Interspecific hybridization and island colonization history, not rarity, most strongly affect the genetic diversity in a clade of Mascarene-endemic trees

Many factors shape the genetic diversity of island-endemic trees, with important implications for conservation. Oceanic island-endemic lineages undergo an initial founding bottleneck during the colonization process and subsequently accumulate diversity following colonization. Moreover, many island endemics occur in small populations and are further threatened by anthropogenic factors that cause population declines, making them susceptible to losses in genetic diversity through genetic drift, inbreeding, and bottlenecks. However, life-history traits commonly found in trees, such as outcrossing mechanisms, long lifespans, and a propensity for interspecific hybridization, may help buffer against losses of genetic variation. To assess the relative importance of colonization history, rarity, and distribution in shaping genetic diversity of island-endemic trees, we conducted a comparative population genomic analysis of 13 species of Diospyros (Ebenaceae) endemic to the Mascarene Islands that differ in island colonization history, distribution, population size, and IUCN threat status. We genotyped 328 individuals across the islands using 2b-RADseq, compared genetic diversity both among and within species, and assessed patterns of genetic structure. Genetic diversity did not vary significantly by IUCN status, but we found that species that co-occur with others on the same intermediate-aged island (Mauritius) had much greater genetic diversity than those that occur solitarily on an island (Réunion and Rodrigues), likely because of greater interspecific hybridization among species with overlapping distributions and processes related to time since island colonization. Results presented here were used to determine priority localities for in situ and ex situ conservation efforts to maximize the genetic diversity of each Mascarene Diospyros species.诸多因素共同塑造了岛屿特有树木的遗传多样性，这对物种保护工作具有重要启示。大洋岛屿特有谱系在定殖过程中会经历初始奠基者瓶颈效应，随后在定殖后逐步积累遗传多样性。此外，多数岛屿特有物种种群规模偏小，且面临导致种群衰退的人为因素威胁，因此更易因遗传漂变、近交及瓶颈效应发生遗传多样性丢失。不过树木普遍具有的生活史特征，如异交机制、较长寿命以及种间杂交倾向，或可缓冲遗传变异的丢失。为评估定殖历史、种群稀有性以及分布格局在塑造岛屿特有树木遗传多样性中的相对重要性，我们针对马斯克林群岛（Mascarene Islands）的13种柿属（Diospyros，柿科Ebenaceae）特有树种开展了比较种群基因组学分析，这些物种在岛屿定殖历史、分布格局、种群规模以及世界自然保护联盟（IUCN）濒危等级方面均存在差异。我们利用2b-RADseq技术对群岛范围内的328个个体进行了基因分型，比较了物种种间与种内的遗传多样性，并评估了遗传结构模式。遗传多样性并未随IUCN濒危等级出现显著差异，但我们发现，与其他物种同域分布于中等年龄岛屿（毛里求斯）的物种，其遗传多样性远高于仅单独分布于单一岛屿（留尼旺与罗德里格斯）的物种，这可能是因为分布重叠的物种间发生了更强的种间杂交，以及与岛屿定殖时长相关的演化过程所导致。本研究所得结果可用于确定原位保护与迁地保护的优先区域，以最大化保留各马斯克林群岛柿属物种的遗传多样性。