Genome-wide analysis revisits incipient sympatric and allopatric speciation in a beetle

Abstract

The grain beetle, Oryzaephilus surinamensis, is a widespread species distributed in the wild and in granaries. Our earlier extensive biological studies indicated that the beetle shows incipient sympatric speciation (SS) in the wild at Evolution Canyon I (EC-I), Israel, and allopatric speciation, in a granary. Here we provide genome-wide evidence supporting our adaptive evolution scenario involving two models of speciation, SS in the wild, and allopatric in the granary. The EC-I microsite is a hot spot of SS across life from bacteria to mammals caused by the sharp opposite microclimates. The tropical hot, dry and savannoid biome dubbed the “African” slope (AS), sharply contrasts with the opposite temperate, cool, humid, and forested biome on the European” slope (ES), separated by only ~250 meters. The third allopatric granary population is 26 km north of EC-I. The granary population showed larger genomic, morphological, and behavioral distances, smaller genome size, more unique transposable elements, and reproductive isolation, displaying faster genomic divergence than between the wild populations at EC-I. The incipient SS of the wild populations, and the speciation of the granary population are reinforced by the substantial genomic divergence among the three beetle populations, supporting again the evolutionary scenario of incipient SS with gene flow at EC-I, and allopatric speciation in the granary population. We propose additional studies in Israel, the Mediterranean basin, and worldwide, to negate alternative explanations, based on a broader sampling and analysis.