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

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.

Genomic divergence and adaptive convergence in Drosophila simulans from Evolution Canyon, Israel

Biodiversity refugia formed by unique features of the Mediterranean arid landscape, such as the dramatic ecological contrast of “Evolution Canyon,” provide a natural laboratory in which local adaptations to divergent microclimate conditions can be investigated. Significant insights have been provided by studies of Drosophila melanogaster diversifying along the thermal gradient in Evolution Canyon, but a comparative framework to survey adaptive convergence across sister species at the site has been lacking. To fill this void, we present an analysis of genomic polymorphism and evolutionary divergence of Drosophila simulans, a close relative of Drosophila melanogaster with which it co-occurs on both slopes of the canyon. Our results show even deeper interslope divergence in D. simulans than in D. melanogaster, with extensive signatures of selective sweeps present in flies from both slopes but enhanced in the population from the hotter and drier south-facing slope. Interslope divergence was enriched for genes related to electrochemical balance and transmembrane transport, likely in response to increased selection for dehydration resistance on the hotter slope. Both species shared genomic regions that underwent major selective sweeps, but the overall level of adaptive convergence was low, demonstrating no shortage of alternative genomic solutions to cope with the challenges of the microclimate contrast. Mobile elements were a major source of genetic polymorphism and divergence, affecting all parts of the genome, including coding sequences of mating behavior-related genes.

Sympatric speciation of spiny mice, Acomys, unfolded transcriptomically at Evolution Canyon, Israel

Spiny mice, Acomys cahirinus, colonized Israel 30,000 y ago from dry tropical Africa and inhabited rocky habitats across Israel. Earlier, we had shown by mtDNA that A. cahirinus incipiently sympatrically speciates at Evolution Canyon I (EC I) in Mount Carmel, Israel because of microclimatic interslope divergence. The EC I microsite consists of a dry and hot savannoid “African” slope (AS) and an abutting humid and cool-forested “European” slope (ES). Here, we substantiate incipient SS in A. cahirinus at EC I based on the entire transcriptome, showing that multiple slope-specific adaptive complexes across the transcriptome result in two divergent clusters. Tajima’s D distribution of the abutting Acomys interslope populations shows that the ES population is under stronger positive selection, whereas the AS population is under balancing selection, harboring higher genetic polymorphisms. Considerable sites of the two populations were differentiated with a coefficient of FST = 0.25–0.75. Remarkably, 24 and 37 putatively adaptively selected genes were detected in the AS and ES populations, respectively. The AS genes involved DNA repair, growth arrest, neural cell differentiation, and heat-shock proteins adapting to the local AS stresses of high solar radiation, drought, and high temperature. In contrast, the ES genes involved high ATP associated with energetics stress. The sharp ecological interslope divergence led to strong slope-specific selection overruling the interslope gene flow. Earlier tests suggested slope-specific mate choice. Habitat interslope-adaptive selection across the transcriptome and mate choice substantiate sympatric speciation (SS), suggesting its prevalence at EC I and commonality in nature.