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Genome Evolution of Blind Subterranean Mole Rats: Adaptive Peripatric Versus Sympatric Speciation

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Genome Evolution of Blind Subterranean Mole Rats: Adaptive Peripatric Versus Sympatric Speciation Genome evolution of blind subterranean mole rats: Adaptive peripatric versus sympatric speciation Kexin Lia,b,1,2, Shangzhe Zhanga,1, Xiaoying Songc,1, Alexandra Weyrichd,1, Yinjia Wanga, Xi Liua, Na Wana, Jianquan Liua, Matej Lövye, Haihong Cuif, Vladimir Frenkelb, Avi Titievskyg, Julia Panovg,h, Leonid Brodskyg, and Eviatar Nevob,2 aState Key Laboratory of Grassland Agro-Ecosystem, Institute of Innovation Ecology, Lanzhou University, 730000 Lanzhou, China; bInstitute of Evolution, University of Haifa, 3498838 Haifa, Israel; cSchool of Public Health, Lanzhou University, Lanzhou, 730000, China; dLeibniz Institute for Zoo and Wildlife Research, 10315 Berlin, Germany; eFaculty of Science, University of South Bohemia, 370 05 Ceské Budejovice, Czech Republic; fDepartment of Gastroenterology, The 305 Hospital of PLA, 100017 Beijing, China; gTauber Bioinformatics Research Center, Haifa 3498838, Israel; and hSagol Department of Neurobiology, University of Haifa, Haifa 3498838, Israel Contributed by Eviatar Nevo, October 8, 2020 (sent for review September 8, 2020; reviewed by Sergey Gavrilets and Eugene V. Koonin) Speciation mechanisms remain controversial. Two speciation models galili (2n = 52) is distributed in the humid, cool Upper Galilee and occur in Israeli subterranean mole rats, genus Spalax: a regional spe- underwent further sympatric speciation (i.e., speciation in the same ciation cline southward of four peripatric climatic chromosomal species homeland [patria]), with ongoing gene flow between the abutting and a local, geologic-edaphic, genic, and sympatric speciation. Here populations evolving into two different species due to geologic- we highlight their genome evolution. The five species were sepa- edaphic (soil) divergence from S. galili ancestor species on Seno- rated into five genetic clusters by single nucleotide polymorphisms, nian (Upper Cretaceous) chalk rocks to S. galili,thederivative copy number variations (CNVs), repeatome, and methylome in sym- species evolving on Pleistocene volcanic basalt (7–9) (Fig. 1B). S. patry. The regional interspecific divergence correspond to Pleistocene golani (2n = 54) inhabits the semihumid, cold northern Golan and climatic cycles. Climate warmings caused chromosomal speciation. Mount Hermon region (Fig. 1C). Spalax carmeli (2n = 58) ranges Triple effective population size, Ne, declines match glacial cold cycles. Adaptive genes evolved under positive selection to underground from the warm southern Golan to the humid and warm lower stresses and to divergent climates, involving interspecies reproduc- Galilee, Mount Carmel, and Coastal Plain and down to the Yarkon = tive isolation. Genomic islands evolved mainly due to adaptive evo- River (10) (Fig. 1C). Spalax judaei (2n 60) occurs in the warm, dry EVOLUTION lution involving ancient polymorphisms. Repeatome, including both southern Samaria and Judea Mountains, southern coastal plain, CNV and LINE1 repetitive elements, separated the five species. Meth- and northern Negev Desert (10) (Fig. 1C). Thus, the four chro- ylation in sympatry identified geologically chalk-basalt species that mosomal sibling species (2n = 52, 54, 58, 60) are distributed in four differentially affect thermoregulation, hypoxia, DNA repair, P53, and climatic regions based on a combination of temperature and other pathways. Genome adaptive evolution highlights climatic and humidity (10–12). In contrast, the sole sympatric species occurs geologic-edaphic stress evolution and the two speciation models, locally in the same macroclimate but is divergent geologically peripatric and sympatric. Significance subterranean rodents | genomic sequencing | speciation models | methylation | repeatome We substantiate genomically, repeatomically, and epigenomi- cally the origin, demography, and timing of two divergent he remarkable ecological adaptation of mammals to the speciation models in the Israeli five blind subterranean species Tunderground environment due to climatic change in Eocene of Spalax ehrenbergi superspecies. Four species demonstrate a times, approximately 50 million years ago (Mya), is one of na- regional, chromosomal, peripatric, climatic aridity speciation ’ ture s best-studied long-term evolutionary adaptive experiments. model trending southward from the northern cold and humid It involves mosaic evolution of regression, progression, and Golan and Upper Galilee to the hot, dry Negev Desert. The fifth global convergent adaptations to their common, unique subter- species shows a local, genic, geologic-edaphic, and sympatric ranean ecology (1). The genus Spalax (Spalacidae, Rodentia; speciation model demonstrating primary sympatric speciation Fig. 1A), originated in Asia Minor and displays