Sympatric speciation revealed by genome-wide divergence in the blind mole rat Spalax.
Sympatric speciation (SS), i.e., speciation within a freely breeding population or in contiguous populations, was first proposed by Darwin [Darwin C (1859) On the Origins of Species by Means of Natural Selection] and is still controversial despite theoretical support [Gavrilets S (2004) Fitness Landscapes and the Origin of Species (MPB-41)] and mounting empirical evidence. Speciation of subterranean mammals generally, including the genus Spalax, was considered hitherto allopatric, whereby new species arise primarily through geographic isolation. Here we show in Spalax a case of genome-wide divergence analysis in mammals, demonstrating that SS in continuous populations, with gene flow, encompasses multiple widespread genomic adaptive complexes, associated with the sharply divergent ecologies. The two abutting soil populations of S. galili in northern Israel habituate the ancestral Senonian chalk population and abutting derivative Plio-Pleistocene basalt population. Population divergence originated ∼0.2-0.4 Mya based on both nuclear and mitochondrial genome analyses. Population structure analysis displayed two distinctly divergent clusters of chalk and basalt populations. Natural selection has acted on 300+ genes across the genome, diverging Spalax chalk and basalt soil populations. Gene ontology enrichment analysis highlights strong but differential soil population adaptive complexes: in basalt, sensory perception, musculature, metabolism, and energetics, and in chalk, nutrition and neurogenetics are outstanding. Population differentiation of chemoreceptor genes suggests intersoil population's mate and habitat choice substantiating SS. Importantly, distinctions in protein degradation may also contribute to SS. Natural selection and natural genetic engineering [Shapiro JA (2011) Evolution: A View From the 21st Century] overrule gene flow, evolving divergent ecological adaptive complexes. Sharp ecological divergences abound in nature; therefore, SS appears to be an important mode of speciation as first envisaged by Darwin [Darwin C (1859) On the Origins of Species by Means of Natural Selection].
Department of Ecology, College of Life Sciences, Wuhan University, Wuhan 430072, China; Institute of Evolution, University of Haifa, Haifa 3498838, Israel;
Kexin
K
Li
Department of Ecology, College of Life Sciences, Wuhan University, Wuhan 430072, China;
Wei
W
Hong
Department of Ecology, College of Life Sciences, Wuhan University, Wuhan 430072, China;
Hengwu
H
Jiao
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China;
Guo-Dong
GD
Wang
Sam and Anne Barshop Center for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229; Department of Physiology, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229;
Karl A
KA
Rodriguez
Sam and Anne Barshop Center for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229; Department of Physiology, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229; Calico, South San Francisco, CA 94080.
Rochelle
R
Buffenstein
Institute of Evolution, University of Haifa, Haifa 3498838, Israel;
Yang
Y
Zhao
Institute of Evolution, University of Haifa, Haifa 3498838, Israel; nevo@research.haifa.ac.il huabinzhao@whu.edu.cn.
Eviatar
E
Nevo
Department of Ecology, College of Life Sciences, Wuhan University, Wuhan 430072, China; nevo@research.haifa.ac.il huabinzhao@whu.edu.cn.
Huabin
H
Zhao
D000818:Animals; D001499:Bayes Theorem; D063990:Gene Ontology; D049810:Genetic Speciation; D014644:Genetic Variation; D016678:Genome; D015810:Linkage Disequilibrium / Q000235:genetics; D008969:Molecular Sequence Data; D010802:Phylogeny; D020641:Polymorphism, Single Nucleotide / Q000235:genetics; D011157:Population Dynamics; D059748:Proteolysis; D018035:Receptors, Odorant / Q000235:genetics; D017422:Sequence Analysis, DNA; D046308:Spalax / Q000235:genetics*; D061350:Sympatry / Q000235:genetics*
D018035:Receptors, Odorant
ecological adaptation; genome divergence; natural selection; population genetics; sympatric speciation