What is the difference between meiosis in human males and females

Anaphase I: The pair of chromosomes are then pulled apart by the meiotic spindle, which pulls one chromosome to one pole of the cell and the other chromosome to the opposite pole.

In meiosis I the sister chromatids stay together. This is different to what happens in mitosis and meiosis II. Telophase I and cytokinesis: The chromosomes complete their move to the opposite poles of the cell. At each pole of the cell a full set of chromosomes gather together. A membrane forms around each set of chromosomes to create two new nuclei. The single cell then pinches in the middle to form two separate daughter cells each containing a full set of chromosomes within a nucleus.

This process is known as cytokinesis. Meiosis II 6. Prophase II: Now there are two daughter cells, each with 23 chromosomes 23 pairs of chromatids. In each of the two daughter cells the chromosomes condense again into visible X-shaped structures that can be easily seen under a microscope.

The membrane around the nucleus in each daughter cell dissolves away releasing the chromosomes. The centrioles duplicate. The meiotic spindle forms again. Metaphase II: In each of the two daughter cells the chromosomes pair of sister chromatids line up end-to-end along the equator of the cell. The centrioles are now at opposites poles in each of the daughter cells.

Meiotic spindle fibres at each pole of the cell attach to each of the sister chromatids. Anaphase II: The sister chromatids are then pulled to opposite poles due to the action of the meiotic spindle. For this analysis, each chromosome arm was divided into five equal segments: centromeric, proximal, interstitial, distal, and telomeric. For most chromosomes, males had a higher proportion of distally-placed MLH1 foci and females had a preponderance of interstitially-placed foci.

Statistically significant sex-specific differences in MLH1 placement were seen on the p- and q-arms of chromosomes 1, 6, 16, and 18 and the q-arms of chromosomes 13, 21, and 22; significant sex-specific differences were not noted for chromosomes 9, 14, and 15 see legends of Figures 3 for statistical results. The chromosomal locations of MLH1 foci were determined using the same cells as in Figure 2 for ten representative large, medium and small chromosomes.

Each chromosome arm was arbitrarily divided into five equal regions — centromeric, proximal, interstitial, distal, and telomeric — and the distribution of MLH1 foci recorded for both chromosome arms for metacentric and sub-metacentric chromosomes or for the q-arm only of acrocentric chromosomes. To identify possible sex-specific differences in the spacing of exchanges, we examined chromosomes with multiple MLH1 foci.

We restricted our analyses to chromosomes 1, 13, 14, 16, 18 and 22, since at least 25 observations per sex were available on each of these chromosomes. For chromosomes 13, 14, 16, 18 and 22 we examined chromosomes with two MLH1 foci, calculating the inter-focal distance as a proportion of the total SC length; for chromosome 1, which had a higher mean number of MLH1 foci, we restricted our analysis to chromosomes with four MLH1 foci. For all six chromosomes, we binned the inter-focal distances into ten equal groups and compared the distributions between males and females Figure 4.

The distributions were significantly different for each of the six chromosomes see Figure 4 legend for statistical results , and were attributable to increased inter-focal distances in males by comparison with females. Inter-focal distances, calculated as the percent of the length of the synaptonemal complex between adjacent MLH1 foci, were determined using the same cells as in Figure 2 ; male data are depicted in white, female data in black.

To obtain sufficient numbers of cells for direct male:female comparisons, we restricted our analysis to chromosomes having the same number of MLH1 foci in males and females; i. Thus, for chromosome 1, we made three measurements of inter-focal distances per cell, while for chromosomes 13, 14, 16, 18 and 22 we made a single measurement of inter-focal distance per cell.

For chromosomes 6, 9, 15 and 21 we had a limited number of cells with the same number of MLH1 foci in both sexes; thus, these chromosomes were excluded from the analysis. Previous studies by us [ 28 ] and others [ 19 ] have suggested an association between the length of the synaptonemal complex and the number of MLH1 foci. Accordingly, we compared genome-wide SC lengths, defined as the sum of the lengths in microns of the SYCP3 signals, between males and females. Consistent with immunofluorescence and electron micrographic analyses of SCs in males and females e.

Subsequently, we conducted similar analyses of the same 10 individual chromosomes analyzed for MLH1 foci and found that, for each chromosome, male SC lengths were significantly shorter than female Figure 5A ; see Figure 5 legend for statistical results.

Male data are in white, female data in black. For chromosomes 1 and 16, we measured the width of the FISH signal at the centromere and three points on each chromosome arm, and averaged the seven values.