an outstanding in subterranean mammals. The five species are differentiated three-pronged adaptive climatic radiation into the Balkans, at multiple genomic levels and demonstrate different ecologi- Ukraine, and Near East southward to North Africa, reflected in cal mechanisms of speciation in the superspecies. Sympatric an increasing diploid set of chromosome numbers, from 2n = 36 speciation may be common in nature. Numerous ecologically in Asia Minor to 2n = 62 associated with high ecological stresses divergent microsites—geologic, edaphic, climatic, abiotic, in all three prongs (1). The divergence of chromosomes resulted biotic—abound globally, where selection overrules gene flow from Robertsonian chromosomal fission mutations (2, 3) and led homogenization. to a southward ecological chromosomal speciation cline of the Spalax ehrenbergi superspecies in Israel. Ecogeographically, Spalax Author contributions: K.L. and E.N. designed research; K.L., X.S., N.W., M.L., and H.C. performed research; S.Z. contributed new reagents/analytic tools; K.L., A.W., Y.W., X.L., chromosome sets are increasing southward toward the Negev V.F., A.T., J.P., and L.B. analyzed data; and K.L., A.W., J.L., J.P., and E.N. wrote the paper. Desert. They are associated with extreme changes in ecological Reviewers: S.G., University of Tennessee at Knoxville; and E.V.K., National Institutes factors (1), especially the climate of Israel from the northern of Health. humid, cold Galilee and Golan region southward to the hot, dry The authors declare no competing interest. Negev Desert, representing an ecology of increasing climatic Published under the PNAS license. aridity southward (SI Appendix, Table S1) (4). 1K.L., S.Z., X.S., and A.W. contributed equally to this work. Notably, Spalax has largely been known to speciate chromosomally 2To whom correspondence may be addressed. Email: [email protected] or nevo@ (5), adaptively, allopatrically (i.e., separated distantly geographically research.haifa.ac.il. without ongoing gene flow), or peripatrically (i.e., isolated relatively This article contains supporting information online at https://www.pnas.org/lookup/suppl/ closely in peripheral populations surrounding the main range but doi:10.1073/pnas.2018123117/-/DCSupplemental. without ongoing gene flow) (6), a kind of close allopatry. Spalax First published December 4, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2018123117 PNAS | December 22, 2020 | vol. 117 | no. 51 | 32499–32508 Downloaded by guest on September 30, 2021 A C S.galili (2n=52) D S. golani (2n=54) Golan-2A G G G Golan-1 olan olan G G olan- olan- basalt chalk olan- G S. galili-chalk (2n=52) olan - - 3A 9A 7A 8 4 - EC-4B A A (2n=54) B 6 A EC-8A EC-1A F EC-6A EC-2A EC-5B EC-10A Sheva-11A Sheva-6A SCN- Sheva-8A Sheva-12A S CN- 1 Sheva-4A S A S h 2 Sheva-5A e CN S.carmelii A She e - Sheva-1A k v 4A a S S.golani S CN-5 Sheva-2A al e al v -9 heva- a- Divergence of SNPs of noncoding areas (2n=58) A A Sheva-3A 3 Divergence of SNPs within genes Shev 2A A SCN-6 Sheva-9A e a A Golan-8B lil - 0.02 1 S CN- Golan-2A (2n=60)S A 7A heva- Golan-1A aG 5 Sheva- A SCN-8 Golan-9A 4A A Golan-3A Sheva-12A Golan-7A SBN- Golan-4A S heva- 8 A 8 S A Golan-6A S .galili-basalt (2n=52) B .galili-basalt S S heva-6 N-1A S SCN-1A A BN- SCN-2A Shev S B 5A SCN-4A Mediterranean Sea a-11 S N-7 S. judaei S BN SCN-5A A S B A SBN-1 SCN-6A S B N -3 B - SCN-7A N-11 6A A N- SCN-8A 4A SBN-8A 2 A SBN-1A A E C-1 SBN-5A E C- SBN-7A 0 E A 5B C SBN-3A EC-6 - E 2 SBN-6A A S.judaei C-1 SBN-11A (2n=58) E EC A SBN-12A C A - SBN-4A -8 4 B (2n=60) A 5.0 5.0 E carmeli S. S.galili-Basalt G 0.15 K=5 0.1 S.galili-Chalk B Dead Sea 0.05 S. judaei 0 K=4 S.carmeli -0.05 -0.1 K=3 -0.15 -0.2 K=2 Principal component 2 (9.03%) -0.25 S. golani -0.3 -0.2 -0.15 -0.1 -0.05 0 0.05 0.1 0.15 Red Sea S.galili Basalt S.galili Chalk Principal component 1 (26.95%) .carmeli S.golani S. judaei S Fig. 1. The ecogeographic distribution and the genomic divergence among Spalax species in Israel. (A) Blind mole rat, Spalax.(B) Geological map of east Upper Galilee including the Evolution plateau. (C) Ecogeographic map of species distribution (from north to south marked in different colors) and sampling sites (red dots) of the four climatic and chromosomal peripatric species, and the fifth S. galili (2n = 52) marked in green, which diverged edaphically and genetically from sympatric species derivative S. galili_basalt) (2n = 52) marked with a red circle and its ancestor S. galili_chalk (2n = 52) marked with a blue circle, S. golani (2n = 54) marked in blue, S. carmeli (2n = 58) marked in violet, and S. judaei (2n = 60) marked in brown. (D) A neighbor-joining tree reconstructed with the allele shared matrix of SNPs of the five blind mole rat species populations. The scale bar represents the p distance. (E) Genetic clusters of the four species shown by PCA based on SNPs; only principal component 1 (26.95%) and principal component 2 (9.03%) are displayed.
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