Meiotic pairing and double strand break formation along the heteromorphic threespine stickleback sex chromosomes

Abstract

Double strand break repair during meiosis is normally achieved using the homologous chromosome as a repair template. Heteromorphic sex chromosomes have reduced sequence homology with one another, presenting unique challenges to the repair of double strand breaks. Our understanding of how heteromorphic sex chromosomes behave during meiosis has been largely limited to the ancient sex chromosomes of mammals, where the X and Y differ markedly in overall structure and gene content. Consequently, pairing of the X and Y chromosomes is limited to a small pseudoautosomal region. It remains unclear how more recently evolved sex chromosomes, that share considerably more sequence homology with one another, pair and repair double strand breaks during meiosis. One possibility is barriers to pairing evolve rapidly. Alternatively, recently evolved sex chromosomes may exhibit pairing and double strand break repair that more closely resembles that of their autosomal ancestors. Here we use the recently evolved X and Y chromosomes of the threespine stickleback fish (Gasterosteus aculeatus) to study patterns of pairing and double stranded break formation using molecular cytogenetics. We found that the sex chromosomes of threespine stickleback fish do not pair exclusively in the pseudoautosomal region. Instead, the chromosomes fully pair in a non-homologous fashion. To achieve this, the X chromosome underwent synaptic adjustment during pachytene to match the axis length of the Y chromosome. Double strand break formation and repair rate also matched that of the autosomes. Our results highlight that recently evolved sex chromosomes exhibit meiotic behavior that is reminiscent of autosomes and argues for further work to identify the homologous templates that are used to repair double strand breaks on the X and Y chromosomes.

Sex chromosome differentiation via changes in the Y chromosome repeat landscape in African annual killifishes Nothobranchius furzeri and N. kadleci

“…Sex chromosome differentiation gradually affects their pairing in meiosis, regions with substantial sequence divergence might exhibit delayed pairing or remain asynaptic. Bivalent formed by heteromorphic sex chromosomes often undergoes size equalization also known as synaptic adjustment, as also reported from fishes [55,60,76,77]. Our analyses of meiotic chromosomes showed that despite their differentiation, X and Y sex chromosomes fully pair in N. furzeri and N. kadleci .…”

“…The rationale is that sex chromosomes of different sizes should display different locations of telomeric signals if they are heteromorphic and aligned into bivalent without a synaptic adjustment (e.g. [59, 60]). In our sampling the telomeric signals were always confined to the very ends of all bivalents (S14 Fig), suggesting synaptic adjustment in heteromorphic XY bivalent.…”