Genomic conflict drives patterns of X‐linked population structure in Drosophila neotestacea

Intragenomic conflict has the potential to cause widespread changes in patterns of genetic diversity and genome evolution. In this study, we investigate the consequences of sex‐ratio (SR) drive on the population genetic patterns of the X‐chromosome in Drosophila neotestacea. An SR X‐chromosome prevents the maturation of Y‐bearing sperm during male spermatogenesis and thus is transmitted to ~100% of the offspring, nearly all of which are daughters. Selection on the rest of the genome to suppress SR can be strong, and the resulting conflict over the offspring sex ratio can result in the accumulation of multiple loci on the X‐chromosome that are necessary for the expression of drive. We surveyed variation at 12 random X‐linked microsatellites across 16 populations of D. neotestacea that range in SR frequency from 0% to 30%. First, every locus was differentiated between SR and wild‐type chromosomes, and this drives genetic structure at the X‐chromosome. Once the association with SR is accounted for, the patterns of differentiation among populations are similar to the autosomes. Second, within wild‐type chromosomes, the relative heterozygosity is reduced in populations with an increased prevalence of drive, and the heterozygosity of SR chromosomes is higher than expected based on its prevalence. The combination of the relatively high prevalence of SR drive and the structuring of polymorphism between the SR and wild‐type chromosomes suggests that genetic conflict because of SR drive has had significant consequences on the patterns of X‐linked polymorphism and thus also probably affects the tempo of X‐chromosome evolution in D. neotestacea.     

Occasional recombination of a selfish X‐chromosome may permit its persistence at high frequencies in the wild

The sex‐ratio X‐chromosome (SR) is a selfish chromosome that promotes its own transmission to the next generation by destroying Y‐bearing sperm in the testes of carrier males. In some natural populations of the fly Drosophila neotestacea, up to 30% of the X‐chromosomes are SR chromosomes. To investigate the molecular evolutionary history and consequences of SR, we sequenced SR and standard (ST) males at 11 X‐linked loci that span the ST X‐chromosome and at seven arbitrarily chosen autosomal loci from a sample of D. neotestacea males from throughout the species range. We found that the evolutionary relationship between ST and SR varies among individual markers, but genetic differentiation between SR and ST is chromosome‐wide and likely due to large chromosomal inversions that suppress recombination. However, SR does not consist of a single multilocus haplotype: we find evidence for gene flow between ST and SR at every locus assayed. Furthermore, we do not find long‐distance linkage disequilibrium within SR chromosomes, suggesting that recombination occurs in females homozygous for SR. Finally, polymorphism on SR is reduced compared to that on ST, and loci displaying signatures of selection on ST do not show similar patterns on SR. Thus, even if selection is less effective on SR, our results suggest that gene flow with ST and recombination between SR chromosomes may prevent the accumulation of deleterious mutations and allow its long‐term persistence at relatively high frequencies.     

Phylogeography of sex ratio and multiple mating in stalk-eyed flies from southeast Asia

The factors maintaining sex chromosome meiotic drive, or sex ratio (SR), in natural populations remain uncertain. Coevolution between segregation distortion and modifiers should produce transient SR distortion while selection can result in a stable polymorphism. We hypothesize that if SR is maintained by selection, then phylogenetically related populations should exhibit similar SR frequency and intensity. Furthermore, when drive is present, females should mate with multiple males more often both to insure fertility and to increase the probability of producing male progeny. In this paper we report on variation in SR frequency and multiple mating among seven populations and three species of stalk-eyed flies, genus Cyrtodiopsis, from southeast Asia. Using a phylogenetic hypothesis based on 1100 bp of mtDNA sequence we find that while sex chromosome meiotic drive is present in all populations of C. whitei and C. dalmanni, the frequency and intensity of drive only differs between populations or species with greater than 4.8% sequence divergence. The frequency of females mating with multiple males is higher in populations with SR. In addition, SR males mate less often, possibly to compensate for sperm depletion. Our results suggest that sex chromosome drive is maintained by balancing selection in populations of C. whitei and C. dalmanni. Nevertheless, coevolution between drive and suppressors deserves further study.     

