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. 2024 May 31:12:e17482.
doi: 10.7717/peerj.17482. eCollection 2024.

A genomic hotspot of diversifying selection and structural change in the hoary bat (Lasiurus cinereus)

Robert S Cornman  1
Affiliations

A genomic hotspot of diversifying selection and structural change in the hoary bat (Lasiurus cinereus)

Robert S Cornman. PeerJ. .

Abstract

Background: Previous work found that numerous genes positively selected within the hoary bat (Lasiurus cinereus) lineage are physically clustered in regions of conserved synteny. Here I further validate and expand on those finding utilizing an updated L. cinereus genome assembly and additional bat species as well as other tetrapod outgroups.

Methods: A chromosome-level assembly was generated by chromatin-contact mapping and made available by DNAZoo (www.dnazoo.org). The genomic organization of orthologous genes was extracted from annotation data for multiple additional bat species as well as other tetrapod clades for which chromosome-level assemblies were available from the National Center for Biotechnology Information (NCBI). Tests of branch-specific positive selection were performed for L. cinereus using PAML as well as with the HyPhy package for comparison.

Results: Twelve genes exhibiting significant diversifying selection in the L. cinereus lineage were clustered within a 12-Mb genomic window; one of these (Trpc4) also exhibited diversifying selection in bats generally. Ten of the 12 genes are landmarks of two distinct blocks of ancient synteny that are not linked in other tetrapod clades. Bats are further distinguished by frequent structural rearrangements within these synteny blocks, which are rarely observed in other Tetrapoda. Patterns of gene order and orientation among bat taxa are incompatible with phylogeny as presently understood, implying parallel evolution or subsequent reversals. Inferences of positive selection were found to be robust to alternative phylogenetic topologies as well as a strong shift in background nucleotide composition in some taxa.

Discussion: This study confirms and further localizes a genomic hotspot of protein-coding divergence in the hoary bat, one that also exhibits an increased tempo of structural change in bats compared with other mammals. Most genes in the two synteny blocks have elevated expression in brain tissue in humans and model organisms, and genetic studies implicate the selected genes in cranial and neurological development, among other functions.

