Genomic analysis reveals hidden biodiversity within colugos, the sister group to primates

Abstract

Colugos are among the most poorly studied mammals despite their centrality to resolving supraordinal primate relationships. Two described species of these gliding mammals are the sole living members of the order Dermoptera, distributed throughout Southeast Asia. We generated a draft genome sequence for a Sunda colugo and a Philippine colugo reference alignment, and used these to identify colugo-specific genetic changes that were enriched in sensory and musculoskeletal-related genes that likely underlie their nocturnal and gliding adaptations. Phylogenomic analysis and catalogs of rare genomic changes overwhelmingly support the contested hypothesis that colugos are the sister group to primates (Primatomorpha), to the exclusion of treeshrews. We captured ~140 kb of orthologous sequence data from colugo museum specimens sampled across their range and identified large genetic differences between many geographically isolated populations that may result in a >300% increase in the number of recognized colugo species. Our results identify conservation units to mitigate future losses of this enigmatic mammalian order.

Keywords: Colugo; Southeast Asia; biogeography; genetics; genomic analysis; phylogenomics; population dynamics.

Fig. 1. Phylogenetic placement of Dermoptera.

(A) Phylogenies depicting alternative hypotheses for dermopteran relationships relative to primates and treeshrews. (B) Number of indels supporting each evolutionary relationship. (C) Number of transposed elements supporting each evolutionary relationship.

Fig. 2. Functional gene evolution and positive selection in colugos and ancestral primates.

(A) Relative abundance of functional V1R (orange) and OR (blue) genes across sequenced mammals. The size of the circles is proportional to the number of functional genes. (B) Colugo gliding with patagium fully extended. (C). Venn diagram showing relationship between categories of enriched disease gene categories of colugo positively selected genes.

Fig. 3. Colugo phylogeography based on museomics.

(A to C) Timetrees based on major lineages within phylogenies representing maternal (mtDNA; 16.6 kb), biparental (autosome + chrX; 115.6 kb), and paternal (chrY; 24.3 kb) evolutionary histories (figs. S7 to S12). Nodes with 100% maximum likelihood bootstrap support are denoted with red asterisks. Maps depict sample collection locations for each tree with corresponding colored symbol. Boxes indicate highly supported monophyletic clusters or divergent lineages representing putative species. Gray vertical bars denote times of low sea stands. VNM, Vietnam; THA, Thailand; PM, Peninsular Malaysia; S. SUM, south Sumatra; E/SE. BOR, east/southeast Borneo; NE BOR, northeast Borneo; SW BOR, southwest Borneo; NW. BOR, northwest Borneo; BUN, Bunguran; BAS, Basilan; E. MIN, eastern Mindanao; W. MIN, western Mindanao; BOL, Bohol; LTE, Leyte; SAM, Samar; DIN, Dinagat.

Fig. 4. Comparison of genetic distance between well-established species and proposed species groups for Galeopterus and Cynocephalus.

(A and B) mtDNA and nuclear DNA. The x axis lists the name of each genus followed by the number of species in that genus that were compared. For colugo genera, this number represents a conservative number of proposed groups/species. Colugo genera are highlighted in red and blue boxes.