Complete mitochondrial genomes of three vulnerable cave bat species and their phylogenetic relationships within the order Chiroptera

Abstract

The IUCN Red List of Threatened Species contains 175 Brazilian bat species that are threatened by extinction in some degree. From this perspective, it is essential to expand the knowledge about the genetic diversity of vulnerable bats. Genomic sequencing can be useful to generate robust and informative genetic references, increasing resolution when analyzing relationships among populations, species, or higher taxonomic levels. In this study, we sequenced and characterized in detail the first complete mitochondrial genomes of Furipterus horrens, Lonchorhina aurita, and Natalus macrourus, and investigated their phylogenetic position based on amino acid sequences of protein-coding genes (PCGs). The mitogenomes of these species are 16,516, 16,697, and 16,668 bp in length, respectively, and each comprises 13 PCGs, 22 tRNA genes, two rRNA genes, and a putative control region (CR). In the three species, genes were arranged similarly to all other previously described bat mitogenomes, and nucleotide composition was also consistent with the reported range. The length and arrangement of rrnS and rrnL were also consistent with those of other bat species, showing a positive AT-skew and a negative GC-skew. Except for trnS1, for which we did not observe the DHU arm, all other tRNAs showed the cloverleaf secondary structure in the three species. In addition, the mitogenomes showed minor differences in start and stop codons, and in all PCGs, codons ending in adenine were more common compared to those ending in guanine. We found that PCGs of the three species use multiple codons to encode each amino acid, following the previously documented pattern. Furthermore, all PCGs are under purifying selection, with atp8 experiencing the most relaxed purifying selection. Considering the phylogenetic reconstruction, F. horrens was recovered as sister to Noctilio leporinus, L. aurita and Tonatia bidens shared a node within Phyllostomidae, and N. macrourus appeared as sister to Molossidae and Vespertilionidae.

Fig 1. Circular genome depiction of the mitochondrial genomes of Furipterus horrens, Lonchorhina aurita, and Natalus macrourus, and their sampling locations in the Carajás National Forest, Pará, Brazil.

Colored arrows pointing to the left and right in the circular map of the mitogenomes represent the transcription regions of protein coding genes (blue), rRNA genes (red) and tRNA genes (purple) on the L and H strands, respectively. Furipterus horrens was collected in the cave S11D_0064, while both L. aurita and N. macrourus were collected in the cave S11D_0094.

Fig 2. Selective pressure analysis in the protein coding genes of Furipterus horrens, Lonchorhina aurita, and Natalus macrourus.

The Ka/Ks ratio variation is presented for each protein-coding gene.

Fig 3. Phylogenetic relationships among Chiroptera genera using mitogenome protein-coding genes.

Majority-rule consensus tree based on Bayesian inference evidencing the phylogenetic relationships among the mitogenomes of Furipterus horrens, Lonchorhina aurita, Natalus macrourus, and 54 other bat genera, with one species each, indicating their respective family affiliations and GenBank accession numbers. The circles on the nodes and triangles over the branches indicate the following posterior probabilities (PP) and bootstrap (BS) supports, respectively: black means PP = 1.00 and BS ≥ 90%; red is for PP between 0.95–0.99 and BS between 80–89%; and white is for PP between 0.90–0.94 and BS between 70–79%.