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.     

Sex‐biased transcriptome divergence along a latitudinal gradient

Sex‐dependent gene expression is likely an important genomic mechanism that allows sex‐specific adaptation to environmental changes. Among Drosophila species, sex‐biased genes display remarkably consistent evolutionary patterns; male‐biased genes evolve faster than unbiased genes in both coding sequence and expression level, suggesting sex differences in selection through time. However, comparatively little is known of the evolutionary process shaping sex‐biased expression within species. Latitudinal clines offer an opportunity to examine how changes in key ecological parameters also influence sex‐specific selection and the evolution of sex‐biased gene expression. We assayed male and female gene expression in Drosophila serrata along a latitudinal gradient in eastern Australia spanning most of its endemic distribution. Analysis of 11 631 genes across eight populations revealed strong sex differences in the frequency, mode and strength of divergence. Divergence was far stronger in males than females and while latitudinal clines were evident in both sexes, male divergence was often population specific, suggesting responses to localized selection pressures that do not covary predictably with latitude. While divergence was enriched for male‐biased genes, there was no overrepresentation of X‐linked genes in males. By contrast, X‐linked divergence was elevated in females, especially for female‐biased genes. Many genes that diverged in D. serrata have homologs also showing latitudinal divergence in Drosophila simulans and Drosophila melanogaster on other continents, likely indicating parallel adaptation in these distantly related species. Our results suggest that sex differences in selection play an important role in shaping the evolution of gene expression over macro‐ and micro‐ecological spatial scales.     

X chromosome drive in a widespread Palearctic woodland fly,Drosophila testacea

Selfish genes that bias their own transmission during meiosis can spread rapidly in populations, even if they contribute negatively to the fitness of their host. Driving X chromosomes provide a clear example of this type of selfish propagation. These chromosomes have important evolutionary and ecological consequences, and can be found in a broad range of taxa including plants, mammals and insects. Here, we report a new case of X chromosome drive (X drive) in a widespread woodland fly, Drosophila testacea. We show that males carrying the driving X (SR males) sire 80–100% female offspring and possess a diagnostic X chromosome haplotype that is perfectly associated with the sex ratio distortion phenotype. We find that the majority of sons produced by SR males are sterile and appear to lack a Y chromosome, suggesting that meiotic defects involving the Y chromosome may underlie X drive in this species. Abnormalities in sperm cysts of SR males reflect that some spermatids are failing to develop properly, confirming that drive is acting during gametogenesis. By screening wild‐caught flies using progeny sex ratios and a diagnostic marker, we demonstrate that the driving X is present in wild populations at a frequency of ~ 10% and that suppressors of drive are segregating in the same population. The testacea species group appears to be a hot spot for X drive, and D. testacea is a promising model to compare driving X chromosomes in closely related species, some of which may even be younger than the chromosomes themselves.     

SUPPRESSION OF SEX-RATIO MEIOTIC DRIVE AND THE MAINTENANCE OF Y-CHROMOSOME POLYMORPHISM IN DROSOPHILA

Like several other species of Drosophila, D. quinaria is polymorphic for X-chromosome meiotic drive; matings involving males that carry a “sex-ratio” X chromosome (X^SR) result in the production of strongly female-biased offspring sex ratios (Jaenike 1996). A survey of isofemale lines of D. quinaria from several populations reveals that there is genetic variation for partial suppression of this meiotic drive. Crossing experiments show that there is Y-linked, and probably autosomal, variation for suppression of drive. Y-linked suppressors of X-chromosome drive have now been described in several species of Diptera. I develop a simple model for the maintenance of Y-chromosome polymorphism in species polymorphic for X-linked meiotic drive. One interesting feature of this model is that, if there is a stable Y-chromosome polymorphism, then the equilibrium frequency of the standard and sex-ratio X chromosomes is determined solely by Y-chromosome parameters, not by the fitness effects of the different X chromosomes on their carriers. This model suggests that Y-chromosome polymorphism may be easier to maintain than previously thought, and I hypothesize that karyotypic variation in Y chromosomes will be found to be associated with suppression of sex-ratio meiotic drive in other species of Drosophila.     

