Sympatric speciation revealed by genome-wide divergence in the blind mole rat Spalax

Abstract

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].

Keywords: ecological adaptation; genome divergence; natural selection; population genetics; sympatric speciation.

Fig. 1.

Study subject, ecological, and genomic divergence in sympatric speciation. (A) The blind mole rat, S. galili. (B) Vegetation formation exposed with mounds in basalt and covered by dense bushes of Sarcoptherium spinosum in chalk. (C) Geological map. Chalk is in yellow and basalt is in pink, separated by a geological fault. (D) NJ tree based on all of the SNPs. Red, basalt individuals; black, chalk individuals. (E) PCA of two Spalax soil populations. Red triangles, basalt individuals; black circles, chalk individuals. (F) Population genetic structure of two Spalax soil populations when K = 2, 3, and 4.

Fig. S1.

Unique and shared SNPs between the chalk and basalt mole rat populations shown by Venn diagram.

Fig. 2.

LD and demographic structure. (A) LD decay of two continuous S. galili populations. x axis stands for physical distances (bp), whereas y axis stands for r². (B) Inferred demographic history for the two abutting soil populations (chalk vs. basalt) of S. galili. The extant and ancestral population sizes (Ne) of the chalk and basalt populations are indicated, and the migration rates between the two populations are provided. The divergence time (T) between two populations was inferred.

Fig. 3.

GO enrichment analysis of putatively selected genes in chalk and basalt S. galili populations. Gene number is provided next to each GO term.

Fig. S2.

Olfactory receptor genes analyses. Neighbor-joining phylogenetic tree of all 1,042 intact and complete olfactory receptor (OR) genes identified from the reference genome of S. galili. Red branches denote the 22 olfactory receptor genes surveyed in 29 blind mole rats from basalt and chalk populations. Nomenclature of the 22 OR genes was arbitrary.

Fig. S3.

Bayesian phylogenetic tree of 32 S. galili and 35 mouse Tas2r genes that are complete and intact. The numbers at the nodes are the Bayesian posterior probabilities shown as percentages. Blue branches indicate the 32 Tas2r genes from S. galili, whereas the remaining genes are from the mouse. Blue branches denote the 20 Tas2r genes surveyed in 29 individuals of S. galili from basalt and chalk populations. Nomenclature of the 20 Tas2r genes was arbitrary.

Fig. 4.

Differences in the proteolytic machinery of Spalax galili basalt and chalk populations. (A) 20S proteasome activity measured by degradation of optimized peptides cleaved by the three active sites, chymotrypsin-like (ChTL), trypsin-like (TL), and postglutamyl, peptide hydrolyzing (PGPH) or caspase-like, show higher levels of activity in the basalt population. (B) Higher levels of the constitutive 20S proteasome subunit α7 support the observation of the increase in activity in basalt population. (C) The chalk population protein degradation profile suggests more of a reliance on autophagy, with significantly higher levels of ATG7 and autophagic flux (LC3II/LC3I ratio).