Diverge and conquer: Phylogenomics of southern Wallacean forest skinks (Genus: Sphenomorphus) and their colonization of the Lesser Sunda Archipelago

The archipelagos of Wallacea extend between the Sunda and Sahul Shelves, serving as a semi-permeable two-way filter influencing faunal exchange between Asia and Australo-Papua. Forest skinks (Genus Sphenomorphus) are widespread throughout southern Wallacea and exhibit complex clinal, ontogenetic, sexual, and seasonal morphological variation rendering species delimitation difficult. We screened a mitochondrial marker for 245 Sphenomorphus specimens from this area to inform the selection of 104 samples from which we used targeted sequence-capture to generate a dataset of 1154 nuclear genes (~1.8 Mb) plus complete mitochondrial genomes. Phylogenomic analyses recovered many deeply divergent lineages, three of which are now sympatric, that began to diversify in the late Miocene shortly after the oldest islands are thought to have become emergent. We infer a complex and non-stepping-stone pattern of island colonization, with the group having originated in the Sunda Arc islands before using Sumba as a springboard for colonization of the Banda Arcs. Estimates of population structure and gene flow across the region suggest total isolation except between two Pleistocene Aggregate Island Complexes that become episodically land-bridged during glacial maxima. These historical processes have resulted in at least 11 Sphenomorphus species in the region, nine of which require formal description. This fine-scale geographic partitioning of undescribed species highlights the importance of utilizing comprehensive genomic studies for defining biodiversity hotspots to be considered for conservation protection.

华莱士区（Wallacea）的群岛分布于巽他陆架（Sunda Shelves）与萨胡尔陆架（Sahul Shelves）之间，是一道半渗透性的双向过滤屏障，影响着亚洲与澳巴布亚（Australo-Papua）地区的动物区系交流。蜓蜥属（Sphenomorphus）的森林石龙子广泛分布于华莱士区南部，其形态变异复杂多样，涵盖渐变群、个体发育、性别及季节维度，这给物种界定工作带来了极大挑战。我们对该区域的245份蜓蜥属标本开展了线粒体分子标记筛选，以此确定104份样本用于后续研究；随后通过靶向序列捕获（targeted sequence-capture）技术，构建了包含1154个核基因（约1.8 Mb）以及完整线粒体基因组的数据集。系统发育基因组学分析发现了多个深度分化的支系，其中3个支系如今呈同域分布；这些支系的多样化始于中新世晚期（Late Miocene），恰好是学界认为最古老的岛屿浮出海面之后不久。我们推断该类群的岛屿定殖模式复杂且并非阶梯式扩散：该类群起源于巽他弧（Sunda Arc）岛屿，随后以松巴岛（Sumba）为跳板，完成了对班达弧（Banda Arcs）区域的定殖。对该区域种群结构与基因流的估算结果显示，除两处更新世（Pleistocene）复合岛屿群外，其余区域的种群均处于完全隔离状态；这两处复合岛屿群在冰期极盛期（glacial maxima）会间歇性形成陆桥相连。上述历史进程使得该区域至少存在11种蜓蜥属物种，其中9种尚待正式描述发表。这种未描述物种的精细地理分布格局，凸显了利用全面基因组学研究来界定生物多样性热点区域并纳入保护考量的重要性。