Spatiotemporal Variation in Hatching Success and Nestling Sex Ratios Track Rapid Movement of a Songbird Hybrid Zone

Abstract

Hybridization often occurs at the parapatric range interface between closely related species, but fitness outcomes vary: hybrid offspring exhibit diverse rates of viability and reproduction compared with their parental species. The mobile hybrid zone between two chickadee congeners (Poecile atricapillus #Poecile carolinensis) has been well studied behaviorally and genetically, but the viability of hybrids and the underlying mechanisms contributing to hybrid fitness have remained unclear. To better characterize the fitness costs of hybridization in this system, we analyzed 21 years of data from four sites, including more than 1,400 breeding attempts by the two species, to show that rates of hatching success changed substantially as the zone of hybridization moved across the landscape. Admixture-associated declines in hatching success correlated with reduced proportions of heterogametic (female) offspring, as predicted by Haldane’s rule. Our data support an underlying mechanism implicating genetic admixture of the homogametic (male) parent as the primary determinant of offspring sex ratio, via incompatibilities on the hemizygous Z chromosome. Our long-term study is the first to directly measure changes in fitness costs as a vertebrate hybrid zone moves, and it shows that changes in these costs are a way to track the distribution of a hybrid zone across the landscape.摘要：物种杂交通常出现在亲缘关系密切的物种之间的邻域边界范围内，但适应性结果不尽相同：与他们的双亲物种相比，杂交后代呈现出不同的成活率和繁殖率。移动杂交区域内的两种同类山雀 - 黑顶山雀和卡罗莱纳山雀 （Poecile atricapillus × Poecile carolinensis） 的行为和基因都已经得 到很好的研究，但杂交成活 力以及促成杂交后代适应性的潜在机制仍不清楚。为了更好的描述该系统中杂交的适应性代价，我们分析了来自四个地点21年的数据，包括两个物种之间超过1400次的育种尝试，从而表明随着杂交区在整个景观的变化，孵化成功率也发生了显著地变化。正如霍尔丹规则所预测的一样, 与杂交混合率相关的孵化成功率递减和异 配子（雌性）后代的比例降低呈相 关。我们的数据佐证一个潜在的机制，即同配 子（雄性）亲本遗传基因混合通过纯合子Z 染色体上 出现的不相容性，而成为后 代性别比例主要决定因素。我们的长期研究首次直接测量了随着脊椎动物杂交区域移动的适应性代价变化，并证明了这些代价的变化是追踪杂交区域在整个景观中分布的一种方式。