MULTIPLE ORIGINS OF SEX CHROMOSOME FUSIONS CORRELATED WITH CHIASMA LOCALIZATION IN HABRONATTUS JUMPING SPIDERS (ARANEAE: SALTICIDAE)

Entelegyne spiders rarely show fusions yielding neo‐Y chromosomes, which M. J. D. White attributed to a constraint in spiders, namely their proximal chiasma localization acting to upset meiotic segregation in males with fusions. Of the 75 taxa of Habronattus and outgroups studied, 47 have X₁X₂0 sex chromosomes in males, 10 have X₁X₂Y, 15 have X₁X₂X₃Y, 2 have X0, and one has both X₁X₂0 and X₁X₂X₃Y. Chromosome numbers and behavior suggest neo‐Ys formed by an autosome‐X fusion to make X₁X₂Y, with a second fusion to an autosome to make X₁X₂X₃Y. Phylogeny shows at least 8–15 gains (or possibly some losses) of neo‐Y (i.e., X‐autosome fusions), a remarkable number for such a small clade. In contrast to the many X‐autosome fusions, at most one autosome–autosome fusion is indicated. Origins of neo‐Y are correlated significantly with distal localization of chiasmata, supporting White's hypothesis that evolution of neo‐Y systems is facilitated by looser pairing (distal chiasmata) at meiosis. However, an alternative (or contributing) explanation for the correlation is that X‐autosome fusions were selected to permit isolation of male‐favored alleles to the neo‐Y chromosome, aided by distal chiasmata limiting recombination. This intralocus sexual conflict hypothesis could explain both the many X‐autosome fusions, and the stunning complexity of male Habronattus courtship displays.     

THE CONTRIBUTION OF FEMALE MEIOTIC DRIVE TO THE EVOLUTION OF NEO‐SEX CHROMOSOMES

Sex chromosomes undergo rapid turnover in certain taxonomic groups. One of the mechanisms of sex chromosome turnover involves fusions between sex chromosomes and autosomes. Sexual antagonism, heterozygote advantage, and genetic drift have been proposed as the drivers for the fixation of this evolutionary event. However, all empirical patterns of the prevalence of multiple sex chromosome systems across different taxa cannot be simply explained by these three mechanisms. In this study, we propose that female meiotic drive may contribute to the evolution of neo‐sex chromosomes. The results of this study showed that in mammals, the XY₁Y₂ sex chromosome system is more prevalent in species with karyotypes of more biarmed chromosomes, whereas the X₁X₂Y sex chromosome system is more prevalent in species with predominantly acrocentric chromosomes. In species where biarmed chromosomes are favored by female meiotic drive, X‐autosome fusions (XY₁Y₂ sex chromosome system) will be also favored by female meiotic drive. In contrast, in species with more acrocentric chromosomes, Y‐autosome fusions (X₁X₂Y sex chromosome system) will be favored just because of the biased mutation rate toward chromosomal fusions. Further consideration should be given to female meiotic drive as a mechanism in the fixation of neo‐sex chromosomes.     

Turnover of sex chromosomes and speciation in fishes

Closely related species of fishes often have different sex chromosome systems. Such rapid turnover of sex chromosomes can occur by several mechanisms, including fusions between an existing sex chromosome and an autosome. These fusions can result in a multiple sex chromosome system, where a species has both an ancestral and a neo-sex chromosome. Although this type of multiple sex chromosome system has been found in many fishes, little is known about the mechanisms that select for the formation of neo-sex chromosomes, or the role of neo-sex chromosomes in phenotypic evolution and speciation. The identification of closely related, sympatric species pairs in which one species has a multiple sex chromosome system and the other has a simple sex chromosome system provides an opportunity to study sex chromosome turnover. Recently, we found that a population of threespine stickleback (Gasterosteus aculeatus) from Japan has an X₁X₂Y multiple sex chromosome system resulting from a fusion between the ancestral Y chromosome and an autosome, while a sympatric threespine stickleback population has a simple XY sex chromosome system. Furthermore, we demonstrated that the neo-X chromosome (X ₂) plays an important role in phenotypic divergence and reproductive isolation between these sympatric stickleback species pairs. Here, we review multiple sex chromosome systems in fishes, as well as recent advances in our understanding of the evolutionary role of sex chromosome turnover in stickleback speciation.     