Social constraint and an absence of sex‐biased dispersal drive fine‐scale genetic structure in white‐winged choughs

This study used eight polymorphic microsatellite loci to examine the relative effects of social organization and dispersal on fine‐scale genetic structure in an obligately cooperative breeding bird, the white‐winged chough (Corcorax melanorhamphos). Using both individual‐level and population‐level analyses, it was found that the majority of chough groups consisted of close relatives and there was significant differentiation among groups (F_ST = 0.124). However, spatial autocorrelation analysis revealed strong spatial genetic structure among groups up to 2 km apart, indicating above average relatedness among neighbours. Multiple analyses showed a unique lack of sex‐biased dispersal. As such, choughs may offer a model species for the study of the evolution of sex‐biased dispersal in cooperatively breeding birds. These findings suggest that genetic structure in white‐winged choughs reflects the interplay between social barriers to dispersal resulting in large family groups that can remain stable over long periods of times, and short dispersal distances which lead to above average relatedness among neighbouring groups.     

The influence of demography and local mating environment on sex ratios in a wind‐pollinated dioecious plant

Negative frequency‐dependent selection should result in equal sex ratios in large populations of dioecious flowering plants, but deviations from equality are commonly reported. A variety of ecological and genetic factors can explain biased sex ratios, although the mechanisms involved are not well understood. Most dioecious species are long‐lived and/or clonal complicating efforts to identify stages during the life cycle when biases develop. We investigated the demographic correlates of sex‐ratio variation in two chromosome races of Rumex hastatulus, an annual, wind‐pollinated colonizer of open habitats from the southern USA. We examined sex ratios in 46 populations and evaluated the hypothesis that the proximity of males in the local mating environment, through its influence on gametophytic selection, is the primary cause of female‐biased sex ratios. Female‐biased sex ratios characterized most populations of R.  hastatulus (mean sex ratio = 0.62), with significant female bias in 89% of populations. Large, high‐density populations had the highest proportion of females, whereas smaller, low‐density populations had sex ratios closer to equality. Progeny sex ratios were more female biased when males were in closer proximity to females, a result consistent with the gametophytic selection hypothesis. Our results suggest that interactions between demographic and genetic factors are probably the main cause of female‐biased sex ratios in R. hastatulus. The annual life cycle of this species may limit the scope for selection against males and may account for the weaker degree of bias in comparison with perennial Rumex species.     

SEX RATIO DRIVE PROMOTES SEXUAL CONFLICT AND SEXUAL COEVOLUTION IN THE FLY DROSOPHILA PSEUDOOBSCURA

Selfish genetic elements occur in all living organisms and often cause reduced fertility and sperm competitive ability in males. In the fruit fly Drosophila pseudoobscura, the presence of a sex‐ratio distorting X‐chromosome meiotic driver Sex Ratio (SR) has been shown to promote the evolution of increased female remating rates in laboratory populations. This is favored because it promotes sperm competition, which decreases the risk to females of producing highly female‐biased broods and to their offspring of inheriting the selfish gene. Here, we show that non‐SR males in these SR populations evolved an increased ability to suppress female remating in response to the higher female remating rates, indicating male–female coevolution. This occurred even though SR was rare in the populations. This was further supported by a correlation between females’ remating propensity and males’ ability to suppress female remating across populations. Thus SR can generate sexual conflict over female remating rate between females and the noncarrier males that make up the majority of the males, promoting evolution of increased ability of males to suppress female remating.     

