Parental population range expansion before secondary contact promotes heterosis

AbstractPopulation genomic analysis of hybrid zones is instrumental to our understanding of the evolution of reproductive isolation. Many temperate hybrid zones are formed by the secondary contact between two parental populations that have undergone post-glacial range expansion. Here we show that explicitly accounting for historical parental isolation followed by range expansion prior to secondary contact is fundamental for explaining genetic and fitness patterns in these hybrid zones. Specifically, ancestral population expansion can result in allele surfing where neutral or slightly deleterious mutations drift to high frequency at the expansion front. If these surfed deleterious alleles are recessive, they can contribute to substantial heterosis in hybrids produced at secondary contact, counteracting negative effects of Bateson-Dobzhansky-Muller incompatibilities (BDMIs) hence weakening reproductive isolation. When BDMIs are linked to such recessive deleterious alleles the fitness benefit of introgression at these loci can facilitate introgression at the BDMIs. The extent to which this occurs depends on the strength of selection against the linked deleterious alleles and the distribution of recombination across the chromosome. Finally, surfing of neutral loci can alter the expected pattern of population ancestry, thus accounting for historical population expansion is necessary to develop accurate null genomic models of secondary-contact hybrid zones.

**摘要** 杂交带的群体基因组学分析，对理解生殖隔离的演化进程具有关键意义。多数温带杂交带由两个经历冰期后范围扩张的亲本种群二次接触形成。本研究表明，若要合理解释此类杂交带中的遗传与适合度模式，必须明确纳入冰期前亲本种群的分化隔离与二次接触前的种群范围扩张过程。具体而言，祖先种群的范围扩张可引发等位基因冲浪（allele surfing）现象：中性或轻度有害突变会在扩张前沿通过遗传漂变达到较高频率。若此类经冲浪的有害等位基因为隐性，则会在二次接触产生的杂交后代中引发显著的杂种优势，抵消Bateson-Dobzhansky-Muller不相容性（BDMIs）的负面影响，进而削弱生殖隔离。当BDM不相容性与这类隐性有害等位基因连锁时，这些位点的基因渗入所带来的适合度优势，可促进BDM不相容性位点的基因渗入。该效应的强弱取决于连锁有害等位基因的选择压强度，以及染色体上重组位点的分布格局。最后，中性位点的等位基因冲浪可改变预期的群体祖先成分分布模式，因此，若要构建二次接触杂交带的精准基因组零模型，必须纳入历史种群扩张的相关因素。