Sex Differences In Recombination Research Articles

A high-density linkage map reveals broad- and fine-scale sex differences in recombination in the hihi (stitchbird; Notiomystis cincta)

Recombination, the process of DNA exchange between homologous chromosomes during meiosis, plays a major role in genomic diversity and evolutionary change. Variation in recombination rate is widespread despite recombination often being essential for progression of meiosis. One such variation is heterochiasmy, where recombination rates differ between sexes. Heterochiasmy has been observed across broad taxonomic groups, yet it remains an evolutionary enigma. We used Lep-MAP3, a pedigree-based software that is efficient in handling large datasets, to generate linkage maps for the hihi or stitchbird (Notiomystis cincta), utilising information from >36 K SNPs and 36 families. We constructed 29 linkage maps, including for the previously unscaffolded Z chromosome. The hihi is an endangered passerine endemic to Aotearoa New Zealand that is sexually dimorphic and exhibits high levels of sexual conflict, including sperm competition. Patterns in recombination in the hihi are consistent with those in other birds, including higher recombination rates in micro-chromosomes. Heterochiasmy in the hihi is male-biased, in line with predictions of the Haldane-Huxley rule, with the male linkage map being 15% longer. Micro-chromosomes exhibit heterochiasmy to a greater extent, contrary to that reported in other birds. At the intra-chromosomal level, heterochiasmy is higher nearer to chromosome ends and in gene-rich regions. Regions of extreme heterochiasmy are enriched for genes implicated in cell structure. This study adds an important contribution in assessing evolutionary theories of heterochiasmy and provides a framework for future studies investigating fine-scale heterochiasmy.

Genetic architecture of individual meiotic crossover rate and distribution in Atlantic Salmon

Meiotic recombination through chromosomal crossovers ensures proper segregation of homologous chromosomes during meiosis, while also breaking down linkage disequilibrium and shuffling alleles at loci located on the same chromosome. Rates of recombination can vary between species, but also between and within individuals, sex and chromosomes within species. Indeed, the Atlantic salmon genome is known to have clear sex differences in recombination with female biased heterochiasmy and markedly different landscapes of crossovers between males and females. In male meiosis, crossovers occur strictly in the telomeric regions, whereas in female meiosis crossovers tend to occur closer to the centromeres. However, little is known about the genetic control of these patterns and how this differs at the individual level. Here, we investigate genetic variation in individual measures of recombination in > 5000 large full-sib families of a Norwegian Atlantic salmon breeding population with high-density SNP genotypes. We show that females had 1.6 × higher crossover counts (CC) than males, with autosomal linkage maps spanning a total of 2174 cM in females and 1483 cM in males. However, because of the extreme telomeric bias of male crossovers, female recombination is much more important for generation of new haplotypes with 8 × higher intra-chromosomal genetic shuffling than males. CC was heritable in females (h2 = 0.11) and males (h2 = 0.10), and shuffling was also heritable in both sex but with a lower heritability in females (h2 = 0.06) than in males (h2 = 0.11). Inter-sex genetic correlations for both traits were close to zero, suggesting that rates and distribution of crossovers are genetically distinct traits in males and females, and that there is a potential for independent genetic change in both sexes in the Atlantic Salmon. Together, these findings give novel insights into the genetic architecture of recombination in salmonids and contribute to a better understanding of how rates and distribution of recombination may evolve in eukaryotes more broadly.

Recombination landscape dimorphism and sex chromosome evolution in the dioecious plant Rumex hastatulus.

There is growing evidence from 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 because low recombination in the heterogametic sex can favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus and provide the first evidence and characterization of sex differences in recombination landscape in a dioecious plant. We present data on significant sex differences in recombination, with regions of very low recombination in males covering over half of the genome. This pattern is evident on both sex chromosomes and autosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Our analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. We hypothesize that sex differences in the recombination landscape have contributed to the formation of a large heteromorphic pair of sex chromosomes in R. hastatulus, but more comparative analyses of recombination will be important to investigate this hypothesis further. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.

Variation in Genetic Relatedness Is Determined by the Aggregate Recombination Process.

