Data from: Large-scale introduction of the Indo-Pacific damselfish Abudefduf viagiensis into Hawai‘i promotes genetic swamping of the endemic congener A. abdominalis

Hybridization in the ocean was once considered rare, a process prohibited by the rapid evolution of intrinsic reproductive barriers in a high-dispersal medium. However, recent genetic surveys have prompted a reappraisal of marine hybridization as an important demographic and evolutionary process. The Hawaiian Archipelago offers an unusual case history in this arena, due to the recent arrival of the widely distributed Indo-Pacific Sergeant (Abudefduf vaigiensis), which is hybridizing with the endemic congener A. abdominals. Surveys of mtDNA and three nuclear loci across Hawai‘i (N = 396, A. abdominalis and N = 314, A. vaigiensis) reveal that hybridization is significantly higher in the human-perturbed southeast archipelago (19.8%), tapering off to 5.9% in the pristine northwest archipelago. While densities of the two species varied throughout Hawai‘i, hybridization was highest in regions with similar species densities, contradicting the generalization that unequal densities promote hybridization. Our finding of later generation hybrids throughout the archipelago invokes the possibility of genetic swamping of the endemic species. An exaption, an adaptation with unintended consequences, may explain these findings: the endemic species has transient yellow coloration during reproduction, whereas the introduced species has yellow coloration continuously as adults, in effect a permanent signal of reproductive receptivity. Haplotype diversity is higher in Hawaiian A. vaigiensis than in our samples from the native range, indicating large-scale colonization almost certainly facilitated by the historically recent surge of marine debris. In this chain of events, marine debris promotes colonization, exaption promotes hybridization, and introgression invokes the possible collapse of an endemic species.

海洋杂交曾被认为是罕见现象，在高扩散介质中，内在生殖屏障的快速演化本会阻断该过程的发生。然而，近期的遗传学调查促使学界重新评估海洋杂交，将其视为重要的种群动态与演化过程。夏威夷群岛为此类研究提供了一则罕见的典型案例：近期广泛分布的印度-太平洋雀鲷（Indo-Pacific Sergeant，*Abudefduf vaigiensis*）传入该海域，并与特有近缘种白带豆娘鱼（*A. abdominalis*）发生杂交。本次研究对夏威夷群岛范围内的线粒体DNA（mtDNA）与3个核基因座（nuclear loci）开展了调查，共采样396尾白带豆娘鱼（*A. abdominalis*）与314尾印度-太平洋雀鲷（*A. vaigiensis*）。结果显示，群岛东南部受人类活动干扰的区域杂交率显著更高（19.8%），而在未受破坏的西北部区域杂交率降至5.9%。尽管夏威夷群岛内两种鱼类的种群密度存在空间差异，但杂交率在两者密度相近的区域达到峰值，这与“种群密度不均会促进杂交”的通用结论相悖。本次研究在全群岛范围内均检测到晚世代杂交个体，这提示存在特有物种遭遇遗传淹没（genetic swamping）的潜在风险。预适应（exaption）——即带来非预期后果的适应性特征——或可解释上述结果：特有种仅在繁殖期呈现短暂的黄色体色，而传入种的成体则终生保持黄色体色，本质上是一种永久性的繁殖接受信号。夏威夷群岛的印度-太平洋雀鲷单倍型多样性（haplotype diversity）高于我们在其原生分布区采集的样本，这表明该物种的大规模定殖很可能得益于近年全球海洋垃圾数量激增的助力。在这一系列事件链中，海洋垃圾促进物种定殖，预适应推动杂交发生，而基因渐渗（introgression）则可能最终导致特有物种的种群崩溃。