Sex Chromosome Synapsis and Recombination in Male Guppies

Abstract

Guppy X and Y chromosomes represent an early stage in sex chromosome divergence. Synapsis and recombination between X and Y chromosomes attract special attention because recombination suppression promotes their differentiation, but previous studies have given contradictory results. Linkage analysis indicated that recombination between X and Y was extremely rare (<10%) and occurred in the medial part of the Y chromosome, while cytological analysis demonstrated regular association between the distal ends of the X and Y at diakinesis. In this study, we examine pairing and recombination between X and Y chromosomes using immunolocalization of MLH1 to mark recombination nodules, and genomic in situ hybridization with a male DNA probe to identify the Y-specific heterochromatic region. Pairing between X and Y is initiated distally. Single crossovers were detected in 87% of XY synaptonemal complexes, most often in the distal region and less frequently in a median position indicating that end-to-end associations between X and Y are chiasmatic. Thus, we suggest that the very low frequency of recombination detected by linkage analysis in a previous study resulted from a lack of informative markers in distal regions.

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

“…We estimate the overall number and distribution of recombination events along the chromosomes of these species, using immunolocalization of SYCP3, the protein of the SC lateral elements, MLH1, the mismatch repair protein marking mature recombination nodules, and centromere proteins. This method has been successfully used to analyze recombination landscapes in fish (Moens 2006;Lisachov et al 2015), reptiles (Lisachov et al 2017b, c), mammals (Capilla et al 2016) and birds (Pigozzi 2016). This approach has lower resolution than linkage analysis at the fine scale level.…”

Heteromorphism of “Homomorphic” Sex Chromosomes in Two Anole Species (Squamata, Dactyloidae) Revealed by Synaptonemal Complex Analysis

“…We did not observe recombination in the fragment that is distal to the loop in D. coelestinus (short arm of the short homologue), but this region is presumably homologous because it forms a normal SC. Otherwise the distal heteromorphic fragments would be unpaired at earlier stages, and the XY bivalent would undergo synaptic adjustment similar to that detected in the sex bivalents of birds [Solari, 1992] and guppy [Lisachov et al, 2015]. The occurrence of MLH1 foci in all parts of the sex bivalents except the loop regions indicates high conservation of homology between the X and Y chromosomes.…”

“…During meiotic progression the axes become equalized and the loop disappears. The equalization or synaptic adjustment of heteromorphic chromosomes has been described for the sex chromosomes of the guppy ( Poecilia reticulata ) [Traut and Winking, 2001;Lisachov et al, 2015], the Nile tilapia ( Oreochromis niloticus ) [Carrasco et al, 1999], and birds [Pigozzi, 2001]. A similar synaptic pattern has been observed in fence lizards (genus Sceloporus , Pleurodonta), which have an XY system homologous to the anole system.…”

“…Moreover, because the homologues are paired, regional differences in size and content can be detected as SC asymmetry. The distribution of recombination nodules along the XY SC clearly identifies the location of the pseudoautosomal region and indicates the distinction between common and differential segments [Pigozzi and Solari, 2005;Pigozzi, 2011;Lisachov et al, 2015].…”

Microchromosome polymorphism in the sand lizard, Lacerta agilis Linnaeus, 1758 (Reptilia, Squamata)

“…The SC analysis via electron microscopy and immunofluorescent staining is widely used in vertebrate cytogenetics (Lisachov et al 2015; Wallace and Wallace 1995; Reed et al 1990; Calderon and Pigozzi 2006; Basheva et al 2014). At pachytene, the compactization of chromatin is much lower than at metaphase, and thus the SC analysis provides higher resolution than the conventional metaphase techniques.…”