Recombination landscape dimorphism contributes to sex chromosome evolution in the dioecious plant Rumex hastatulus

There is growing evidence across diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution and turnover because low recombination in the heterogametic sex can help favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus, representing the first characterization of sex differences in recombination landscape in a dioecious plant. We provide evidence for strong sex differences in recombination, with pericentromeric regions of highly suppressed recombination in males that cover over half of the genome. These differences are found on autosomes as well as sex chromosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. Our results are consistent with the hypothesis that sex differences in the recombination landscape contributed to the formation of a large heteromorphic pair of sex chromosomes, and that pollen competition is an important determinant of recombination dimorphism.

Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes

The pseudoautosomal region 1 (PAR1) is a 2.7 Mb telomeric region of human sex chromosomes. As the largest point of contact between the X and Y, PAR1 has a crucial role in ensuring proper segregation of sex chromosomes during male meiosis, exposing it to extreme recombination and associated mutational processes. We investigate PAR1 evolution using population genomic datasets of extant humans, eight populations of great apes and two archaic human genome sequences. We find that the PAR1 sequence is closer to nucleotide equilibrium than autosomal telomeric sequences. We detect a difference between long-term substitution patterns and extant diversity in PAR1 that is mainly driven by the conflict between strong mutation and recombination-associated fixation bias at CpG sites. Additionally, we detect excess C→G mutations in PAR1 of all great ape species, specific to the mutagenic effect of male recombination. Analysis of differences between frequencies of alleles segregating in females and males provided no evidence for sexually antagonistic selection in this region. Furthermore, despite recent evidence for Y chromosome introgression from humans into Neanderthals, we find that the Neanderthal PAR1 retained similarity to the Denisovan sequence, as is the case for the X chromosome and the autosomes. Lastly, we study repeat content and double-strand break hotspot regions in PAR1 and find that they may play roles in ensuring the obligate X-Y recombination event during male meiosis. Our study provides an unprecedented quantification of population genetic forces and insight into evolutionary processes governing PAR1 biology.

Evolutionary dynamics of the human pseudoautosomal regions

Recombination between the X and Y human sex chromosomes is limited to the two pseudoautosomal regions (PARs) that present quite distinct evolutionary origins. Despite the crucial importance for male meiosis, genetic diversity patterns and evolutionary dynamics of these regions are poorly understood. In the present study, we analyzed and compared the genetic diversity of the PAR regions using publicly available genomic sequences encompassing both PAR1 and PAR2. Comparisons were performed through allele diversities, linkage disequilibrium status and recombination frequencies within and between X and Y chromosomes. In agreement with previous studies, we confirmed the role of PAR1 as a male-specific recombination hotspot, but also observed similar characteristic patterns of diversity in both regions although male recombination occurs at PAR2 to a much lower extent (at least one recombination event at PAR1 and in ≈1% in normal male meioses at PAR2). Furthermore, we demonstrate that both PARs harbor significantly different allele frequencies between X and Y chromosomes, which could support that recombination is not sufficient to homogenize the pseudoautosomal gene pool or is counterbalanced by other evolutionary forces. Nevertheless, the observed patterns of diversity are not entirely explainable by sexually antagonistic selection. A better understanding of such processes requires new data from intergenerational transmission studies of PARs, which would be decisive on the elucidation of PARs evolution and their role in male-driven heterosomal aneuploidies.

Correction to: Male recombination map of the autosomal genome in German Holstein

An amendment to this paper has been published and can be accessed via the original article.

Male recombination map of the autosomal genome in German Holstein

Background Recombination is a process by which chromosomes are broken and recombine to generate new combinations of alleles, therefore playing a major role in shaping genome variation. Recombination frequencies ($$\theta$$ θ ) between markers are used to construct genetic maps, which have important implications in genomic studies. Here, we report a recombination map for 44,696 autosomal single nucleotide polymorphisms (SNPs) according to the coordinates of the most recent bovine reference assembly. The recombination frequencies were estimated across 876 half-sib families with a minimum number of 39 and maximum number of 4236 progeny, comprising over 367 K genotyped German Holstein animals. Results Genome-wide, over 8.9 million paternal recombination events were identified by investigating adjacent markers. The recombination map spans 24.43 Morgan (M) for a chromosomal length of 2486 Mbp and an average of ~ 0.98 cM/Mbp, which concords with the available pedigree-based linkage maps. Furthermore, we identified 971 putative recombination hotspot intervals (defined as $$\theta$$ θ > 2.5 standard deviations greater than the mean). The hotspot regions were non-uniformly distributed as sharp and narrow peaks, corresponding to ~ 5.8% of the recombination that has taken place in only ~ 2.4% of the genome. We verified genetic map length by applying a likelihood-based approach for the estimation of recombination rate between all intra-chromosomal marker pairs. This resulted in a longer autosomal genetic length for male cattle (25.35 cM) and in the localization of 51 putatively misplaced SNPs in the genome assembly. Conclusions Given the fact that this map is built on the coordinates of the ARS-UCD1.2 assembly, our results provide the most updated genetic map yet available for the cattle genome.

