USGS Science⌕ Search
Home/Archive/USGS

USGS · 70229992

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

Robert S. Cornman·Paul M. Cryan
View original source ↗Export metadata ↓

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.

Explore related subjects

PeerJArticle

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Robert S. Cornman, Paul M. Cryan. 2022-03-17. Positively selected genes in the hoary bat (Lasiurus cinereus) lineage: Prominence of thymus expression, immune and metabolic function, and regions of ancient synteny. https://doi.org/10.7717/peerj.13130

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related USGS reports

USGS2026

The Appalbees menu: A multiyear, multilocus metagenetic assessment of pollen foraging by Appalachian Bombus affinis workers

Background Detailed studies of foraging behavior are needed for scientific management of the endangered rusty-patched bumblebee ( Bombus affinis ) in the disjunct and ecologically differentiated habitats it presently occupies. Current knowledge gaps hinder recovery planning but are challenging to redress through direct observation of rare interactions in the field. Methods We used genetic metabarcoding to characterize the taxonomic composition of pollen collected by B. affinis workers in the Appalachian mountains of Virginia and West Virginia from 2021–2023. We developed a custom sequence database of the regional flora and compared results for two independent genetic loci, internal transcribed spacer 1 and internal transcribed spacer 2 (ITS1 and ITS2). Results While ITS2 consistently detected more plant diversity, results from the two loci were broadly concordant with a few notable exceptions. The plant genera Hydrangea , Actaea , Rhododendron , Tilia , and (unexpectedly) Laportea were prominent in midsummer samples, with Rubus a consistent contributor in late spring and early summer. Pea flowers (family Fabaceae) were relatively infrequent but the genera Securigera and Trifolium were detected before the Hydrangea bloom and again in late summer afterwards. The diversity of forage plants was highest in late summer, driven primarily by various genera of Asteraceae. Comparing the current data with previous work indicates regional differentiation in forage plants between Appalachia and the upper Midwest, but also allows ‘consensus’ forage sources that are supported by multiple lines of evidence and shared between regions to be tabulated. These results should help managers focus survey efforts for this endangered species and plan habitat enhancements.

Illinois, Virginia, West Virginia, Wisconsin↗
USGS2025

Gram staining reveals diverse bacterial associations in coral cell-associated microbial aggregates in the Pacific Ocean

Cell-associated microbial aggregates (CAMAs) (also referred to as coral-associated microbial aggregates) have been observed in 24 coral species from the Pacific Ocean, and studies indicate most contain gram-negative bacilli from the genus Endozoicomonas. Here, we used histology with Gram staining to evaluate the morphology and distribution of CAMAs in six species of scleractinian corals from Hawaii and Palmyra. Within CAMAs, we observed the coexistence of bacteria with differing morphologies and Gram-staining properties both within and among coral species. Pocillopora and Acropora had mostly gram-negative bacilli, whereas gram-negative cocci dominated in Porites . Acropora had the highest abundance of gram-positive CAMAs. The anatomical distribution of CAMAs varied by coral species. CAMAs dominated in the tentacles of Pocillopora meandrina , Pocillopora grandis , and Porites evermanni, were mostly in the coenenchyme of Acropora cytherea , and were found equally between tentacles and coenenchyme in Porites compressa and Porites lobata . Tissue-layer distribution also varied, with CAMAs mainly in the epidermis of Pocillopora but in the gastrodermis of Porites and Acropora . The diversity of bacteria in CAMAs and their anatomic distribution in Pacific corals may be more complex than previously understood. This indicates other bacterial species, in addition to Endozoicomonas, are colonizing CAMAs in corals from the Pacific Ocean.

Hawaii↗
USGS2025

Molecular evolution of TRPC4 regulatory sequences supports a role in mammalian thermoregulatory adaptation

Background Proteins encoded by the canonical transient receptor potential (Trpc) gene family form transmembrane channels involved in diverse signal-transduction pathways. Trpc4 has been shown necessary for the induction of nonshivering thermogenesis (NST) in mice, a key component of which is thermogenic brown adipose tissue (BAT). In bats, T rpc4 exhibited diversifying selection within exons encoding regulatory binding sites of TRPC4. Methods To assess whether diversification of these regulatory sequences mirrors the diversification of mammalian thermoregulatory strategies, the ratio of nonsynonymous to synonymous substitutions (ω) was estimated for multiple tetrapod outgroups and eutherian orders. Four questions were addressed: (1) Did the ancestral eutherian Trpc4 diverge under positive selection from nonplacental mammals that lack BAT? (2) Did Trpc4 subsequently become more constrained in descendant eutherian clades? (3) In eutherian clades that subsequently lost BAT by inactivation of the thermogenin gene Ucp1 , did Trpc4 become less constrained? (4) Does the evolutionary rate of Trpc4 differ between quantitatively more heterothermic mammal orders (bats and rodents) relative to quantitatively less heterothermic outgroups (carnivores, artiodactylids, and primates)? Results Coincident with the advent of BAT, Trpc4 evolutionary rate increased significantly in ancestral eutheria after their divergence from nonplacental mammals but a branch-site model did not support a rate class ω > 1 along that branch. In descendant eutherian mammals, Trpc4 became far more constrained, with an evolutionary rate less than half that of tetrapod clades lacking NST, a pattern was not seen in other Trp channel genes. Intensifying selection in descendent eutherian mammals was further supported with the RELAX program, which also indicated reduced constraint on Trpc4 in clades that have secondarily lost BAT. However, no consistent pattern was identified within mammalian orders with strong variation in heterothermy: evidence of increased evolutionary rate was again found in bats for Trpc4 as well as homologs it directly binds in heteromeric membrane channels ( Trpc5 and Trpc1 ), yet all rodent Trpc genes had low evolutionary rates. Evolutionary rates of Trpc4 and Trpc1 in bats were consistent with relaxed constraint whereas bat Trpc5 experienced diversifying selection. Most variation among tetrapod TRPC4 sequences lies within an 85 amino-acid window that is functionally uncharacterized. Sequence alignments demonstrated that the TRPC4 β isoform, which lacks a portion of the C-terminal regulatory region, originated in basal eutherians but appears to be lost in many tip lineages. Collectively, the data indicate that the C-terminal region of TRPC4 has responded to selection on NST thermoregulation during the diversification of eutherian mammals. The drivers of increased diversification of Trpc4 and interacting genes in bats remain to be determined.

PeerJ↗