Population differentiation, <i>F</i>_ST.

Secondary contact between closely related taxa represents a “moment of truth” for speciation—an opportunity to test the efficacy of reproductive isolation that evolved in allopatry and to identify the genetic, behavioral, and/or ecological barriers that separate species in sympatry. Sex chromosomes are known to rapidly accumulate differences between species, an effect that may be exacerbated for neo-sex chromosomes that are transitioning from autosomal to sex-specific inheritance. Here we report that, in the Solomon Islands, two closely related bird species in the honeyeater family—Myzomela cardinalis and Myzomela tristrami—carry neo-sex chromosomes and have come into recent secondary contact after ~1.1 my of geographic isolation. Hybrids of the two species were first observed in sympatry ~100 years ago. To determine the genetic consequences of hybridization, we use population genomic analyses of individuals sampled in allopatry and in sympatry to characterize gene flow in the contact zone. Using genome-wide estimates of diversity, differentiation, and divergence, we find that the degree and direction of introgression varies dramatically across the genome. For sympatric birds, autosomal introgression is bidirectional, with phenotypic hybrids and phenotypic parentals of both species showing admixed ancestry. In other regions of the genome, however, the story is different. While introgression on the Z/neo-Z-linked sequence is limited, introgression of W/neo-W regions and mitochondrial sequence (mtDNA) is highly asymmetric, moving only from the invading M. cardinalis to the resident M. tristrami. The recent hybridization between these species has thus enabled gene flow in some genomic regions but the interaction of admixture, asymmetric mate choice, and/or natural selection has led to the variation in the amount and direction of gene flow at sex-linked regions of the genome.

亲缘关系相近的类群间的次生接触（secondary contact）是物种形成进程中的‘关键时刻’——借此可检验在异域分化（allopatry）中演化形成的生殖隔离的有效性，并鉴定同域分布（sympatry）中分隔不同物种的遗传、行为或生态障碍。已知性染色体（sex chromosomes）会快速积累物种间的遗传差异，而对于正从常染色体向性别特异性遗传模式转变的新近形成的性染色体（neo-sex chromosomes）而言，这一效应可能会被进一步强化。本研究报道，在所罗门群岛，吸蜜鸟科中的两种亲缘关系相近的鸟类——红吸蜜鸟（Myzomela cardinalis）与特氏吸蜜鸟（Myzomela tristrami）——携带有新近形成的性染色体，且在经历约110万年的地理隔离后，近期发生了次生接触。这两个物种的杂交个体最早于约100年前在同域分布区域被观测到。为阐明杂交事件的遗传后果，我们对采自异域分布区和同域分布区的个体开展群体基因组学分析，以刻画该物种接触带中的基因流（gene flow）特征。基于全基因组水平的多样性、分化与趋异估计，我们发现基因组不同区域的基因渐渗（introgression）程度与方向存在显著差异。对于同域分布的鸟类而言，常染色体区域的基因渐渗呈双向模式，两个物种的表型杂交个体与表型亲本个体均呈现混合的祖先成分。然而，基因组的其他区域则呈现截然不同的模式：尽管Z/新近Z连锁序列区域的基因渐渗较为有限，但W/新近W区域以及线粒体DNA（mtDNA）的基因渐渗具有高度的不对称性，仅从入侵物种红吸蜜鸟流向本地物种特氏吸蜜鸟。因此，这两个物种间的近期杂交使得部分基因组区域发生了基因交流，但遗传混合、不对称配偶选择以及自然选择的共同作用，导致基因组性连锁区域的基因流在数量与方向上存在差异。