Interspecific introgression and widespread intraspecific gene flow in a clade of tropical and subtropical seabirds

The mechanisms that restrict gene flow between populations and facilitate population differentiation and speciation vary across the tree of life. In systems where physical barriers to gene flow are dynamic over time and space, such as many marine species, genetic introgression may be a major factor in the speciation process. In sympatric species of seabirds, hybridization has been frequently observed but few studies have investigated patterns of introgression. We used whole-genome sequence data to test for interspecific introgression between five pairs of tropical and subtropical seabird species and to test for gene flow within species across major land mass barriers and ocean basins. We found evidence for introgression between: blue-footed (Sula nebouxii) and Peruvian boobies (S. variegata); masked (S. dactylatra) and Nazca boobies (S. granti); and blue-footed and Nazca boobies. We found no evidence of introgression between blue-footed and brown boobies (S. leucogaster), or masked and brown boobies, despite observed hybridization between these species. We also found evidence for gene flow across several major land masses in three pantropical species: red-footed (S. sula), brown, and masked boobies. Finally, we report mixed evidence for ancient introgression between brown boobies and the ancestor of blue-footed, Peruvian, masked, and Nazca boobies. Our work indicates (1) that interspecific introgression has shaped contemporary booby diversity in the eastern Pacific, and (2) that contemporary physical barriers to gene flow between booby colonies are not absolute. Our findings contribute novel insights to the growing body of evidence that introgression is a widespread evolutionary process.

限制种群间基因流、推动种群分化与物种形成的机制，在生命之树中呈现出广泛的多样性。在基因流物理屏障随时间与空间动态变化的类群（如多数海洋物种）中，遗传渐渗（genetic introgression）可能是物种形成过程中的关键影响因素。在海鸟的同域物种中，杂交现象已被频繁观测到，但针对遗传渐渗模式的研究却寥寥无几。本研究利用全基因组测序数据，对5对热带与亚热带海鸟物种间的种间遗传渐渗进行了检验，同时检测了跨主要陆地屏障与海盆的种群内基因流情况。研究发现以下类群间存在遗传渐渗证据：蓝脚鲣鸟（Sula nebouxii）与秘鲁鲣鸟（S. variegata）；蓝脸鲣鸟（S. dactylatra）与纳斯卡鲣鸟（S. granti）；以及蓝脚鲣鸟与纳斯卡鲣鸟。尽管已有观测记录显示蓝脚鲣鸟与棕鲣鸟（S. leucogaster）、蓝脸鲣鸟与棕鲣鸟之间存在杂交现象，但本研究未发现这两组类群间存在遗传渐渗的证据。此外，我们在3种泛热带海鸟物种中发现了跨主要陆地屏障的基因流证据：红脚鲣鸟（S. sula）、棕鲣鸟与蓝脸鲣鸟。最后，本研究报道了棕鲣鸟与蓝脚鲣鸟、秘鲁鲣鸟、蓝脸鲣鸟及纳斯卡鲣鸟的祖先之间存在古老遗传渐渗的混合证据。本研究表明：其一，种间遗传渐渗塑造了东太平洋地区现存的鲣鸟物种多样性；其二，鲣鸟种群间现存的基因流物理屏障并非绝对。本研究的发现为日益增多的证据链提供了新的见解，证实遗传渐渗是一种广泛存在的进化过程。