Positively selected genes in the hoary bat (Lasiurus cinereus) lineage: prominence of thymus expression, immune and metabolic function, and regions of ancient synteny

Abstract

Background Bats of the genus Lasiurus occur throughout the Americas and have diversified into at least 20 species among three subgenera. The hoary bat (Lasiurus cinereus) is highly migratory and ranges farther across North America than any other wild mammal. Despite the ecological importance of this species as a major insect predator, and the particular susceptibility of lasiurine bats to wind turbine strikes, our understanding of hoary bat ecology, physiology, and behavior remains poor. Methods To better understand adaptive evolution in this lineage, we used whole-genome sequencing to identify protein-coding sequence and explore signatures of positive selection. Gene models were predicted with Maker and compared to seven well-annotated and phylogenetically representative species. Evolutionary rate analysis was performed with PAML. Results Of 9,447 single-copy orthologous groups that met evaluation criteria, 150 genes had a significant excess of nonsynonymous substitutions along the L. cinereus branch (P < 0.001 after manual review of alignments). Selected genes as a group had biased expression, most strongly in thymus tissue. We identified 23 selected genes with reported immune functions as well as a divergent paralog of Steep1 within suborder Yangochiroptera. Seventeen genes had roles in lipid and glucose metabolic pathways, partially overlapping with 15 mitochondrion-associated genes; these adaptations may reflect the metabolic challenges of hibernation, long-distance migration, and seasonal variation in prey abundance. The genomic distribution of positively selected genes differed significantly from background expectation by discrete Kolmogorov–Smirnov test (P < 0.001). Remarkably, the top three physical clusters all coincided with islands of conserved synteny predating Mammalia, the largest of which shares synteny with the human cat-eye critical region (CECR) on 22q11. This observation coupled with the expansion of a novel Tbx1-like gene family may indicate evolutionary innovation during pharyngeal arch development: both the CECR and Tbx1 cause dosage-dependent congenital abnormalities in thymus, heart, and head, and craniodysmorphy is associated with human orthologs of other positively selected genes as well.