Genetic evidence for male‐biased dispersal in the Qinghai toad‐headed agamid Phrynocephalus vlangalii and its potential link to individual social interactions

Sex‐biased dispersal has profound impacts on a species' biology and several factors have been attributed to its evolution, including mating system, inbreeding avoidance, and social complexity. Sex‐biased dispersal and its potential link to individual social interactions were examined in the Qinghai toad‐headed agamid (Phrynocephalus vlangalii). We first determined the pattern of sex‐biased dispersal using population genetic methods. A total of 345 specimens from 32 sites in the Qaidam Basin were collected and genotyped for nine microsatellite DNA loci. Both individual‐based assignment tests and allele frequency‐based analyses were conducted. Females revealed much more genetic structure than males and all results were consistent with male‐biased dispersal. First‐generation migrants were also identified by genetic data. We then examined eight social interaction‐related morphological traits and explored their potential link to sex‐biased dispersal. Female residents had larger heads and longer tails than female migrants. The well‐developed signal system among females, coupled with viviparity, might make remaining on natal sites beneficial, and hence promote female philopatry. Dominant females with larger heads were more likely to stay. Contrary to females, male migrants had larger heads and belly patches than residents, suggesting that dispersal might confer selective advantages for males. Such advantages may include opportunities for multiple mating and escaping from crowded sites. Large belly patches and several other morphological traits may assist their success in obtaining mates during dispersal. Furthermore, a relatively high relatedness (R = 0.06) among females suggested that this species might have rudimentary social structure. Case studies in “less” social species may provide important evidence for a better understanding of sex‐biased dispersal.     

Geographic variation in sex‐chromosome differentiation in the common frog (Rana temporaria)

In sharp contrast with birds and mammals, sex‐determination systems in ectothermic vertebrates are often highly dynamic and sometimes multifactorial. Both environmental and genetic effects have been documented in common frogs (Rana temporaria). One genetic linkage group, mapping to the largest pair of chromosomes and harbouring the candidate sex‐determining gene Dmrt1, associates with sex in several populations throughout Europe, but association varies both within and among populations. Here, we show that sex association at this linkage group differs among populations along a 1500‐km transect across Sweden. Genetic differentiation between sexes is strongest (F_ST = 0.152) in a northern‐boreal population, where male‐specific alleles and heterozygote excesses (F_IS = ?0.418 in males, +0.025 in females) testify to a male‐heterogametic system and lack of X‐Y recombination. In the southernmost population (nemoral climate), in contrast, sexes share the same alleles at the same frequencies (F_ST = 0.007 between sexes), suggesting unrestricted recombination. Other populations show intermediate levels of sex differentiation, with males falling in two categories: some cluster with females, while others display male‐specific Y haplotypes. This polymorphism may result from differences between populations in the patterns of X‐Y recombination, co‐option of an alternative sex‐chromosome pair, or a mixed sex‐determination system where maleness is controlled either by genes or by environment depending on populations or families. We propose approaches to test among these alternative models, to disentangle the effects of climate and phylogeography on the latitudinal trend, and to sort out how this polymorphism relates to the ‘sexual races’ described in common frogs in the 1930s.     

Cytological identification of two X-chromosome types in the wood lemming (Myopus schisticolor)

In the wood lemming (Myopus schisticolor) three genetic types of sex chromosome constitution in females are postulated: XX, X^*X and X^*Y (X^*=X with a mutation inactivating the male determining effect of the Y chromosome). Males are all XY. It is shown in the present paper that the two types of X chromosomes, X and X^*, exhibit differences in the G-band patterns of their short arms. In addition, it was demonstrated in unbanded chromosomes that the short arm in X^* is shorter than in X. The origin of these differences is still obscure; but they allow to identify and to distinguish the individual types of sex chromosome constitution, as of XX versus X^*X females and of X^*Y females versus XY males, on the basis of G-banded chromosome preparations from somatic cells.     

