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.

See supplementary methods for a detailed description of the datasets, which include mitochondrial ND4 sequence data (GenBank accession numbers MW291696–291940), and a targeted sequence capture dataset that includes 1,154 nuclear loci and complete mitochondrial genomes for 104 samples. The targeted capture dataset was sequenced on the Illumina platform with paired end 100 bp reads that have been deposited in the NCBI sequence read archive under accession number PRJNA682772.