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Transcriptome, Genetic Editing, and Microrna Divergence Substantiate Sympatric Speciation of Blind Mole Rat, Spalax

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Transcriptome, Genetic Editing, and Microrna Divergence Substantiate Sympatric Speciation of Blind Mole Rat, Spalax Transcriptome, genetic editing, and microRNA divergence substantiate sympatric speciation of blind mole rat, Spalax Kexin Lia,b,1,2, Liuyang Wangc,1, Binyamin A. Knisbacher1, Qinqin Xue,1, Erez Y. Levanond, Huihua Wanga, Milana Frenkel-Morgensternf, Satabdi Tagoref, Xiaodong Fangg, Lily Bazakd, Ilana Buchumenskid, Yang Zhaob, Matej Lövyh, Xiangfeng Lii, Lijuan Hang, Zeev Frenkelb, Avigdor Beilesb, Yi Bin Caoj,2, Zhen Long Wangk,2, and Eviatar Nevob,2 aInstitute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China; bInstitute of Evolution, University of Haifa, Haifa 3498838, Israel; cDepartment of Molecular Genetics and Microbiology, School of Medicine, Duke University, Durham, NC 27708; dThe Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel; eThe People’s Hospital of Qinghai Province, Xining 810007, China; fFaculty of Medicine, Bar-Ilan University, Safed 13195, Israel; gBeijing Genomics Institute, BGI-Shenzhen, Shenzhen 518083, China; hDepartment of Zoology, Faculty of Science, University of South Bohemia, 37005 Ceske Budejovice, Czech Republic; iUniversity of Chinese Academy of Sciences, Beijing 100049, China; jCollege of Chemistry and Life Science, Zhejiang Normal University, Jinhua, Zhejiang 321004, China; and kSchool of Life Sciences, Zhengzhou University, Zhengzhou 450001, Henan, China Contributed by Eviatar Nevo, May 18, 2016 (sent for review April 1, 2016; reviewed by Sergey Gavrilets and Morris Soller) Incipient sympatric speciation in blind mole rat, Spalax galili,in gene flow. The functions of selected genes adaptively met the di- Israel, caused by sharp ecological divergence of abutting chalk– vergent ecological stress very well, which suggests that natural se- basalt ecologies, has been proposed previously based on mito- lection overruled gene flow and drove ecological SS (5). Ecological chondrial and whole-genome nuclear DNA. Here, we present new speciation predicts that (i) population pairs from abutting divergent evidence, including transcriptome, DNA editing, microRNA, and ecologies have greater RI than those from similar but distant codon usage, substantiating earlier evidence for adaptive diver- ecologies (9, 10); (ii) adaptive divergence will limit genetic exchange gence in the abutting chalk and basalt populations. Genetic diver- between populations (11, 12), expediting RI evolution. Gene ex- gence, based on the previous and new evidence, is ongoing pression, both down- or up-regulation, and alternative splicing, play despite restricted gene flow between the two populations. The an important role in shaping the phenotype of organisms colonizing principal component analysis, neighbor-joining tree, and genetic a new environment (13). Consequently, it will enhance the adaptive structure analysis of the transcriptome clearly show the clustered spectrum, affecting genetic traits promoting RI. divergent two mole rat populations. Gene-expression level analy- DNA and RNA editing have the potential to accelerate sis indicates that the population transcriptome divergence is dis- genome evolution (14). DNA editing by apolipoprotein B mRNA- played not only by soil divergence but also by sex. Gene ontology editing enzymes, catalytic polypeptide-like (APOBECs), func- enrichment of the differentially expressed genes from the two abut- tions in various biological pathways in health and disease. In ting soil populations highlights reproductive isolation. Alternative genome defense, it restricts retroelements by introducing dele- splicing variation of the two abutting soil populations displays two terious hypermutation into the retroelement DNA synthesized distinct splicing patterns. L-shaped FST distribution indicates that the two populations have undergone divergence with gene flow. Tran- scriptome divergent genes highlight neurogenetics and nutrition Significance characterizing the chalk population, and energetics, metabolism, musculature, and sensory perception characterizing the abutting Speciation is the basis of the origin of biodiversity in nature. basalt population. Remarkably, microRNAs also display divergence Sympatric speciation (SS) is still a controversial model of the origin between the two populations. The GC content is significantly higher of new species, since first proposed by Darwin in 1859. Here, we in chalk than in basalt, and stress-response genes mostly prefer complement earlier genomic evidence with new analyses of tran- nonoptimal codons. The multiple lines of evidence of ecological– scriptome profiling, DNA editing, and microRNA, examined in the genomic and genetic divergence highlight