Autosomal suppression and fitness costs of an old driving X chromosome in Drosophila testacea

Driving X chromosomes (X^Ds) bias their own transmission through males by killing Y‐bearing gametes. These chromosomes can in theory spread rapidly in populations and cause extinction, but many are found as balanced polymorphisms or as “cryptic” X^Ds shut down by drive suppressors. The relative likelihood of these outcomes and the evolutionary pathways through which they come about are not well understood. An X^D was recently discovered in the mycophagous fly, Drosophila testacea, presenting the opportunity to compare this X^D with the well‐studied X^D of its sister species, Drosophila neotestacea. Comparing features of independently evolved X^Ds in young sister species is a promising avenue towards understanding how X^Ds and their counteracting forces change over time. In contrast to the X^D of D. neotestacea, we find that the X^D of D. testacea is old, with its origin predating the radiation of three species: D. testacea, D. neotestacea and their shared sister species, Drosophila orientacea. Motivated by the suggestion that older X^Ds should be more deleterious to carriers, we assessed the effect of the X^D on both male and female fertility. Unlike what is known from D. neotestacea, we found a strong fitness cost in females homozygous for the X^D in D. testacea: a large proportion of homozygous females failed to produce offspring after being housed with males for several days. Our male fertility experiments show that although X^D male fertility is lower under sperm‐depleting conditions, X^D males have comparable fertility to males carrying a standard X chromosome under a free‐mating regime, which may better approximate conditions in wild populations of D. testacea. Lastly, we demonstrate the presence of autosomal suppression of X chromosome drive. Our results provide support for a model of X^D evolution where the dynamics of young X^Ds are governed by fitness consequences in males, whereas in older X^D systems, both suppression and fitness consequences in females likely supersede male fitness costs.     

Aerial performance of stalk-eyed flies that differ in eye span

Stalk-eyed flies have eyes placed laterally away from the head on elongated peduncles. The elongation of eye span may increase the energetic cost of flight, reduce flight performance via aerodynamic effects or via increased load, or necessitate compensatory changes in other body dimensions. Body mass and body dimensions were measured to test the hypothesis that elongation of eye span is correlated with increased head mass in two closely related species of stalk-eyed flies. Cyrtodiopsis whitei is sexually dimorphic, with the eye span of larger males exceeding body length. Cyrtodiopsis quinqueguttata is sexually monomorphic with eye span substantially less than body length. Although eye span was significantly longer in C. whitei, head mass did not differ between species after accounting for differences in body mass. C. whitei males had longer wings, heavier thoraxes, and lighter abdomens in relation to body mass than did female C. whitei or C. quinqueguttata of either sex. Three-dimensional tracking of flight paths showed that path velocity and the horizontal component of velocity did not differ according to species or sex, but the long-eyed C. whitei males showed reduced overall aerial performance by flying at shallower ascent angles and reduced vertical velocity. Although increased mass loading does not occur in C. whitei males, increased drag, aerodynamic effects from the wake of the eye stalks, and constrained visual processing are possible mechanisms which could cause their reduced performance. Accepted: 7 June 2000     

Population genetic structure and direct observations reveal sex‐reversed patterns of dispersal in a cooperative bird

Sex‐biased dispersal is pervasive and has diverse evolutionary implications, but the fundamental drivers of dispersal sex biases remain unresolved. This is due in part to limited diversity within taxonomic groups in the direction of dispersal sex biases, which leaves hypothesis testing critically dependent upon identifying rare reversals of taxonomic norms. Here, we use a combination of observational and genetic data to demonstrate a rare reversal of the avian sex bias in dispersal in the cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali). Direct observations revealed that (i) natal philopatry was rare, with both sexes typically dispersing locally to breed, and (ii), unusually for birds, males bred at significantly greater distances from their natal group than females. Population genetic analyses confirmed these patterns, as (i) corrected Assignment index (AIc), F_ST tests and isolation‐by‐distance metrics were all indicative of longer dispersal distances among males than females, and (ii) spatial autocorrelation analysis indicated stronger within‐group genetic structure among females than males. Examining the spatial scale of extra‐group mating highlighted that the resulting ‘sperm dispersal’ could have acted in concert with individual dispersal to generate these genetic patterns, but gamete dispersal alone cannot account entirely for the sex differences in genetic structure observed. That leading hypotheses for the evolution of dispersal sex biases cannot readily account for these sex‐reversed patterns of dispersal in white‐browed sparrow weavers highlights the continued need for attention to alternative explanations for this enigmatic phenomenon. We highlight the potential importance of sex differences in the distances over which dispersal opportunities can be detected.     