When Sex Chromosomes Recombine Only in the Heterogametic Sex: Heterochiasmy and Heterogamety in Hyla Tree Frogs

Sex chromosomes are classically predicted to stop recombining in the heterogametic sex, thereby enforcing linkage between sex-determining (SD) and sex-antagonistic (SA) genes. With the same rationale, a pre-existing sex asymmetry in recombination is expected to affect the evolution of heterogamety, for example, a low rate of male recombination might favor transitions to XY systems, by generating immediate linkage between SD and SA genes. Furthermore, the accumulation of deleterious mutations on nonrecombining Y chromosomes should favor XY-to-XY transitions (which discard the decayed Y), but disfavor XY-to-ZW transitions (which fix the decayed Y as an autosome). Like many anuran amphibians, Hyla tree frogs have been shown to display drastic heterochiasmy (males only recombine at chromosome tips) and are typically XY, which seems to fit the above expectations. Instead, here we demonstrate that two species, H. sarda and H. savignyi, share a common ZW system since at least 11 Ma. Surprisingly, the typical pattern of restricted male recombination has been maintained since then, despite female heterogamety. Hence, sex chromosomes recombine freely in ZW females, not in ZZ males. This suggests that heterochiasmy does not constrain heterogamety (and vice versa), and that the role of SA genes in the evolution of sex chromosomes might have been overemphasized.

The Classic Lobe Eye Phenotype of Drosophila Is Caused by Transposon Insertion-Induced Misexpression of a Zinc-Finger Transcription Factor

Drosophila Lobe (L) alleles were first discovered ∼100 years ago as spontaneous dominant mutants with characteristic developmental eye defects. However, the molecular basis for L dominant eye phenotypes has not been clearly understood. A previous work reported identification of CG10109/PRAS40 as the L gene, but subsequent analyses suggested that PRAS40 may not be related to L. Here, we revisited the L gene to clarify this discrepancy and understand the basis for the dominance of L mutations. Genetic analysis localized the L gene to Oaz, which encodes a homolog of the vertebrate zinc finger protein 423 (Zfp423) family transcriptional regulators. We demonstrate that RNAi knockdown of Oaz almost completely restores all L dominant alleles tested. Lrev6-3, a revertant allele of the L2 dominant eye phenotype, has an inframe deletion in the Oaz coding sequence. Molecular analysis of L dominant mutants identified allele-specific insertions of natural transposons (roo[ ]L1, hopper[ ]L5, and roo[ ]Lr) or alterations of a preexisting transposon (L2-specific mutations in roo[ ]Mohr) in the Oaz region. In addition, we generated additional L2-reversion alleles by CRISPR targeting at Oaz. These new loss-of-function Oaz mutations suppress the dominant L eye phenotype. Oaz protein is not expressed in wild-type eye disc but is expressed ectopically in L2/+ mutant eye disc. We induced male recombination between Oaz-GAL4 insertions and the L2 mutation through homologous recombination. By using the L2-recombined GAL4 reporters, we show that Oaz-GAL4 is expressed ectopically in L2 eye imaginal disc. Taken together, our data suggest that neomorphic L eye phenotypes are likely due to misregulation of Oaz by spontaneous transposon insertions.

Sex-Specific Evolution of the Genome-wide Recombination Rate

ABSTRACTAlthough meiotic recombination is required for successful gametogenesis in most species that reproduce sexually, the rate of crossing over varies among individuals. Differences in recombination rate between females and males are perhaps the most striking form of this variation. To determine how sex shapes the evolution of recombination, we directly compared the genome-wide recombination rate in females and males across a common set of genetic backgrounds in house mouse. Our results reveal highly discordant evolutionary trajectories in the two sexes. Whereas male recombination rates show rapid evolution over short timescales, female recombination rates measured in the same strains are mostly static. Strains with high recombination in males have more double-strand breaks and stronger crossover interference than strains with low recombination in males, suggesting that these factors contribute to the sex-specific evolution we document. Our findings provide the strongest evidence yet that sex is a primary driver of recombination rate evolution.