Although species differences in crossover rate are often much larger than the sex differences observed within species, evolutionary insights from this dataset are, overwhelmingly, based on data from one sex.
Both the number of chromosomes and the number of chromosome arms are strongly positively correlated with crossover counts across mammals Table 4.
The magnitude of the correlation with chromosome number is nominally higher than that with the number of autosomal chromosome arms, a finding inconsistent with prior results Dutrillaux ; Pardo-Manuel De Villena and Sapienza ; Segura et al. This discrepancy likely owes to the sensitivity of this correlation to both the method for estimating crossover frequency and taxonomic sampling. For example, karyotype is a weaker predictor of crossover frequency estimated from MLH1 foci than from chiasma counts, and the autosomal fundamental number explains a greater fraction of the variance in chiasma counts than does the number of chromosomes Table 4.
Repeated, random down-sampling of the full dataset to include just 45 species [comparable to the number of taxa analyzed by Pardo-Manuel De Villena and Sapienza ] yields considerable variation in the magnitude of the correlations between crossover frequency and both 2N and FN. In addition, simulation replicates vary with regard to whether 2N or FN is the stronger predictor of crossover rate Figure S4.
For Overall, the results of these simple simulations indicate that insights into the relationship between karyotype and the meiotic crossover constraint based on correlational analyses are sensitive to sampling.
In addition, for the 17 mammalian species with crossover rate estimates available from multiple experimental methods, there is strong consensus on the crossover-to-karyotype relationship across approaches Table S1. Nonetheless, MLH1-based crossover counts are almost certainly underestimates of the true crossover rate Hollingsworth and Brill ; Holloway et al. The phylogenetic distribution of the meiotic constraint on crossing over in mammals.
An informal supertree was assembled to depict the evolutionary relationships among taxa for which crossover frequency estimates are available.
Note that branch lengths on this cladogram are not proportional to evolutionary divergence and represent only the relations among taxa. Poorly resolved species relationships are represented as polytomies. The column to the right of each species name denotes whether available recombination estimates for that species derive from analysis of chiasma counts red dot , MLH1 foci counts blue dot , or genetic linkage maps green dot.
Lineages leading to species with fewer crossovers than chromosome arms are shown in red. The names of species with karyotypes composed of only acrocentric chromosomes are shown in blue. To gain a window onto the evolution of the meiotic constraint on recombination, I investigated the phylogenetic relationships among species with variable chromosomal crossover distributions at meiosis Figure 5.
Several important findings emerge from analyzing these data in an evolutionary context. These patterns suggest that the meiotic constraint on recombination in the mammalian common ancestor was likely at the level of the chromosome arm. By extension, most taxa with only a single crossover per homologous chromosome pair at meiosis have emerged recently in mammalian evolution. A second key observation is that species with fewer crossovers than chromosome arms are nonrandomly distributed across the tree, with multiple independent transitions from one crossover per chromosome arm to one crossover per chromosome evident in mammals.
Three of the four macaque species analyzed exhibit fewer crossovers per meiosis than chromosome arms, pointing to a possible relaxation of the chromosomal constraint on recombination in the common ancestor of Macaca.
The cotton-top tamarin Saguinus oedipus also conforms to this trend, revealing multiple independent shifts in the chromosomal distribution of crossovers within the primate clade alone. Two of the four Caniformia species in this analysis Mustela vison and Vulpes vulpes also fall short of the one-crossover-per-chromosome-arm threshold. Interestingly, the karyotype of the other two species analyzed in this clade, the domestic dog and gray wolf, are composed exclusively of acrocentric chromosomes.
These species may only appear to superficially meet the one-per-chromosome-arm criterion because the number of chromosome arms and chromosomes are equivalent. Thus, the common ancestor of Caniformia may have also experienced a relaxation in the chromosomal constraint on meiotic recombination.
In general, the emergence of acrocentric karyotypes in mammals appears to be preceded by a relaxation of the distributional constraint to one crossover per chromosome. A further hint at this trend is apparent in the murine rodents. The most basal species analyzed in this clade—the Norway rat Rattus norvegicus —has fewer crossovers than chromosome arms, suggesting that the minimum number of crossover events in the common ancestor of Murinae was defined by the haploid chromosome number.