Genomic changes following the reversal of a Y chromosome to an autosome in Drosophila pseudoobscura

Robertsonian translocations resulting in fusions between sex chromosomes and autosomes shape karyotype evolution by creating new sex chromosomes from autosomes. These translocations can also reverse sex chromosomes back into autosomes, which is especially intriguing given the dramatic differences between autosomes and sex chromosomes. To study the genomic events following a Y chromosome reversal, we investigated an autosome‐Y translocation in Drosophila pseudoobscura. The ancestral Y chromosome fused to a small autosome (the dot chromosome) approximately 10–15 Mya. We used single molecule real‐time sequencing reads to assemble the D. pseudoobscura dot chromosome, including this Y‐to‐dot translocation. We find that the intervening sequence between the ancestral Y and the rest of the dot chromosome is only ～78 Kb and is not repeat‐dense, suggesting that the centromere now falls outside, rather than between, the fused chromosomes. The Y‐to‐dot region is 100 times smaller than the D. melanogaster Y chromosome, owing to changes in repeat landscape. However, we do not find a consistent reduction in intron sizes across the Y‐to‐dot region. Instead, deletions in intergenic regions and possibly a small ancestral Y chromosome size may explain the compact size of the Y‐to‐dot translocation.     

Evidence of a neo-sex chromosome in birds

Neo-sex chromosomes often originate from sex chromosome–autosome fusions and constitute an important basis for the study of gene degeneration and expression in a sex chromosomal context. Neo-sex chromosomes are known from many animal and plant lineages, but have not been reported in birds, a group in which genome organization seems particularly stable. Following indications of sex linkage and unexpected sex-biased gene expression in warblers (Sylvioidea; Passeriformes), we have conducted an extensive marker analysis targeting 31 orthologues of loci on zebra finch chromosome 4a in five species, representative of independent branches of Passerida. We identified a region of sex linkage covering approximately the first half (10 Mb) of chromosome 4a, and associated to both Z and W chromosomes, in three Sylvioidea passerine species. Linkage analysis in an extended pedigree of one species additionally confirmed the association between this part of chromosome 4a and the Z chromosome. Markers located between 10 and 21 Mb of chromosome 4a showed no signs of sex linkage, suggesting that only half of the chromosome was involved in this transition. No sex linkage was observed in non-Sylvioidea passerines, indicating that the neo-sex chromosome arose at the base of the Sylvioidea branch of the avian phylogeny, at 47.4–37.6 millions years ago (MYA), substantially later than the ancestral sex chromosomes (150 MYA). We hypothesize that the gene content of chromosome 4a might be relevant in its transition to a sex chromosome, based on the presence of genes (for example, the androgen receptor) that could offer a selective advantage when associated to Z-linked sex determination loci.     

Patterns of replication in the neo-sex chromosomes ofDrosophila nasuta albomicans

Drosophila nasuta albomicans (with 2n = 6), contains a pair of metacentric neo-sex chromosomes. Phylogenetically these are products of centric fusion between ancestral sex (X, Y) chromosomes and an autosome (chromosome 3). The polytene chromosome complement of males with a neo-X- and neo-Y-chromosomes has revealed asynchrony in replication between the two arms of the neo-sex chromosomes. The arm which represents the ancestral X-chromosome is faster replicating than the arm which represents ancestral autosome. The latter arm of the neo-sex chromosome is synchronous with other autosomes of the complement. We conclude that one arm of the neo-X/Y is still mimicking the features of an autosome while the other arm has the features of a classical X/Y-chromosome. This X-autosome translocation differs from the other evolutionary X-autosome translocations known in certain species ofDrosophila.     

Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila

In the textbook view, the ratio of X chromosomes to autosome sets, X:A, is the primary signal specifying sexual fate in Drosophila. An alternative idea is that X chromosome number signals sex through the direct actions of several X-encoded signal element (XSE) proteins. In this alternative, the influence of autosome dose on X chromosome counting is largely indirect. Haploids (1X;1A), which possess the male number of X chromosomes but the female X:A of 1.0, and triploid intersexes (XX;AAA), which possess a female dose of two X chromosomes and the ambiguous X:A ratio of 0.67, represent critical tests of these hypotheses. To directly address the effects of ploidy in primary sex determination, we compared the responses of the signal target, the female-specific SxlPe promoter of the switch gene Sex-lethal, in haploid, diploid, and triploid embryos. We found that haploids activate SxlPe because an extra precellular nuclear division elevates total X chromosome numbers and XSE levels beyond those in diploid males. Conversely, triploid embryos cellularize one cycle earlier than diploids, causing premature cessation of SxlPe expression. This prevents XX;AAA embryos from fully engaging the autoregulatory mechanism that maintains subsequent Sxl expression, causing them to develop as sexual mosaics. We conclude that the X:A ratio predicts sexual fate, but does not actively specify it. Instead, the instructive X chromosome signal is more appropriately seen as collective XSE dose in the early embryo. Our findings reiterate that correlations between X:A ratios and cell fates in other organisms need not implicate the value of the ratio as an active signal.     