Keywords: Adaptation; Comparative genomics; Evolutionary rate analysis; Hoary bat.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. A pronounced cluster of positively selected genes occurs in the chromosome-level assembly of hoary bat (Lasiurus cinereus).
The genomic region containing the cluster of selection candidates is labeled “NF-CE block”, see text for details. (A) Cumulative proportion of all single-copy orthologs tested for positive selection in a previous study (see text for details) compared with the cumulative proportion of genes with significant test results. (B) Histogram of the number of positive selection candidates in windows of comparable size to the 12-Mb region identified in panel A. The observed value for the NF-CE block is ten.
Figure 2
Figure 2. Demarcation of the cat-eye (CE) synteny block based on the gene order in human.
Each row is a genomic data track derived from the University of California Santa Cruz (UCSC) Genome Browser, with the approximate location in the human genome indicated in the upper left. The top track shows ideograms of the human RefSeq genes curated by the National Center for Biotechnology Information (NCBI), indicating exon structure and orientation, labeled with the gene symbols used in the text. Asterisks indicate genes with evidence of positive selection within the Lasiurus cinereus branch of the tested phylogeny. The subsequent tracks identify blocks of conserved sequence in representative Tetrapoda of increasing evolutionary distance to human. Within each species, alignments on the same chromosome share a common color and are linked by flow lines if contiguous. Regions that are approximately uniform in color and contiguous within each species are syntenic. See Methods for data track sources.
Figure 3
Figure 3. Demarcation of the NF synteny block based on gene order in human.
Each row is a genomic data track derived from the University of California Santa Cruz (UCSC) Genome Browser, with the approximate location in the human genome indicated in the upper left. The top track shows ideograms of human genes curated by the Gencode consortium, indicating exon-intron structure and orientation, labeled with the gene symbols used in the text. Asterisks indicate genes with evidence of positive selection within the Lasiurus cinereus branch of the tested phylogeny. The subsequent tracks identify blocks of conserved sequence in representative Tetrapoda of increasing evolutionary distance to human. Within each species, alignments on the same chromosome share a common color and are linked by flow lines if contiguous. Regions that are approximately uniform in color and contiguous within each species are syntenic. Not the human gene Ccdc169, which lies between Sohlh2 and Spart, is not conserved across mammals and therefore not labeled here. See Methods for data track sources.
Figure 4
Figure 4. Alignment of predicted protein sequences of the Trpc4 gene in representative Carnivora and Chiroptera.
The gray-shaded C-terminal region corresponds to the inositol triphosphate receptor (ITPR) binding region annotated in the human protein and discussed in the text. Residues that are unchanged from the first sequence in the alignment are represented by a dot to better highlight variable positions. Dashes indicate missing sequence. The alignment wraps to each row of the figure, position numbers are not shown for clarity.
Figure 5
Figure 5. Relative positions in tetrapod genomes of synteny blocks and individual genes analyzed in this study.
Each species diagram consists of one gene per row, represented by the human gene symbol for the orthologous group. A plus or minus sign indicates the orientation of the gene on the reference sequence. Gaps between gene blocks indicate they are on different linkage groups. A double line between genes on the same linkage group indicates a gap greater than 10 Mb. The Nbea-Foxo1 (NF) synteny block is colored green and the cat-eye (CE) synteny block is colored orange (see text for definitions of these blocks). Within each block, genes are numbered according to their order in the human genome as a reference. The genes Sacs, Fgf9, and Amer3 are not numbered because they are not considered part of either synteny block; rather, they are shown because they were identified as positive selection candidates closely linked to the two synteny blocks in Lasiurus cinereus. These three genes are colored blue, purple, and brown, respectively. Gene symbols are in unitalicized upper case for legibility. Genes that are unannotated and presumed absent in a species are grayed.
Figure 6
Figure 6. Relative positions in twelve tetrapod genomes of synteny blocks and individual genes analyzed in this study.
Each species diagram consists of one gene per row, represented by the human gene symbol for the orthologous group. A plus or minus sign indicates the orientation of the gene on the reference sequence. Gaps between genes indicate they are on different linkage groups. A double line between genes on the same linkage group indicates a physical distance greater than 10 Mb. The Nbea-Foxo1 (NF) synteny block is colored green and the cat-eye (CE) synteny block is colored orange (see text for definitions of these blocks). Within each block, genes are numbered according to their order in the human genome as a reference. The genes Sacs, Fgf9 and Amer3 are not numbered because they are not considered part of either synteny block; rather, they are shown because they were identified as positive selection candidates closely linked to the two synteny blocks in Lasiurus cinereus. These three genes are colored blue, purple, and brown, respectively. Gene symbols are in unitalicized upper case for legibility. Genes that are unannotated and presumed absent in a species are grayed. Species are grouped by phylogenetic position using the same color scheme as in Fig. 7. The asterisk denotes uncertainty as to whether the gene Bid is functional in L. cinereus.
Figure 7
Figure 7. Hypothesized sequence of structural changes in gene organization in bats.
Taxa for which chromosome-scale assemblies were available for this analysis are marked by colored boxes, which correspond to the colors used in Fig. 6. Grayed taxa were not analyzed for synteny because the relevant genes were not on large linkage groups. Genes are identified by their gene symbols, whereas NF and CE denote synteny blocks described in the text. GC denotes G + C content of gene coding sequences.
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References

    1. Agnarsson I, Zambrana-Torrelio CM, Flores-Saldana NP, May-Collado LJ. A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia) PLOS Currents Tree of Life. 2011;3:RRN1212. - PMC - PubMed
    1. Aguileta G, Refregier G, Yockteng R, Fournier E, Giraud T. Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infection, Genetics and Evolution. 2009;9(4):656–670. doi: 10.1016/j.meegid.2009.03.010. - DOI - PubMed
    1. Amador LI, Moyers Arevalo RL, Almeida FC, Catalano SA, Giannini NP. Bat systematics in the light of unconstrained analyses of a comprehensive molecular supermatrix. Journal of Mammalian Evolution. 2018;25(1):37–70. doi: 10.1007/s10914-016-9363-8. - DOI
    1. Anisimova M, Nielsen R, Yang Z. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics. 2003;164(3):1229–1236. doi: 10.1093/genetics/164.3.1229. - DOI - PMC - PubMed
    1. Arbour J, Curtis A, Santana S. Sensory adaptations reshaped intrinsic factors underlying morphological diversification in bats. BMC Biology. 2021;19(1):1–13. doi: 10.1186/s12915-021-01022-3. - DOI - PMC - PubMed

Grants and funding

The author received no external funding for this work. The work was supported by internal funds of the U.S. Geological Survey. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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