The genomic proportion that two relatives share identically by descent-their genetic relatedness-can vary depending on the history of recombination and segregation in their pedigree. Previous calculations of the variance of genetic relatedness have defined genetic relatedness as the proportion of total genetic map length (cM) shared by relatives, and have neglected crossover interference and sex differences in recombination. Here, we consider genetic relatedness as the proportion of the total physical genome (bp) shared by relatives, and calculate its variance for general pedigree relationships, making no assumptions about the recombination process. For the relationships of grandparent-grandoffspring and siblings, the variance of genetic relatedness is a simple decreasing function of [Formula: see text], the average proportion of locus pairs that recombine in meiosis. For general pedigree relationships, the variance of genetic relatedness is a function of metrics analogous to [Formula: see text] Therefore, features of the aggregate recombination process that affect [Formula: see text] and analogs also affect variance in genetic relatedness. Such features include the number of chromosomes and heterogeneity in their size, the number of crossovers and their spatial organization along chromosomes, and sex differences in recombination. Our calculations help to explain several recent observations about variance in genetic relatedness, including that it is reduced by crossover interference (which is known to increase [Formula: see text]). Our methods further allow us to calculate the neutral variance of ancestry among F2s in a hybrid cross, enabling precise statistical inference in F2-based tests for various kinds of selection.

A frog with three sex chromosomes that co-mingle together in nature: Xenopus tropicalis has a degenerate W and a Y that evolved from a Z chromosome.

In many species, sexual differentiation is a vital prelude to reproduction, and disruption of this process can have severe fitness effects, including sterility. It is thus interesting that genetic systems governing sexual differentiation vary among-and even within-species. To understand these systems more, we investigated a rare example of a frog with three sex chromosomes: the Western clawed frog, Xenopus tropicalis. We demonstrate that natural populations from the western and eastern edges of Ghana have a young Y chromosome, and that a male-determining factor on this Y chromosome is in a very similar genomic location as a previously known female-determining factor on the W chromosome. Nucleotide polymorphism of expressed transcripts suggests genetic degeneration on the W chromosome, emergence of a new Y chromosome from an ancestral Z chromosome, and natural co-mingling of the W, Z, and Y chromosomes in the same population. Compared to the rest of the genome, a small sex-associated portion of the sex chromosomes has a 50-fold enrichment of transcripts with male-biased expression during early gonadal differentiation. Additionally, X. tropicalis has sex-differences in the rates and genomic locations of recombination events during gametogenesis that are similar to at least two other Xenopus species, which suggests that sex differences in recombination are genus-wide. These findings are consistent with theoretical expectations associated with recombination suppression on sex chromosomes, demonstrate that several characteristics of old and established sex chromosomes (e.g., nucleotide divergence, sex biased expression) can arise well before sex chromosomes become cytogenetically distinguished, and show how these characteristics can have lingering consequences that are carried forward through sex chromosome turnovers.

Sex Differences in Recombination in Sticklebacks.

Recombination often differs markedly between males and females. Here we present the first analysis of sex-specific recombination in Gasterosteus sticklebacks. Using whole-genome sequencing of 15 crosses between G. aculeatus and G. nipponicus, we localized 698 crossovers with a median resolution of 2.3 kb. We also used a bioinformatic approach to infer historical sex-averaged recombination patterns for both species. Recombination is greater in females than males on all chromosomes, and overall map length is 1.64 times longer in females. The locations of crossovers differ strikingly between sexes. Crossovers cluster toward chromosome ends in males, but are distributed more evenly across chromosomes in females. Suppression of recombination near the centromeres in males causes crossovers to cluster at the ends of long arms in acrocentric chromosomes, and greatly reduces crossing over on short arms. The effect of centromeres on recombination is much weaker in females. Genomic differentiation between G. aculeatus and G. nipponicus is strongly correlated with recombination rate, and patterns of differentiation along chromosomes are strongly influenced by male-specific telomere and centromere effects. We found no evidence for fine-scale correlations between recombination and local gene content in either sex. We discuss hypotheses for the origin of sexual dimorphism in recombination and its consequences for sexually antagonistic selection and sex chromosome evolution.