The sex chromosome system can influence the evolution of sex‐biased dispersal

Sex‐biased dispersal is a much‐discussed feature in literature on dispersal. Diverse hypotheses have been proposed to explain the evolution of sex‐biased dispersal, a difference in dispersal rate or dispersal distance between males and females. An early hypothesis has indicated that it may rely on the difference in sex chromosomes between males and females. However, this proposal was quickly rejected without a real assessment. We propose a new perspective on this hypothesis by investigating the evolution of sex‐biased dispersal when dispersal genes are sex‐linked, that is when they are located on the sex chromosomes. We show that individuals of the heterogametic sex disperse relatively more than do individuals of the homogametic sex when dispersal genes are sex‐linked rather than autosomal. Although such a sex‐biased dispersal towards the heterogametic sex is always observed in monogamous species, the mating system and the location of dispersal genes interact to modulate sex‐biased dispersal in monandry and polyandry. In the context of the multicausality of dispersal, we suggest that sex‐linked dispersal genes can influence the evolution of sex‐biased dispersal.     

Dmrt1 polymorphism and sex‐chromosome differentiation in Rana temporaria

Sex‐determination mechanisms vary both within and among populations of common frogs, opening opportunities to investigate the molecular pathways and ultimate causes shaping their evolution. We investigated the association between sex‐chromosome differentiation (as assayed from microsatellites) and polymorphism at the candidate sex‐determining gene Dmrt1 in two Alpine populations. Both populations harboured a diversity of X‐linked and Y‐linked Dmrt1 haplotypes. Some males had fixed male‐specific alleles at all markers (“differentiated” Y chromosomes), others only at Dmrt1 (“proto‐” Y chromosomes), while still others were genetically indistinguishable from females (undifferentiated X chromosomes). Besides these XX males, we also found rare XY females. The several Dmrt1 Y haplotypes differed in the probability of association with a differentiated Y chromosome, which we interpret as a result of differences in the masculinizing effects of alleles at the sex‐determining locus. From our results, the polymorphism in sex‐chromosome differentiation and its association with Dmrt1, previously inferred from Swedish populations, are not just idiosyncratic features of peripheral populations, but also characterize highly diverged populations in the central range. This implies that an apparently unstable pattern has been maintained over long evolutionary times.     

Sex reversal and primary sex ratios in the common frog (Rana temporaria)

Sex reversal has been suggested to have profound implications for the evolution of sex chromosomes and population dynamics in ectotherms. Occasional sex reversal of genetic males has been hypothesized to prevent the evolutionary decay of nonrecombining Y chromosomes caused by the accumulation of deleterious mutations. At the same time, sex reversals can have a negative effect on population growth rate. Here, we studied phenotypic and genotypic sex in the common frog (Rana temporaria) in a subarctic environment, where strongly female‐biased sex ratios have raised the possibility of frequent sex reversals. We developed two novel sex‐linked microsatellite markers for the species and used them with a third, existing marker and a Bayesian modelling approach to study the occurrence of sex reversal and to determine primary sex ratios in egg clutches. Our results show that a significant proportion (0.09, 95% credible interval: 0.04–0.18) of adults that were genetically female expressed the male phenotype, but there was no evidence of sex reversal of genetic males that is required for counteracting the degeneration of Y chromosome. The primary sex ratios were mostly equal, but three clutches consisted only of genetic females and three others had a significant female bias. Reproduction of the sex‐reversed genetic females appears to create all‐female clutches potentially skewing the population level adult sex‐ratio consistent with field observations. However, based on a simulation model, such a bias is expected to be small and transient and thus does not fully explain the observed female‐bias in the field.     

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.