Sympatric incipient speciation of spiny mice Acomys at "Evolution Canyon," Israel

Abstract

Does the paucity of empirical evidence of sympatric speciation in nature reflect reality, despite theoretical support? Or is it due to inappropriate searches in nature with overly restrictive assumptions and an incorrect null hypothesis? Spiny mice, Acomys, described here at Evolution Canyon (EC) incipiently and sympatrically speciate owing to microclimatic interslope divergence. The opposite slopes at EC vary dramatically, physically and biotically, representing the dry and hot south-facing slope savannoid-African continent ["African" slope (AS)], abutting with the north-facing slope forested south-European continent ["European" slope (ES)]. African-originated spiny mice, of the Acomys cahirinus complex, colonized Israel 30,000 y ago based on fossils. Genotypically, we showed significantly higher genetic diversity of mtDNA and amplified fragment length polymorphism of Acomys on the AS compared with the ES. This is also true regionally across Israel. In complete mtDNA, 25% of the haplotypes at EC were slope-biased. Phenotypically, the opposite slope's populations also showed adaptive morphology, physiology, and behavior divergence paralleling regional populations across Israel. Preliminary tests indicate slope-specific mate choices. Colonization of Acomys at the EC first occurred on the AS and then moved to the ES. Strong slope-specific natural selection (both positive and negative) overrules low interslope gene flow. Both habitat slope selection and mate choices suggest ongoing incipient sympatric speciation. We conclude that Acomys at the EC is ecologically and genetically adaptively, incipiently, sympatrically speciating on the ES owing to adaptive microclimatic natural selection.

Keywords: adaptation; ecological-speciation; microscale; rodents.

Fig. 1.

A maximum likelihood-phylogenetic tree of Acomys cahirinus from complete mtDNA sequences at EC. The bootstrap values are based on 1,000 cycles. A, AS samples collected from AS; E, ES samples collected from ES.

Fig. 2.

A maximum likelihood chronogram based on Cytb from different Acomys species. Deomys was used as an outgroup. The bootstrap values are based on 1,000 cycles. The bootstrap values equal zero or very small ones are showing some individuals from EC are genetically identical or very similar.

Fig. 3.

A minimum spanning network constructed by means of SplitsTree (54) from 17 Acomys cahirinus samples from EC.

Fig. 4.

A median joining network representing all complete mtDNA sequences in A. cahirinus at EC. Numerals describe position of polymorphic sites. Nucleotide position in red and green refers to the positive and negative selections, respectively. Ref refers to the ES abundant haplotype Y1 (Table S3 gives details).