A high density recombination map of the pig reveals a correlation between sex-specific recombination and GC content

BackgroundThe availability of a high-density SNP genotyping chip and a reference genome sequence of the pig (Sus scrofa) enabled the construction of a high-density linkage map. A high-density linkage map is an essential tool for further fine-mapping of quantitative trait loci (QTL) for a variety of traits in the pig and for a better understanding of mechanisms underlying genome evolution.ResultsFour different pig pedigrees were genotyped using the Illumina PorcineSNP60 BeadChip. Recombination maps for the autosomes were computed for each individual pedigree using a common set of markers. The resulting genetic maps comprised 38,599 SNPs, including 928 SNPs not positioned on a chromosome in the current assembly of the pig genome (build 10.2). The total genetic length varied according to the pedigree, from 1797 to 2149 cM. Female maps were longer than male maps, with a notable exception for SSC1 where male maps are characterized by a higher recombination rate than females in the region between 91–250 Mb. The recombination rates varied among chromosomes and along individual chromosomes, regions with high recombination rates tending to cluster close to the chromosome ends, irrespective of the position of the centromere. Correlations between main sequence features and recombination rates were investigated and significant correlations were obtained for all the studied motifs. Regions characterized by high recombination rates were enriched for specific GC-rich sequence motifs as compared to low recombinant regions. These correlations were higher in females than in males, and females were found to be more recombinant than males at regions where the GC content was greater than 0.4.ConclusionsThe analysis of the recombination rate along the pig genome highlighted that the regions exhibiting higher levels of recombination tend to cluster around the ends of the chromosomes irrespective of the location of the centromere. Major sex-differences in recombination were observed: females had a higher recombination rate within GC-rich regions and exhibited a stronger correlation between recombination rates and specific sequence features.

Scrambling Eggs: Meiotic Drive and the Evolution of Female Recombination Rates

Theories to explain the prevalence of sex and recombination have long been a central theme of evolutionary biology. Yet despite decades of attention dedicated to the evolution of sex and recombination, the widespread pattern of sex differences in the recombination rate is not well understood and has received relatively little theoretical attention. Here, we argue that female meiotic drivers--alleles that increase in frequency by exploiting the asymmetric cell division of oogenesis--present a potent selective pressure favoring the modification of the female recombination rate. Because recombination plays a central role in shaping patterns of variation within and among dyads, modifiers of the female recombination rate can function as potent suppressors or enhancers of female meiotic drive. We show that when female recombination modifiers are unlinked to female drivers, recombination modifiers that suppress harmful female drive can spread. By contrast, a recombination modifier tightly linked to a driver can increase in frequency by enhancing female drive. Our results predict that rapidly evolving female recombination rates, particularly around centromeres, should be a common outcome of meiotic drive. We discuss how selection to modify the efficacy of meiotic drive may contribute to commonly observed patterns of sex differences in recombination.

Construction of a high-resolution genetic linkage map and comparative genome analysis for the reef-building coral Acropora millepora

A high-resolution genetic linkage map for the coral Acropora millepora is constructed and compared with other metazoan genomes, revealing syntenic blocks.

SEX: DIFFERENCES IN MUTATION, RECOMBINATION, SELECTION, GENE FLOW, AND GENETIC DRIFT

In many instances, there are large sex differences in mutation rates, recombination rates, selection, rates of gene flow, and genetic drift. Mutation rates are often higher in males, a difference that has been estimated both directly and indirectly. The higher male mutation rate appears related to the larger number of cell divisions in male lineages but mutation rates also appear gene- and organism-specific. When there is recombination in only one sex, it is always the homogametic sex. When there is recombination in both sexes, females often have higher recombination but there are many exceptions. There are a number of hypotheses to explain the sex differences in recombination. Sex-specific differences in selection may result in stable polymorphisms or for sex chromosomes, faster evolutionary change. In addition, sex-dependent selection may result in antagonistic pleiotropy or sexually antagonistic genes. There are many examples of sex-specific differences in gene flow (dispersal) and a number of adaptive explanations for these differences. The overall effective population size (genetic drift) is dominated by the lower sex-specific effective population size. The mean of the mutation, recombination, and gene flow rates over the two sexes can be used in a population genetics context unless there are sex-specific differences in selection or genetic drift. Sex-specific differences in these evolutionary factors appear to be unrelated to each other. The evolutionary explanations for sex-specific differences for each factor are multifaceted and, in addition, explanations may include chance, nonadaptive differences, or mechanistic, nonevolutionary factors.

Sex differences in recombination and mapping adaptations

Since the raw material of marker based mapping is recombination, understanding how and why recombination rates evolve, and how we can use variation in these rates will ultimately help to improve map resolution. For example, using this variation could help in discriminating between linkage and pleiotropy when QTL for several traits co-locate. It might also be used to improve QTL mapping algorithms. The goals of this chapter are: (1) to highlight differences in recombination rates between the sexes, (2) describe why we might expect these differences, and (3) explore how sex difference in recombination can be used to improve resolution in QTL mapping.