For chromosome 21, loop size was taken as the average of three measurements, one at the centromere and two on the long arm. B Blow-up image of a portion of a representative pachytene stage oocyte, labeled with DAPI blue and a chromosome 1 paint probe red. White bars represent the seven individual DNA loop measurements, three from each chromosome arm and one at the centromere.

C DNA loop size means were significantly greater in males for each chromosome; i. In total, we analyzed 77 pachytene stage cells from three males and 98 cells from seven females; for each chromosome, we recorded the average of multiple measurements of the width of the FISH signals. The results were consistent across all three chromosomes, with males displaying significantly larger DNA domains than females Figure 5C ; see Figure 5 legend for statistical results.

Sex-specific variation in recombination levels could originate at several steps in the recombination pathway; e. To investigate the earliest of these events, we asked whether the number of DSBs differed in males and females. A comparison of genome-wide DSB numbers between the sexes revealed a highly significant difference in mean values; i. This is consistent with previous immunofluorescence analyses of RAD51 in human males [ 33 , 34 ] and females [ 22 ] and suggests that sex-specific recombination differences are already in place when the recombination pathway is initiated.

RAD51 foci were used as a surrogate for DSBs and the number of foci in leptotene stage cells determined [44 cells from 3 males white triangles and 39 cells from 5 females black circles ]. The male and female distributions were virtually non-overlapping, with almost all spermatocytes exhibiting fewer than RAD51 foci and most oocytes more than foci. In simple eukaryotes such as yeast, a direct link has been made between sites of synaptic initiation between homologs and sites of recombination e.

Consequently, we asked whether the male:female differences we observed in the localization of MLH1 foci were reflected by similar sex-specific differences in sites of synaptic initiation. A synaptonemal complex initiation site SCISs can be examined by monitoring localization patterns of the transverse element protein SYCP1 in zygotene stage cells. To determine whether these rules also applied to human females, we examined SCISs in zygotene cells from two individuals. Our observations of SYCP1 localization indicated a remarkably different pattern of synaptic initiation in females.

Further, SCISs were not necessarily telomeric; indeed, interstitial and pericentromeric locations predominated. Taken together, these observations mirror the sex-specific differences noted for recombination since — as was observed for MLH1 foci — females had an increased number of SCISs, and SCISs were more likely to be interstitially or proximally located.

SCISs are located at, or near the telomeres, an arrangement typical for human males. The center panel shows a blow-up of a partially-synapsed bivalent circled and the right panel provides a schematic of the bivalent, with the synapsed regions at the ends of the arms and the proximal regions including the centromeres asynapsed. Center panels provide blow-ups of partially synapsed bivalents circled and the right panel schematics, demonstrating the presence of multiple SCISs per chromosomes and in C , co-localization of the centromere and one of the SCISs.

Consistent with this idea, the frequency of maternally-derived aneuploidy increases exponentially in pregnancies involving women over 35 years of age [ 1 ]. However, there are at least two lines of evidence indicating that events occurring at the earliest, fetal, stages of oogenesis also contribute to the genesis of human aneuploidy.

First, studies of trisomic conceptions link abnormalities in meiotic recombination — a process that takes place in the fetal oocyte — to the origin of maternally-derived cases of trisomies 13, 15, 16, 18, 21, 22 and sex chromosome trisomies [ 1 , 37 ]. Second, recent cytological studies of human pachytene oocytes provide direct evidence for a high proportion of cells with non-recombinant bivalents, indicating that some oocytes are, indeed, predisposed to nondisjunction from the beginning stages of meiosis [ 21 ].

These observations raise an obvious question: Could the well-known excess of maternally-derived trisomies be attributable — at least in part — to sex-specific differences in patterns of meiotic recombination established at the earliest stages of oogenesis and spermatogenesis? Accordingly, we set out to characterize basic features of recombination in males and females, taking a cytological approach to examine early prophase spermatocytes and oocytes to gain insight into the origin of the male:female variation in recombination.

Our cytological analyses of recombination, using MLH1 as a surrogate for crossovers [ 6 , 16 — 18 ], differ from previous linkage studies [ 11 — 15 ] in one important respect, namely the overall rate of recombination. In contrast, recent linkage analyses e.

While this accounts for most, if not all, of the difference between the cytological and linkage-based male maps, it does not explain the magnitude of the difference between the MLH1 and linkage maps for the female. Here we suspect that a unique feature of human female meiosis plays a role. That is, our previous cytological studies of human females [ 21 ] indicate that MLH1 localization occurs over a wide temporal window, suggesting that the analysis of MLH1 foci in pachytene stage cells may not capture all MLH1-mediated recombination events.