Widespread Recombination Suppression Facilitates Plant Sex Chromosome Evolution

Classical models suggest that recombination rates on sex chromosomes evolve in a stepwise manner to localize sexually antagonistic variants in the sex in which they are beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with preexisting recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus. This species has a polymorphic karyotype with a young neo-sex chromosome, resulting from a Robertsonian fusion between the X chromosome and an autosome, in part of its geographic range. We identified the shared and neo-sex chromosomes using comparative genetic maps of the two cytotypes. We found that sex-linked regions of both the ancestral and the neo-sex chromosomes are embedded in large regions of low recombination. Furthermore, our comparison of the recombination landscape of the neo-sex chromosome to its autosomal homolog indicates that low recombination rates mainly preceded sex linkage. These patterns are not unique to the sex chromosomes; all chromosomes were characterized by massive regions of suppressed recombination spanning most of each chromosome. This represents an extreme case of the periphery-biased recombination seen in other systems with large chromosomes. Across all chromosomes, gene and repetitive sequence density correlated with recombination rate, with patterns of variation differing by repetitive element type. Our findings suggest that ancestrally low rates of recombination may facilitate the formation and subsequent evolution of heteromorphic sex chromosomes.     

Step-by-step evolution of neo-sex chromosomes in geographical populations of wild silkmoths,Samia cynthia ssp.

Geographical subspecies of wild silkmoths, Samia cynthia ssp. (Lepidoptera: Saturniidae), differ considerably in sex chromosome constitution owing to sex chromosome fusions with autosomes, which leads to variation in chromosome numbers. We cloned S. cynthia orthologues of 16 Bombyx mori genes and mapped them to chromosome spreads of S. cynthia subspecies by fluorescence in situ hybridization (FISH) to determine the origin of S. cynthia neo-sex chromosomes. FISH mapping revealed that the Z chromosome and chromosome 12 of B. mori correspond to the Z chromosome and an autosome (A₁) of S. c. ricini (Vietnam population, 2n=27, Z0 in female moths), respectively. B. mori chromosome 11 corresponds partly to another autosome (A₂) and partly to a chromosome carrying nucleolar organizer region (NOR) of this subspecies. The NOR chromosome of S. c. ricini is also partly homologous to B. mori chromosome 24. Furthermore, our results revealed that two A₁ homologues each fused with the W and Z chromosomes in a common ancestor of both Japanese subspecies S. c. walkeri (Sapporo population, 2n=26, neo-Wneo-Z) and S. cynthia subsp. indet. (Nagano population, 2n=25, neo-WZ₁Z₂). One homologue, corresponding to the A₂ autosome in S. c. ricini and S. c. walkeri, fused with the W chromosome in S. cynthia subsp. indet. Consequently, the other homologue became a Z₂ chromosome. These results clearly showed a step-by-step evolution of the neo-sex chromosomes by repeated autosome–sex chromosome fusions. We suggest that the rearrangements of sex chromosomes may facilitate divergence of S. cynthia subspecies towards speciation.     

Chromosome evolution and phylogeny in Ronderosia (Orthoptera,Acrididae, Melanoplinae): clues of survivors to the challenge of sympatry?

In an attempt to unveil the origin of neo‐sex chromosomes in Ronderosia Cigliano grasshoppers, we performed a combined phylogenetic analysis based on morphological (external morphology and male genitalia) and molecular data (COI, COII, 16S and ITS2) to explore the chromosome evolution within the genus. We also analysed the distributional patterns of the various Ronderosia species and considered the possible role of chromosome rearrangements (CRs) in speciation processes within the genus in the light of ‘suppressed‐recombination’ models. We mapped the states of three chromosomal characters on the combined tree topology. The combined evidence supported Ronderosia as a monophyletic group. The cytogenetic analyses of the genus demonstrated the importance of rearranged karyotypes with single, complex and multiples neo‐sex chromosome determination systems in all species. The chromosome character optimisation suggests X‐autosome centric fusion as the mechanism responsible for neo‐sex chromosome formation in most Ronderosia species, except in R. dubia and R. bergii. Similar autosomes were involved in fusions with the ancestral X chromosome in Ronderosia, supporting previous hypotheses on the unique origin of X‐autosome fusion for the sex chromosome in the genus. As a source of chromosome variation, autosome‐autosome centric fusion played a secondary role in Ronderosia compared with other Dichroplini. Given the homogeneity in the morphological features, the sympatric distribution of closely related species and the intrinsic property of centric fusion as suppressors of the crossing over, we suggest that CRs may have played a key role during the speciation process within Ronderosia.     

