Linkage mapping reveals strong chiasma interference in sockeye salmon: implications for interpreting genomic data

Meiotic recombination is fundamental for generating new genetic variation and for securing proper disjunction. Further, recombination plays an essential role during the rediploidization process of polyploid-origin genomes because crossovers between pairs of homeologous chromosomes retain duplicated regions. A better understanding of how recombination affects genome evolution is crucial for interpreting genomic data; unfortunately, current knowledge mainly originates from a few model species. Salmonid fishes provide a valuable system for studying the effects of recombination in nonmodel species. Salmonid females generally produce thousands of embryos, providing large families for conducting inheritance studies. Further, salmonid genomes are currently rediploidizing after a whole genome duplication and can serve as models for studying the role of homeologous crossovers on genome evolution. Here, we present a detailed interrogation of recombination patterns in sockeye salmon (Oncorhynchus nerka). First, we use RAD sequencing of haploid and diploid gynogenetic families to construct a dense linkage map that includes paralogous loci and location of centromeres. We find a nonrandom distribution of paralogs that mainly cluster in extended regions distally located on 11 different chromosomes, consistent with ongoing homeologous recombination in these regions. We also estimate the strength of interference across each chromosome; results reveal strong interference and crossovers are mostly limited to one per arm. Interference was further shown to continue across centromeres, but metacentric chromosomes generally had at least one crossover on each arm. We discuss the relevance of these findings for both mapping and population genomic studies.

减数分裂重组（Meiotic recombination）是产生新遗传变异、保障染色体正确分离的核心生物学过程。进一步而言，重组在多倍体起源基因组的再二倍化进程中发挥关键作用，因为部分同源染色体（homeologous chromosomes）间的交叉交换可保留重复基因组区域。深入解析重组对基因组演化的影响机制，对于解读基因组数据至关重要；但遗憾的是，当前相关认知主要源自少数模式物种。鲑科鱼类为研究非模式物种中的重组效应提供了极具价值的实验体系。鲑科雌性通常可产出数千枚胚胎，可为遗传研究提供庞大的家系群体。此外，鲑科基因组在经历全基因组复制（whole genome duplication）后正处于再二倍化阶段，可作为研究部分同源染色体交叉对基因组演化影响的理想模型。
本研究对红大马哈鱼（Oncorhynchus nerka）的重组模式展开了详细解析。首先，我们利用单倍体与二倍体雌核发育家系的RAD测序（RAD sequencing）技术，构建了包含旁系同源基因座（paralogous loci）与着丝粒位置的高密度连锁图谱。研究发现旁系同源基因的分布并非随机，其主要聚集在11条不同染色体的远端延伸区域，这与这些区域持续发生的部分同源重组现象相符。我们还估算了每条染色体上的交换干涉强度，结果显示存在强烈的交换干涉，且每条染色体臂通常仅发生一次交叉。进一步研究表明，交换干涉可跨越着丝粒，但中部着丝粒染色体（metacentric chromosomes）的每条臂通常至少存在一次交叉。最后，我们探讨了本研究结果在连锁图谱构建与群体基因组学研究中的相关意义。