The remaining murine rodents analyzed have acrocentric karyotypes, erasing the distinction between the number of crossovers per chromosome arm and per chromosome. Rigorous tests of coevolution between the chromosomal distribution of crossovers and basic features of karyotype structure, including acrocentric status, will require the application of evolutionary modeling and phylogenetic comparative methods to the dataset compiled here.
In the absence of DNA sequence datasets that can be used to derive branch lengths for these taxa, this objective lies outside the scope of the current analysis and represents an open area for future investigations.
Multiple independent evolutionary shifts in the chromosome-scale distribution of crossovers have occurred during mammalian evolution, raising the question of how changes from one crossover per chromosome arm to one per chromosome are rendered at a mechanistic level. Despite order-of-magnitude differences in chromosome arm number, total genome size varies less than twofold among mammals Bachmann ; Redi and Capanna Consequently, the karyotypes of mammalian species with high chromosome arm numbers are dominated by small chromosomes.
A single crossover may suffice to ensure proper chromosome segregation on small biarmed chromosomes. Changes in chromosome content due to the accumulation of heterochromatin may also influence the chromosomal scale of the meiotic crossover constraint. The expansion of heterochromatic regions is a major mechanism for karyotype evolution in mammals Pathak et al.
Indeed, as noted above, chromosome arms dominated by heterochromatin are commonly achiasmate in North American voles, and several other mammalian species falling below the one-crossover-per-chromosome threshold also harbor large and rapidly evolving heterochromatic regions Pathak et al.
Although the accumulation of heterochromatin-dense chromosome arms that escape crossing over may provide a mechanism for shifts in the chromosomal scale of the meiotic crossover constraint, this common mode of karyotype evolution has likely had limited influence on the overall frequency of recombination in mammalian genomes Pardo-Manuel De Villena and Sapienza That is, the accumulation of recombination-inert heterochromatic sequence is not apt to promote additional crossovers in a genome, even though heterochromatin composition may determine whether the crossover distribution is defined by a minimum of one crossover per chromosome arm or one crossover per chromosome.
In addition to chromosome size and architecture, species differences in kinetochore structure could drive the evolution of the chromosomal requirement for crossing over. The kinetochore is a multiprotein complex that assembles on centromeres to link chromosomes to the spindle Przewloka and Glover Differences in kinetochore size or protein makeup could alter the number or strength of microtubule attachments, translating into unique biomechanical requirements for chiasma number and distribution along chromosomes to counterbalance spindle tension and ensure stable alignment of homologs along the metaphase plate.
Heterochromatic satellite sequences are known to serve as anchor points for the kinetochore protein scaffold Vafa et al. Although kinetochore sizes are known to differ between species Cherry et al. I have shown that house mice and North American voles possess distinct chromosome-scale crossover distributions at meiosis.
In a phylogenetic metaanalysis of recombination and karyotype data, I extended this conclusion to show that the number of crossovers has dropped below the one-per-chromosome-arm threshold multiple independent times during mammalian evolution. Although prior studies have suggested that mammalian crossover rates are constrained by a requirement of one crossover per chromosome arm Pardo-Manuel De Villena and Sapienza ; Segura et al.
These findings add an additional layer of complexity to our growing understanding of the causes of recombination rate variation and the mechanisms contributing to their evolution. At the maximum, recombination rates are presumably held in check by the essential need to maintain genome integrity Coop and Przeworski At the lower extreme, the minimum number of crossovers is constrained by their biological roles in chromosome segregation at meiosis Mather Here, I have demonstrated that this lower bound is not a simple function of chromosome or chromosome arm number, but rather a trait that itself evolves among species.
An intriguing yet unaddressed possibility is that this chromosomal constraint also varies among individuals, potentially rendering certain recombination profiles more liable to induce nondisjunction in different genetic backgrounds. I am grateful to Lisa McGraw for providing the prairie vole tissue samples used in this study. I acknowledge Bret Payseur for many stimulating conversations on the topic of recombination rate evolution that ultimately laid the motivation for this study.
Supplemental material is available online at www. Communicating editor: J. National Center for Biotechnology Information , U. Journal List Genetics v. Published online Nov Beth L. Author information Article notes Copyright and License information Disclaimer. Corresponding author. E-mail: gro. Received Jun 14; Accepted Nov 3. Available freely online through the author-supported open access option. This article has been cited by other articles in PMC.