Origin of a Giant Sex Chromosome

Chromosome size and morphology vary within and among species, but little is known about the proximate or ultimate causes of these differences. Cichlid fish species in the tribe Oreochromini share an unusual giant chromosome that is ∼3 times longer than the other chromosomes. This giant chromosome functions as a sex chromosome in some of these species. We test two hypotheses of how this giant sex chromosome may have evolved. The first hypothesis proposes that it evolved by accumulating repetitive elements as recombination was reduced around a dominant sex determination locus, as suggested by canonical models of sex chromosome evolution. An alternative hypothesis is that the giant sex chromosome originated via the fusion of an autosome with a highly repetitive B chromosome, one of which carried a sex determination locus. We test these hypotheses using comparative analysis of chromosome-scale cichlid and teleost genomes. We find that the giant sex chromosome consists of three distinct regions based on patterns of recombination, gene and transposable element content, and synteny to the ancestral autosome. The WZ sex determination locus encompasses the last ∼105 Mb of the 134-Mb giant chromosome. The last 47 Mb of the giant chromosome shares no obvious homology to any ancestral chromosome. Comparisons across 69 teleost genomes reveal that the giant sex chromosome contains unparalleled amounts of endogenous retroviral elements, immunoglobulin genes, and long noncoding RNAs. The results favor the B chromosome fusion hypothesis for the origin of the giant chromosome.     

X1X1X2X2/X1X2Y sex chromosome systems in the Neotropical Gymnotiformes electric fish of the genus Brachyhypopomus

Several types of sex chromosome systems have been recorded among Gymnotiformes, including male and female heterogamety, simple and multiple sex chromosomes, and different mechanisms of origin and evolution. The X₁X₁X₂X₂/X₁X₂Y systems identified in three species of this order are considered homoplasic for the group. In the genus Brachyhypopomus, only B. gauderio presented this type of system. Herein we describe the karyotypes of Brachyhypopomus pinnicaudatus and B. n. sp. FLAV, which have an X₁X₁X₂X₂/X₁X₂Y sex chromosome system that evolved via fusion between an autosome and the Y chromosome. The morphology of the chromosomes and the meiotic pairing suggest that the sex chromosomes of B. gauderio and B. pinnicaudatus have a common origin, whereas in B . n. sp. FLAV the sex chromosome system evolved independently. However, we cannot discard the possibility of common origin followed by distinct processes of differentiation. The identification of two new karyotypes with an X₁X₁X₂X₂/X₁X₂Y sex chromosome system in Gymnotiformes makes it the most common among the karyotyped species of the group. Comparisons of these karyotypes and the evolutionary history of the taxa indicate independent origins for their sex chromosomes systems. The recurrent emergence of the X₁X₁X₂X₂/X₁X₂Y system may represent sex chromosomes turnover events in Gymnotiformes.     

Did sex chromosome turnover promote divergence of the major mammal groups?

Comparative mapping and sequencing show that turnover of sex determining genes and chromosomes, and sex chromosome rearrangements, accompany speciation in many vertebrates. Here I review the evidence and propose that the evolution of therian mammals was precipitated by evolution of the male‐determining SRY gene, defining a novel XY sex chromosome pair, and interposing a reproductive barrier with the ancestral population of synapsid reptiles 190 million years ago (MYA). Divergence was reinforced by multiple translocations in monotreme sex chromosomes, the first of which supplied a novel sex determining gene. A sex chromosome‐autosome fusion may have separated eutherians (placental mammals) from marsupials 160 MYA. Another burst of sex chromosome change and speciation is occurring in rodents, precipitated by the degradation of the Y. And although primates have a more stable Y chromosome, it may be just a matter of time before the same fate overtakes our own lineage. Also watch the video abstract .     

In vivo analysis of a fluorescent SUMO fusion in transgenic Drosophila

Sumoylation, the covalent attachment of SUMO, a 90 amino acid peptide related to ubiquitin, is a major modulator of protein functions. Fluorescent SUMO protein fusions have been used in cell cultures to visualize SUMO in vivo but not in multicellular organisms. We generated a transgenic line of Drosophila expressing an mCherry-SUMO fusion. We analyzed its pattern in vivo in salivary gland nuclei expressing Venus-HP1 to recognize the different chromatin components (Chromocenter, chromosome IV). We compared it to SUMO immunostaining on squashed polytene chromosomes and observed similar patterns. In addition to the previously reported SUMO localizations (chromosome arms and chromocenter), we identify 2 intense binding sites: the fourth chromosome telomere and the DAPI-bright band in the region 81F.     

