Sotola V Alex, Berg Colette S, Samuli Matthew, Chen Hongfei, Mantel Samuel J, Beardsley Paul A, Yuan Yao-Wu, Sweigart Andrea L, Fishman Lila
Department of Genetics, University of Georgia, Athens, GA 30602, USA.
Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA.
Genetics. 2023 Nov 1;225(3). doi: 10.1093/genetics/iyad156.
The evolution of genomic incompatibilities causing postzygotic barriers to hybridization is a key step in species divergence. Incompatibilities take 2 general forms-structural divergence between chromosomes leading to severe hybrid sterility in F1 hybrids and epistatic interactions between genes causing reduced fitness of hybrid gametes or zygotes (Dobzhansky-Muller incompatibilities). Despite substantial recent progress in understanding the molecular mechanisms and evolutionary origins of both types of incompatibility, how each behaves across multiple generations of hybridization remains relatively unexplored. Here, we use genetic mapping in F2 and recombinant inbred line (RIL) hybrid populations between the phenotypically divergent but naturally hybridizing monkeyflowers Mimulus cardinalis and M. parishii to characterize the genetic basis of hybrid incompatibility and examine its changing effects over multiple generations of experimental hybridization. In F2s, we found severe hybrid pollen inviability (<50% reduction vs parental genotypes) and pseudolinkage caused by a reciprocal translocation between Chromosomes 6 and 7 in the parental species. RILs retained excess heterozygosity around the translocation breakpoints, which caused substantial pollen inviability when interstitial crossovers had not created compatible heterokaryotypic configurations. Strong transmission ratio distortion and interchromosomal linkage disequilibrium in both F2s and RILs identified a novel 2-locus genic incompatibility causing sex-independent gametophytic (haploid) lethality. The latter interaction eliminated 3 of the expected 9 F2 genotypic classes via F1 gamete loss without detectable effects on the pollen number or viability of F2 double heterozygotes. Along with the mapping of numerous milder incompatibilities, these key findings illuminate the complex genetics of plant hybrid breakdown and are an important step toward understanding the genomic consequences of natural hybridization in this model system.
导致杂交后合子障碍的基因组不相容性的进化是物种分化的关键步骤。不相容性有两种常见形式：染色体间的结构差异导致F1杂种严重不育，以及基因间的上位性相互作用导致杂种配子或合子的适应性降低（多布赞斯基 - 穆勒不相容性）。尽管最近在理解这两种不相容性的分子机制和进化起源方面取得了重大进展，但每种不相容性在多代杂交中的表现仍相对未被探索。在这里，我们利用表型不同但自然杂交的猴面花Mimulus cardinalis和M. parishii之间的F2和重组自交系（RIL）杂交群体进行遗传图谱分析，以表征杂交不相容性的遗传基础，并研究其在多代实验杂交中的变化影响。在F2代中，我们发现严重的杂种花粉不育（与亲本基因型相比减少<50%）以及由亲本物种中6号和7号染色体之间的相互易位引起的假连锁。RIL在易位断点周围保留了过多的杂合性，当中间交叉未产生相容的异核型配置时，这会导致大量花粉不育。F2和RIL中强烈的传递率扭曲和染色体间连锁不平衡确定了一种新的两位点基因不相容性，导致与性别无关的配子体（单倍体）致死。后一种相互作用通过F1配子损失消除了预期的9种F2基因型类别中的3种，而对F2双杂合子的花粉数量或活力没有可检测的影响。除了对许多较温和的不相容性进行定位外，这些关键发现揭示了植物杂种衰败的复杂遗传学，是朝着理解该模型系统中自然杂交的基因组后果迈出的重要一步。