that natural selection blind subterranean rodent, Spalax galili, in the Galilee Mountains, overrules the gene flow between the two abutting populations, Israel, all substantiating SS with gene flow. Gene ontology en- substantiating the sharp ecological chalk–basalt divergence driving richment of differentially expressed genes, in the abutting soil sympatric speciation. populations, highlights evolving reproductive isolation, despite a few interpopulation recombinants. Because sharply divergent natural selection | ecological adaptive speciation | DNA editing | geological, edaphic, climatic, and biotic interfaces abound in na- microRNA regulation | nonoptimal codon usage ture, we conclude that SS may be a common model of the origin of new species, as envisaged by Darwin. ympatric speciation (SS)—that is, speciation in a free breeding — Author contributions: E.N. designed research; K.L., E.Y.L., and E.N. performed research; Spopulation has been proposed by Darwin (1) but refuted by K.L., A.B., and Z.L.W. contributed new reagents/analytic tools; K.L., L.W., B.A.K., Q.X., Ernst Mayr, who accepted it later in life (2, 3). Four criteria are H.W., M.F.-M., S.T., X.F., L.B., I.B., Y.Z., M.L., X.L., L.H., Z.F., Y.B.C., and E.N. analyzed data; required for establishing SS: sympatry, reproductive isolation (RI), and K.L., L.W., B.A.K., M.F.-M., and E.N. wrote the paper. sister species, and no historical allopatry (4). However, whether all Reviewers: S.G., University of Tennessee; and M.S., Hebrew University of Jerusalem. these criteria could be detected in all of the emergent SS cases is The authors declare no conflict of interest. still unclear. Rising empirical (5) (SI Appendix, Suggested Reading) Data deposition: The sequences reported in this paper have been deposited in the Gen- Bank database (accession nos. SRP075890 and SRP075930). and theoretical studies (6, 7) demonstrated that SS may be common 1K.L., L.W., B.A.K., and Q.X. contributed equally to this work. in nature, although it is still being highly debated (4). Recently, we 2To whom correspondence may be addressed. Email: [email protected], demonstrated SS in the blind mole rat, Spalax galili,bybothmito- [email protected], [email protected], or [email protected]. chondrial genome (8) and by whole-genome resequencing (5), This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. demonstrating divergence across the whole genome with ongoing 1073/pnas.1607497113/-/DCSupplemental. 7584–7589 | PNAS | July 5, 2016 | vol. 113 | no. 27 www.pnas.org/cgi/doi/10.1073/pnas.1607497113 Downloaded by guest on September 30, 2021 during reverse transcription (among other mechanisms). In some transcriptome (Kolmogorow–Smirnov test, P = 0.002215), and cases, DNA-edited elements successfully enter the genome despite both of them appear as “L-shaped” (SI Appendix, Fig. S5). being hypermutated, containing a series of G-to-A mutations (15, The allele number of SNPs, which is defined as the total 16). These sequences enhance genomic diversity and, therefore, number of alleles in all individuals studied for that SNP at that increase the potential of developing new traits. A-to-I RNA site, was 1.60 and 1.58 in chalk and abutting basalt populations, editing by adenosine deaminases acting on RNAs (ADARs) respectively. It is significantly more in chalk than in basalt (P < enhances diversity through a different mechanism—it confers 0.00001). The heterozygosity of chalk and basalt populations are plasticity to the transcriptome by enabling a single mRNA iso- 0.1660 ± 0.2260 and 0.1454 ± 0.2220, respectively, and it is sig- form to give rise to a multitude of protein variants (17). nificantly more in the chalk population than in basalt (P < 2.2e-16, Here, we show SS in S. galili in upper Galilee, Israel, by tran- Wilcoxon test). scriptome divergence, DNA editing, microRNA regulation, and codon usage associated with the abutting but sharply divergent ecological Gene Expression Divergence Between the Two Mole Rat Soil Populations. environments, basalt and chalk, in the central eastern upper Galilee, A hierarchical cluster analysis was conducted based on the expres- Israel, complementing and reinforcing the genome divergence (5), sion level of 89,860 transcripts to estimate the contribution of sex thereby advancing our in-depth understanding of SS with gene flow. and environments to gene expression. Principal variance component analysis was also performed to estimate the expression divergence Results between the two soil populations (Fig. 1A). The first and second Transcriptome Sequencing and Population Divergence Analyses. The principal components (PCs) explain 55% and 17% expression var- subterranean blind mole rats, S. galili (SI Appendix, Table S1), iance, respectively. The largest PC1 separates the 10 animals by the were collected from the two abutting but sharply divergent
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