and Crotaphytidae, as well as of the family Opluridae which is restricted to Madagascar, all share homologous sex chromosomes. As our sampling represents the majority of the phylogenetic diversity of iguanas, the origin of iguana sex chromosomes can be traced back in history to the basal splitting of this group which occurred during the Cretaceous period. Iguanas thus show a stability of sex chromosomes comparable to mammals and birds and represent the group with the oldest sex chromosomes currently known among amniotic poikilothermic vertebrates.     

Sex chromosomes and sex determination in reptiles

Reptiles occupy a crucial position with respect to vertebrate phylogeny, having roamed the earth for more than 300 million years and given rise to both birds and mammals. To date, this group has been largely ignored by contemporary genomics technologies, although the green anole lizard was recently recommended for whole genome sequencing. Future experiments using flow-sorted chromosome libraries and high-throughout genomic sequencing will help to discover important findings regarding sex chromosome evolution, early events in sex determination, and dosage compensation. This information should contribute extensively toward a general understanding of the genetic control of development in amniotes.     

Sex chromosomes and sex determination in weird mammals

Weird mammals are of two types. Highly divergent mammals, such as the marsupials and monotremes, have informed us of the evolutionary history of the Y chromosome and sex-determining gene, and the recently specialized rodents can help us predict its future. The Y chromosome has had a short but eventful history, and is already heading briskly for oblivion. It originated as a homologous partner of the X when it acquired a sex-determining gene (not necessarily SRY). Most of the genes on the Y, even those with a male-specific function, evolved from genes now on the X. At the mercy of a high rate of variability and the forces of drift and selection, the Y has lost genes at a rate of 3-6 genes/million years, sparing those that acquired critical male-specific functions. Even these genes have disappeared from one mammalian lineage or another as their functions were usurped by genes elsewhere in the genome. The mammalian testis-determining gene, SRY, is a typical Y-borne gene. It arose by truncation of a gene (SOX3) on the X that is expressed in brain development, and it may work by interacting with (inhibiting?) related genes, including SOX9. Variant sex-determining systems in rodents show that the action of SRY can change, as it evidently has in the mouse, and SRY can be inactivated, as in akodont rodents, or even completely superseded, as in mole voles.     

Achiasmatic giant sex chromosomes in the vole Microtus cabrerae (Rodentia, Microtidae).

Conventional and microspread preparations of Microtus cabrerae spermatocytes were made to investigate the chromosomes of this species. Three different types of Y chromosomes, varying in size of the heterochromatic block, were observed; they were alike, however, in regard to synapsis, which was consistently absent. Our results suggest that the heterochromatic blocks are not involved in the lack of synapsis and that asynapsis is a cytological feature common to all species of the family Microtidae. In addition, the co-aligned configuration of the ends of the sex-chromosome axes of this species and the lack of silver-stainable threads or filaments connecting them suggest the existence of two mechanisms for association of the sex chromosomes during prophase I and metaphase I: attachment of the ends of both sex chromosome axes to the nuclear envelope and heterochromatin "stickiness."     

Evolution of heteromorphic sex chromosomes in the order Aulopiformes

The fish order Aulopiformes contains both synchronously hermaphroditic and gonochoristic species. From the cytogenetic viewpoint, few reports show that gonochoristic Aulopiformes have heteromorphic sex chromosomes. Because fish in this order give us a unique opportunity to elucidate the evolution of sex chromosomes, it is important to examine a phylogenetic relationship in Aulopiformes by both molecular evolutionary and cytogenetic methods. Thus, we conducted molecular phylogenetic and cytogenetic studies of six Aulopiform species. Our results suggested that hermaphroditic species were evolutionarily derived from gonochoristic species. It follows that the hermaphroditic species might have lost the heteromorphic sex chromosomes during evolution. Here, we suggest a possibility that heteromorphic sex chromosomes can disappear from the genome, even if they have appeared once in evolution. Taking into account Ohno's hypothesis that heteromorphic sex chromosomes might have emerged from autosomes, we propose the hypothesis that heteromorphic sex chromosomes may have undergone repeated events of appearance and disappearance during the course of fish evolution.     

Evolution of sex determination in mammals

This review summarizes current concepts concerning the evolution of sex chromosomes and the cascade of sex-determining genes in mammals. Untypical sex-determination systems in rodents lacking the Y chromosome and Sry gene are considered using Ellobius as an example.     

Evolution of mammalian sex chromosomes: cooperation of genetic and epigenetic factors

The X and Y chromosomes of mammals, which significantly differ in structure and genetic composition, are thought to originate from a pair of autosomes. During evolution of sex chromosomes in placental mammals, the degradation of the Y chromosome and inactivation spreading along the X chromosome occurred gradually and in concert. Thus, at the molecular level, the genetic and epigenetic factors interacted toward greater differentiation of the X/Y pair. In this review, in context of a comparison permitting to trace this evolutionary pathway, we consider the structural features of mammalian sex chromosomes focusing on the X-chromosomal genes and the unique epigenetic mechanism of their regulation. Possible causes and consequences of the genes skipping inactivation and aspects of molecular mechanism of X-chromosome inactivation are discussed. A number of hypotheses are considered on evolutionary relationships of X-chromosome inactivation and other molecular processes in mammals.     

Decoding sex: Elucidating sex determination and how high-quality genome assemblies are untangling the evolutionary dynamics of sex chromosomes

Sexual reproduction is a diverse and widespread process. In gonochoristic species, the differentiation of sexes occurs through diverse mechanisms, influenced by environmental and genetic factors. In most vertebrates, a master-switch gene is responsible for triggering a sex determination network. However, only a few genes have acquired master-switch functions, and this process is associated with the evolution of sex-chromosomes, which have a significant influence in evolution. Additionally, their highly repetitive regions impose challenges for high-quality sequencing, even using high-throughput, state-of-the-art techniques. Here, we review the mechanisms involved in sex determination and their role in the evolution of species, particularly vertebrates, focusing on sex chromosomes and the challenges involved in sequencing these genomic elements. We also address the improvements provided by the growth of sequencing projects, by generating a massive number of near-gapless, telomere-to-telomere, chromosome-level, phased assemblies, increasing the number and quality of sex-chromosome sequences available for further studies.     

New Y chromosomes and early stages of sex chromosome differentiation: sex determination in <Emphasis Type="Italic">Megaselia</Emphasis>

The phorid fly Megaselia scalaris is a laboratory model for the turnover and early differentiation of sex chromosomes. Isolates from the field have an XY sex-determining mechanism with chromosome pair 2 acting as X and Y chromosomes. The sex chromosomes are homomorphic but display early signs of sex chromosome differentiation: a low level of molecular differences between X and Y. The male-determining function (M), maps to the distal part of the Y chromosome’s short arm. In laboratory cultures, new Y chromosomes with no signs of a molecular differentiation arise at a low rate, probably by transposition of M to these chromosomes. Downstream of the primary signal, the homologue of the Drosophila doublesex (dsx) is part of the sex-determining pathway while Sex-lethal (Sxl), though structurally conserved, is not.