Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference

Abstract

Recombination allows faithful chromosomal segregation during meiosis and contributes to the production of new heritable allelic variants that are essential for the maintenance of genetic diversity. Therefore, an appreciation of how this variation is created and maintained is of critical importance to our understanding of biodiversity and evolutionary change. Here, we analysed the recombination features from species representing the major eutherian taxonomic groups Afrotheria, Rodentia, Primates and Carnivora to better understand the dynamics of mammalian recombination. Our results suggest a phylogenetic component in recombination rates (RRs), which appears to be directional, strongly punctuated and subject to selection. Species that diversified earlier in the evolutionary tree have lower RRs than those from more derived phylogenetic branches. Furthermore, chromosome-specific recombination maps in distantly related taxa show that crossover interference is especially weak in the species with highest RRs detected thus far, the tiger. This is the first example of a mammalian species exhibiting such low levels of crossover interference, highlighting the uniqueness of this species and its relevance for the study of the mechanisms controlling crossover formation, distribution and resolution.

Karyotypes and recombination patterns of the Common Swift (Apus apus Linnaeus, 1758) and Eurasian Hobby (Falco subbuteo Linnaeus, 1758)

“…A relatively even crossover distribution along the macrochromosomes with moderate peaks at the chromosome ends (including pericentromeric ends of acrocentrics) has been observed in the majority of bird species examined cytologically. A polarized distribution is more typical of mammalian chromosomes (Borodin et al 2009;Segura et al 2013) and macrochromosomes of anole lizards (Lisachov et al 2017c). In birds, a pattern like this has so far been described in Zebra Finch and is considered as unique (Calderon and Pigozzi 2006;Backström et al 2010).…”

“…Crossover interference plays an important role in the determination of the number and distribution of crossovers along chromosomes (Berchowitz and Copenhaver 2010;Segura et al 2013). In this study, we measured the interference by relative distances between the neighboring MLH1 foci at the macrochromosomes: the shorter the distance, the weaker the interference.…”

“…Thus, the recombination rate cannot be lower than the haploid chromosome number (n). Studies on mammals demonstrated that chromosome number (2n) and chromosome arm number (FN) are the best predictors of the recombination rate (Pardo-Manuel de Villena and de Sapienza 2001; Segura et al 2013;Capilla et al 2016). A well-known phenomenon of crossover interference (a low probability of crossovers to occur close to each other) is an important constraint of the maximum possible rate of recombination (Berchowitz and Copenhaver 2010;Segura et al 2013).…”

Synapsis and recombination of autosomes and sex chromosomes in two terns (Sternidae, Charadriiformes, Aves)

“…Характеристики уровня рекомбинации и распределе ния кроссоверов на хромосомах изучены у многих видов млекопитающих (Segura et al, 2013;Dumont, 2017). Обна ружено, что у них количество обменов на клетку и их рас пределение по длине хромосом значительно варьируют.…”

Chromosome Synapsis and Recombination in Male Hybrids Between Two Chromosome Races of the Common Shrew (<em>Sorex araneus</em> L., Soricidae, Eulipotyphla)

“…To visualise synaptonemal complexes (SC) and the sites of crossing over we used fluorescently-labelled antibodies to SYCP3, a protein of the lateral elements of SC, and MLH1, a mismatch repair protein marking about 90% of mature recombination nodules. This approach has been successfully applied for mapping the sites of recombination in several species of mammals [15][16][17], including the common shrew [18] …”