Genetic linkage map ofCoffea canephora: effect of segregation distortion and analysis of recombination rate in male and female meioses

Two complementary segregating plant populations of Coffea canephora were produced from the same clone. One population (DH) comprised 92 doubled haploids derived from female gametes, while the other population (TC) was a test cross consisting of 44 individuals derived from male gametes. Based on the DH population, a genetic linkage map comprising 160 loci was constructed. Eleven linkage groups that putatively correspond to the 11 gametic chromosomes of C. canephora were identified. The mapped loci included more than 40 specific sequence-tagged site markers, either single-copy RFLP probes or microsatellites, that could serve as standard landmarks in coffee-genome analyses. Furthermore, comparisons for segregation distortion and recombination frequency between the two populations were performed. Although segregation distortions were observed in both populations, the frequency of loci exhibiting a very pronounced degree of distortion was especially high in the DH population. This observation is consistent with the hypothesis of strong zygotic selection among the DH population. The recombination frequencies in both populations were found to be almost indistinguishable. These results offer evidence in favour of the lack of significant sex differences in recombination in C. canephora.

A comparison of RFLP maps based on anther culture derived, selfed, and hybrid progenies ofSolanum chacoense

Comparative RFLP linkage maps were constructed using five segregating populations derived from two self-incompatible lines (termed PI 230582 and PI 458314) of diploid tuber-bearing Solanum chacoense Bitt. The analysis was based on 84 RFLP loci identified by 73 different cDNA clones. Distortion of expected Mendelian segregation ratios was observed; less than 10% of the markers showed a skewed segregation in the gametes forming the F1, hybrid population compared with 30% in the selfed population and 46 and 70% in the two populations produced by anther culture. For the anther culture derived populations, most of the skewed loci were scattered throughout the genome, whereas in the populations derived from selfing, they were found primarily in linkage group 1, around the S locus. In this study, we also found that the rate of meiotic recombination could differ between the male and female gametes produced by our parental lines. Thus, male gametes of line PI 458314 showed significantly less recombination as assessed by the total length of the map (206 cM for male gametes vs. 375 cM for female gametes) and the phenomenon was genome-wide. In contrast, the maps from the gametes of PI 230582 had about the same length, but some linkage groups were longer in the female gametes, while others were longer in the male gametes. Key words : Solanum chacoense, RFLP, anther culture, skewed segregation, self-incompatibility, sex differences in recombination.

The robustness of recombination frequency estimates in intercrosses with dominant markers.

The robustness of the maximum likelihood estimates of recombination frequencies has been investigated in double intercrosses with complete dominance at both loci. The robustness was investigated with respect to bias in the recombination frequency estimates due to: (1) limited sample sizes, (2) heterogeneity in recombination frequencies between sexes or among meioses and (3) factors that distort the segregation-misclassification or differential viability. In the coupling phase, the recombination frequency estimates are quite robust with respect to most of the investigated factors. Potentially, the most serious cause of a bias is misclassifications, which tend to increase the recombination frequency estimates. In the repulsion phase, misclassifications are particularly serious, leading to extreme discrepancies between true and observed values. In addition, limited sample size and sex differences in recombination can also bias recombination frequency estimates in repulsion. These effects may pose serious problem in genetic mapping with random amplified polymorphic DNA (RAPD) markers.

Sex differences in recombination

AbstractOne of the stronger empirical generalizations to emerge from the study of genetic systems is that achiasmate meiosis, which has evolved 25–30 times, is always restricted to the heterogametic sex in dioecious species, usually the male. Here we collate data on quantitative sex differences in chiasma frequency from 54 species (4 hermaphroditic flatworms, 18 dioecious insects and vertebrates and 32 hermaphroditic plants) to test whether similar trends hold. Though significant sex differences have been observed within many species, only the Liliaceae show a significant sexual dimorphism in chiasma frequency across species, with more crossing over in embryo mother cells than in pollen mother cells; chiasma frequencies are unrelated to sex and gamety in all other higher taxa studied. Further, the magnitude of sexual dimorphism, independent of sign, does not differ among the three main ecological groups (dioecious animals, plants, and hermaphroditic animals), contrary to what would be expected if it reflected sex‐specific selection on recombination. These results indicate that the strong trends for achiasmate meiosis do not apply to quantitative sex differences in recombination, and contradict theories of sex‐specific costs and benefits. An alternative hypothesis suggests that sex differences may be more‐or‐less neutral, selection determining only the mean rate of recombination. While male and female chiasma frequencies are more similar than would be expected under complete neutrality, a less absolute form of the hypothesis is more difficult to falsify. In female mice the sex bivalent has more chiasmata for its length than the autosomes, perhaps compensating for the absence of recombination in males. Finally, we observe that chiasma frequencies in males and females are positively correlated across species, validating the use of only one sex in comparative studies of recombination.

