Possible incipient sympatric ecological speciation in blind mole rats (Spalax)

Abstract

Sympatric speciation has been controversial since it was first proposed as a mode of speciation. Subterranean blind mole rats (Spalacidae) are considered to speciate allopatrically or peripatrically. Here, we report a possible incipient sympatric adaptive ecological speciation in Spalax galili (2n = 52). The study microsite (0.04 km(2)) is sharply subdivided geologically, edaphically, and ecologically into abutting barrier-free ecologies divergent in rock, soil, and vegetation types. The Pleistocene Alma basalt abuts the Cretaceous Senonian Kerem Ben Zimra chalk. Only 28% of 112 plant species were shared between the soils. We examined mitochondrial DNA in the control region and ATP6 in 28 mole rats from basalt and in 14 from chalk habitats. We also sequenced the complete mtDNA (16,423 bp) of four animals, two from each soil type. Remarkably, the frequency of all major haplotype clusters (HC) was highly soil-biased. HCI and HCII are chalk biased. HC-III was abundant in basalt (36%) but absent in chalk; HC-IV was prevalent in basalt (46.5%) but was low (20%) in chalk. Up to 40% of the mtDNA diversity was edaphically dependent, suggesting constrained gene flow. We identified a homologous recombinant mtDNA in the basalt/chalk studied area. Phenotypically significant divergences differentiate the two populations, inhabiting different soils, in adaptive oxygen consumption and in the amount of outside-nest activity. This identification of a possible incipient sympatric adaptive ecological speciation caused by natural selection indirectly refutes the allopatric alternative. Sympatric ecological speciation may be more prevalent in nature because of abundant and sharply abutting divergent ecologies.

Fig. 1.

Geological map of the studied Dalton region in the Upper East Galilee, Israel. S. galili sampling sites, soil type, and number of captured animals are indicated. Colors indicate bedrock type: yellow, chalk; pink, basalt. A bold black line indicates a geological fault. The length of square edge in the map represents 1,000 meters. The image is based on Levitte (54). The smaller map in the upper-left shows the geology of Northern Israel. Note the sharp border between the adjacent examined populations of chalk and basalt.

Fig. 2.

Picture of the site and pie graphs of the schematic phylogenetic relations of HC and their frequencies in basalt or chalk at the microsite. The background shows the sharp divergence of vegetation between chalk and basalt area. See Fig. 1 for geological map of the region and Fig. S1 for the schematic phylogenetic relations between HC. Please note that the pie graphs are not scaled to difference in the sample sizes.

Fig. 3.

(A) Daily activity patterns of mole rats in basalt and chalk habitats. Data are shown as means ± SD. (B) Oxygen consumption is significantly higher in mole rats from the basalt region (black circles) than in mole rats from the chalk region (red squares).