Evolution of karyotype,sex chromosomes,and meiosis in mygalomorph spiders (Araneae: Mygalomorphae)

Spider diversity is partitioned into three primary clades, namely Mesothelae, Mygalomorphae, and Araneomorphae. Mygalomorph cytogenetics is largely unknown. Our study revealed a remarkable karyotype diversity of mygalomorphs. Unlike araneomorphs, they show no general trend towards a decrease of 2n, as the chromosome number was reduced in some lineages and increased in others. A biarmed karyotype is a symplesiomorphy of mygalomorphs and araneomorphs. Male meiosis of some mygalomorphs is achiasmatic, or includes the diffuse stage. The sex chromosome system X₁X₂0, which is supposedly ancestral in spiders, is uncommon in mygalomorphs. Many mygalomorphs exhibit more than two (and up to 13) X chromosomes in males. The evolution of X chromosomes proceeded via the duplication of chromosomes, fissions, X–X, and X‐autosome fusions. Spiders also exhibit a homomorphic sex chromosome pair. In the germline of mygalomorph males these chromosomes are often deactivated; their deactivation and pairing is initiated already at spermatogonia. Remarkably, pairing of sex chromosomes in mygalomorph females is also initiated at gonial cells. Some mygalomorphs have two sex chromosome pairs. The second pair presumably arose in early‐diverging mygalomorphs, probably via genome duplication. The unique behaviour of spider sex chromosomes in the germline may promote meiotic pairing of homologous sex chromosomes and structural differentiation of their duplicates, as well as the establishment of polyploid genomes. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 377–408.     

Evolution of a recent neo-Y sex chromosome in a laboratory population ofDrosophila

In many species of animals, one of the sexes has a chromosome that is structurally and functionally different from its socalled homologue. Conventionally, it is called Y chromosome or W chromosome depending on whether it is present in males or females respectively. The corresponding homologous chromosomes are called X and Z chromosomes. The dimorphic sex chromosomes are believed to have originated from undifferentiated autosomes. In extant species it is difficult to envisage the changes that have occurred in the evolution of dimorphic sex chromosomes. In our laboratory, interracial hybridization between twoDrosophila chromosomal races has resulted in the evolution of a novel race, which we have called Cytorace 1. Here we record that in the genome of Cytorace 1 one of the autosomes of its parents is inherited in a manner similar to that of a classical Y chromosome. Thus this unique Cytorace 1 has the youngest neo-Y sex chromosome (5000 days old; about 300 generations) and it can serve as a ‘window’ for following the transition of an autosome to a Y sex chromosome.     

Chromosome Fusion Affects Genetic Diversity and Evolutionary Turnover of Functional Loci but Consistently Depends on Chromosome Size

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.     

Structural mutants of the W chromosome in Ephestia (Insecta,Lepidoptera)

In a search for genetic markers of W-chromosome-autosome fusions in Ephestia, two closely linked autosomal markers, ml and Us, were found to show sex linkage in several families of chromosome mutant strains. In these families, the wild-type allelomorphs, ml ⁺ and US ⁺, label the autosome that is translocated to the W chromosome. With ml (musterlos) a sex dimorphic strain could be established in which males (ml/ml) have patternless wings and females (ml ⁺/ml) have the normal wing pattern.—Using these genetic markers, stability of the fusion chromosome was studied. Recurrence to autosomal inheritance of the marker occurs at a considerable rate. In two chromosome fusion strains, a cytogenetically detectable breakage of the fusion giving rise to a wild-type-like W chromosome was the predominant cause for the recurrence of the marker to autosomal inheritance. In a third strain a more complicated chromosome rearrangement was the predominant cause: the translocated autosome was replaced by a non-homologous one, presumably after a cytogenetically undetectable breakage event of the original fusion. — The high rate of breakage suggests that the fusion chromosomes are dicentrics, a situation not compatible with a typical holokinetic organization of Lepidoptera chromosomes.     

Cytogenetic studies of Aotus from Eastern Amazonia. Y/Autosome rearrangement

Twenty-one specimens of Aotus were captured on both sides of the Tocantins river when the hydroelectric reservoir of Tucuruí, Brazil, was filled. The males had a diploid number of 49 chromosomes, and the females had 50. The observed difference is a consequence of the fusion of the Y chromosome with an autosome. The karyotype is similar to that of the Bolivian Aotus (A. azarae boliviensis). It differs, however, in the G- and C-banding patterns of the chromosome resulting from the Y/autosome fusion. The nucleolar organizing region is located on the secondary constriction of a pair of submetacentric chromosomes. Considerations are presented on the classification of A. infulatus as a separate species.