Associated Data Data Availability Statement The author states that all data necessary for confirming the conclusions presented in this article are represented fully within the article and its supplemental files. Abstract The segregation of homologous chromosomes at the first meiotic division is dependent on the presence of at least one well-positioned crossover per chromosome. Keywords: recombination, house mouse, Mus musculus , meiosis, Microtus , voles, MLH1, karyotype, crossing over, Robertsonian translocation.
Spermatocyte cell spreads and immunostaining Spermatocyte cell spreads were prepared using the drying down method of Peters et al. Database collection and phylogenetics A database of mammalian recombination and karyotype data was compiled using literature searches Table S1. Data availability The author states that all data necessary for confirming the conclusions presented in this article are represented fully within the article and its supplemental files.
Results and Discussion Crossover rate variation among karyotypically diverse house mice Western European house mice Mus musculus domesticus are a powerful, natural model system for testing whether the chromosome-scale constraint on meiotic recombination lies at the level of the chromosome arm or the whole chromosome.
Table 1 Variation in MLH1 number and distribution in male house mice with diverse karyotypes. Strain Animal 2N No. Open in a separate window. Figure 1. The chromosomal distribution of crossovers in house mice If crossover rates in house mice are constrained by a minimum biological requirement of one crossover per chromosome, mean MLH1 foci counts should decrease in proportion to the number of Rb fusions in a karyotype.
Figure 2. RBF 3. Figure 3. Limitations of Rb mice for testing the meiotic requirement for crossing over A caveat to the use of Rb mice for understanding the meiotic constraints on crossing over is that, in addition to karyotypic differences, strains are also genetically distinct. Patterns of crossover rate variation in Microtus Gray voles of the genus Microtus are a second exemplary system for dissecting the relationship between recombination rate and karyotype.
Table 3 Variation in MLH1 count and distribution in males from karotypically diverse vole species. Figure 4. Crossing over and karyotype variation in mammals Motivated by the apparent difference in the chromosomal constraint on recombination between house mice and voles, I next sought to define the lower bound on meiotic recombination across a broader phylogenetic sample of mammals.
When DSBs happen, a homologous chromosome can serve as the template for synthesis of whatever portion of the genetic material has been lost as a result of the break. In effect, this is a form of recombination, because the broken-off area is replaced with new material from a homologous chromosome. Recombination can also be used in a similar way to repair smaller, single-stranded breaks. In general, recombination can occur any time homologous chromosomes pair up, whether they are freely floating in tandem or lined up on the metaphase plate during meiosis.
This page appears in the following eBook. Aa Aa Aa. Recombination in meiosis. Recombination occurs when two molecules of DNA exchange pieces of their genetic material with each other.
One of the most notable examples of recombination takes place during meiosis specifically, during prophase I , when homologous chromosomes line up in pairs and swap segments of DNA. This process, also known as crossing over , creates gametes that contain new combinations of genes, which helps maximize the genetic diversity of any offspring that result from the eventual union of two gametes during sexual reproduction.
Genetic diversity occurs because certain physical characteristics, like eye color, are variable; this variability is the result of alternate DNA sequences that code for the same physical characteristic. These sequences are commonly referred to as alleles. The various alleles associated with a specific trait are only slightly different from one another, and they are always found at the same location or locus within an organism's DNA.
For example, no matter whether a person has blue eyes, brown eyes, or green eyes, the alleles for eye color are found in the same area of the same chromosome in all humans. The unique combination of alleles that all sexually reproducing organisms receive from their parents is the direct result of recombination during meiosis. What happens during recombination?
Example Question 8 : Understanding Crossing Over. Possible Answers: Tetrads. Correct answer: Homologous chromosomes. Explanation : Crossing over occurs when chromosomal homologs exchange information during metaphase of Meiosis I. Example Question 9 : Understanding Crossing Over. Possible Answers: Interphase. Explanation : Crossing over occurs during prophase I when parts of the homologous chromosomes overlap and switch their genes. Copyright Notice.
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Find the Best Tutors Do not fill in this field. Your Full Name. Phone Number. Zip Code. In meiosis, they're lined up on the meiotic plates, [as they're] sometimes called, and those paired chromosomes then have to have some biological mechanism that sort of keeps them together. And it turns out that there are these things called chiasmata, which are actually where strands of the duplicated homologous chromosomes break and recombine with the same strand of the other homolog.
So if you have two Chromosome 1s lined up, one strand of one Chromosome 1 will break and it will reanneal with a similar breakage on the other Chromosome 1.
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