Reproductive-Biology and the Potential for Genetic-Studies in the Tammar Wallaby, Macropus-Eugenii

The tammar wallaby, Macropus eugenii, has a seasonal breeding cycle which is dependent upon the light regime. Females normally produce one pouch young a year, while carrying a diapausing blastocyst in the uterus. Before the winter solstice, the sucking stimulus of lactation is responsible for inhibition of blastocyst development (lactational quiescence); after this time, inhibition is caused by increasing day length (seasonal quiescence). Lactational quiescence can be broken by removal of the developing young in the pouch, and seasonal quiescence by artificial light regimes, or melatonin treatment; administration of the drug bromocriptine breaks diapause between April and September. Gestation is approximately 28 days and birth is followed by postpartum mating. Hence in theory these interventions can be used to produce up to 12 young per female per year, raising the possibility that the species can be used for genetics. It has a 2n=16 karyotype. In common with other marsupial species, the tammar possesses low allozymic and serum protein variability within the Kangaroo Island population (4/41 loci polymorphic, average heterozygosity of 0.012). However, there are 5/32 fixed differences between the Kangaroo I. and Garden I. tammar populations. Individuals from these two populations will hybridise, although the fertility of the hybrids has yet to be examined. A highly polymorphic major histocompatibility locus exists. A total of 14 loci is probably involved for both intrapopulation and interpopulation markers. We propose to use the species for comparative gene mapping and to see whether sex differences in recombination exist.

Genetic analysis of NF1: Identification of close flanking markers on chromosome 17

The gene causing von Recklinghausen neurofibromatosis, or NF1, has been more precisely localized in the pericentromeric region of chromosome 17. Narrowing of the location for the disease became possible through the identification of eight new DNA probe genetic markers in the centromeric region. Markers that closely flank the centromere also closely flank the NF1 gene. Although there was evidence against this localization in one recombinant, a review of the clinical records revealed a borderline diagnosis of NF1. Significant sex differences in recombination were observed in the pericentric region, and odds for different orders were less discriminating when sex differences were considered in multilocus analyses. The location of the NF1 gene with respect to the centromere could not be determined because recombinants between NF1 and the centromere were not detected in the set of families tested.

Genetic analysis workshop III: Sampling considerations and assumptions in gene mapping

AbstractWe comment on three aspects of genetic linkage studies: 1) estimation of interference, 2) determining order of loci, and 3) sex differences in recombination.

SEX AND CROSSING OVER IN LINKAGE GROUP III OFTRIBOLIUM CASTANEUM

The relative position of the genes black (b), light ocular diaphragm (lod) and aureate (au) for the third linkage group of T. castaneum (Herbst) (Coleoptera, Tenebrionidae) has been determined as b – lod – au. The distances between the various genes vary, depending on the cross. The b++/+ lod au ♂ × + lod au/+ lod au ♀ crosses give the following recombination values: au – lod = 18.32 ± 1.21%; b – lod = 21.05 ± 1.51% and b – au = 37.43 ± 1.27%. The reciprocal crosses give au – lod = 27.67 ± 1.62%; b – lod = 13.97 ± 1.26% and b – au = 39.79 ± 1.78%. For the larger distances encompassed in the b – au region the recombination values in the two sexes were not significantly different. For the shorter b – lod region the recombination values were significantly larger in the females than in the males, while for the adjacent lod – au region the opposite was true. On the basis of the current literature it would appear that the main factors contributing to these sex differences in recombination are the modifiers which are different in the genetic background of the two sexes.

Linkage mapping from pair-wise recombination data

The problem of obtaining a genetic map of a linkage group from pair-wise recombination data is considered. A non-parametric approach is proposed, that does not require the definition of a mapping function, computation of coefficients of coincidence, nor knowledge of map length or sex differences in recombination. An application to Bridges and Morgan's (1923) data on chromosome 3 of Drosophila melanogaster is presented.