Mitochondrial Genomes Suggest Rapid Evolution of Dwarf California Channel Islands Foxes (Urocyon littoralis)

Island endemics are typically differentiated from their mainland progenitors in behavior, morphology, and genetics, often resulting from long-term evolutionary change. To examine mechanisms for the origins of island endemism, we present a phylogeographic analysis of whole mitochondrial genomes from the endangered island fox (Urocyon littoralis), endemic to California’s Channel Islands, and mainland gray foxes (U. cinereoargenteus). Previous genetic studies suggested that foxes first appeared on the islands >16,000 years ago, before human arrival (~13,000 cal BP), while archaeological and paleontological data supported a colonization >7000 cal BP. Our results are consistent with initial fox colonization of the northern islands probably by rafting or human introduction ~9200–7100 years ago, followed quickly by human translocation of foxes from the northern to southern Channel Islands. Mitogenomes indicate that island foxes are monophyletic and most closely related to gray foxes from northern California that likely experienced a Holocene climate-induced range shift. Our data document rapid morphological evolution of island foxes (in ~2000 years or less). Despite evidence for bottlenecks, island foxes have generated and maintained multiple mitochondrial haplotypes. This study highlights the intertwined evolutionary history of island foxes and humans, and illustrates a new approach for investigating the evolutionary histories of other island endemics.岛屿特有物种通常在行为、形态及遗传学特征上与大陆近缘祖先类群存在显著分化，该分化过程多由长期的演化改变所塑造。为探究岛屿特有性的起源机制，本研究针对加州海峡群岛特有濒危物种岛屿狐（Urocyon littoralis）与大陆灰狐（Urocyon cinereoargenteus）的完整线粒体基因组开展系统地理学（phylogeography）分析。既往遗传学研究表明，狐类早在距今16000余年、人类抵达该群岛前（约13000校准年前（cal BP））便已出现在岛屿之上；而考古与古生物学数据则支持其殖民时间早于7000校准年前（cal BP）。本研究结果与下述假说相符：狐类最初于约9200至7100年前通过漂流或人类引入的方式抵达北部岛屿，随后迅速经人类活动被从北部海峡群岛转移至南部群岛。线粒体基因组分析显示，岛屿狐为单系群，且与曾经历全新世（Holocene）气候驱动的分布区变迁的北加州灰狐亲缘关系最近。本研究数据证实岛屿狐在约2000年甚至更短的时间内便发生了快速的形态演化。尽管存在遗传瓶颈的相关证据，岛屿狐仍产生并维持了多种线粒体单倍型。本研究揭示了岛屿狐与人类相互交织的演化历程，并为探究其他岛屿特有物种的演化历史提供了全新的研究范式。