Since this does not appear to be the case for human males Hassold, unpublished observations , only the female map would be affected. Despite the discrepancy between cytological and linkage maps with respect to the overall rate of recombination, the maps share two important features — a highly significant excess of recombination in the female, and sex-specific differences in the placement of exchanges.

These results are consistent with analyses from a variety of mammalian species, which typically indicate overall increases in recombination in females by comparison with males [ 10 , 38 — 40 ]. Thus, we conclude that the cytological approach provides a useful, direct approach to the analysis of the vast majority of recombination events in humans. To investigate the basis of the sex-specific differences, we asked whether we could identify other sexually dimorphic features of meiotic prophase.

Of particular interest was the possibility that the male:female variation might be evident at the beginning of the recombination pathway, as reflected by differences in the number of DSBs. Accordingly, we analyzed RAD51 foci in early prophase meiocytes, and observed nearly twice as many foci in females. Further, we made no attempt to analyze other, later-occurring recombination intermediates e. Nevertheless, our observations provide strong evidence that, at the onset of meiosis, there are more DSBs in human females than in males.

Assuming that a similar proportion of breaks are processed into crossovers in spermatocytes and oocytes, we would expect to visualize more MLH1 foci in females than males, a prediction consistent with our observations. Thus, we suggest that the underlying mechanisms responsible for sex-specific variation in crossing-over are already present at the time of DSB formation. We were also interested in determining whether the way in which homologous chromosomes synapse is different in males and females.

The formation of the mature SC is thought to be dependent on DSBs and studies of several model organisms have shown a correlation between sites of synaptic initiation and the location of crossovers [ 35 , 36 , 41 , 42 ]. Consistent with these reports, we detected a similar relationship between MLH1 foci and SCISs in previous analyses of human males [ 29 ]. Specifically, in our analyses of zygotene spermatocytes, SCISs were predominantly distally located on chromosomes, mimicking the distribution of MLH1 foci in pachytene cells.

Nevertheless the localization patterns were strongly correlated and, accordingly, we were interested in asking whether there was a similar relationship between SCISs and MLH1 foci in human females.

The results of initial studies reported here suggest that the answer is yes. Nevertheless, in the context of male:female meiotic differences the conclusion is clear, sex-specific differences are not restricted to recombination, but are also evident in the way that homologous chromosomes associate with one another.

Fully formed SCs were approximately twice as long in females as in males Figure 5A , while the sizes of the DNA loops emanating from the SC were significantly larger in males than in females Figure 5C. Because these measurements required analyses of fully formed SCs, they were restricted to the stage of meiotic prophase at which all homologous chromosomes are fully synapsed; i.

Since DSB formation and the initiation of synapsis occur much earlier in prophase, it remains unclear whether differences in chromatin configuration are established prior to the onset of meiosis or during early prophase when the recombination pathway is initiated.

Meiosis in males produces sperm. The process is called spermatogenesis. A diploid spermatocyte will undergo the entire process of meiosis to produce four haploid cells. Then these cells become specialized: they lose most of their organelles, and develop a flagellum for locomotion. Meiosis in females produces ova egg cells.

For instance, although several authors have claimed that one-step meiosis exists why go through chromosomal duplication only to then need a second reduction division? It is a shame that we do not highlight the one ubiquitous form of meiotic variation—symmetry versus asymmetry between the sexes—as well as the variation in most anisogamic animals for when sperm are needed to induce the resumption of halted female meiosis.

Feminist critiques of science have a solid basis, as was alluded to in the first paragraph Kevles , Gowaty , Hrdy , Young et al. Textbook views of meiosis help fuel such radical notions. Correcting the male-centric bias in meiosis to show sex-specific variation will enrich our appreciation of biological variation and may help persuade skeptical feminists that scientific epistemology is worthwhile and compatible with feminist perspectives.

Gorelick R Carpinone J. Origin and maintenance of sex: The evolutionary joys of self sex. Biological Journal of the Linnean Society 98 : — Google Scholar. Gowaty PA. Sexual dialectics, sexual selection, and variation in reproductive behavior. Pages — in Gowaty PA , ed. Chapman and Hall. Google Preview. Hrdy SB. Kevles B. Harvard University Press. Rosser SV. Possible implications of feminist theories for the study of evolution.

Pages 21 — 41 in Gowaty PA , ed. Successful same-sex pairing in Laysan albatross.