Abstract
As one of the hotspot regions for sympatric speciation studies, Evolution Canyon (EC) became an ideal place for its high level of microclimatic divergence interslopes. In this study, to highlight the genetic mechanisms of sympatric speciation, phenotypic variation on flowering time and transcriptomic divergence were investigated between two ecotypes of Ricotia lunaria, which inhabit the opposite temperate and tropical slopes of EC I (Lower Nahal Oren, Mount Carmel, Israel) separated by 100 m at the bottom of the slopes. Growth chamber results showed that flowering time of the ecotype from south-facing slope population # 3 (SFS 3) was significantly 3 months ahead of the north-facing slope population # 5 (NFS 5). At the same floral development stage, transcriptome analysis showed that 1,064 unigenes were differentially expressed between the two ecotypes, which enriched in the four main pathways involved in abiotic and/or biotic stresses responses, including flavonoid biosynthesis, α-linolenic acid metabolism, plant–pathogen interaction and linoleic acid metabolism. Furthermore, based on Ka/Ks analysis, nine genes were suggested to be involved in the ecological divergence between the two ecotypes, whose homologs functioned in RNA editing, ABA signaling, photoprotective response, chloroplasts protein-conducting channel, and carbohydrate metabolism in Arabidopsis thaliana. Among them, four genes, namely, SPDS1, FCLY, Tic21 and BGLU25, also showed adaptive divergence between R. lunaria and A. thaliana, suggesting that these genes could play an important role in plant speciation, at least in Brassicaceae. Based on results of both the phenotype of flowering time and comparative transcriptome, we hypothesize that, after long-time local adaptations to their interslope microclimatic environments, the molecular functions of these nine genes could have been diverged between the two ecotypes. They might differentially regulate the expression of the downstream genes and pathways that are involved in the interslope abiotic stresses, which could further diverge the flowering time between the two ecotypes, and finally induce the reproductive isolation establishment by natural selection overruling interslope gene flow, promoting sympatric speciation.
Highlights
Sympatric speciation, first proposed by Darwin as speciation occurring in contiguous populations with ongoing gene flow, was considered as one of the important models of biodiversity origin (Darwin, 1859)
We aimed to address the following questions of adaptive interslopes microecological divergence across ∼100 m: (1) whether the flowering times were significantly differentiated between the two interslope ecotypes; (2) whether the expression or sequence variations on the flowering time genes were diverged between the two ecotypes? Likewise, what regulatory modules of genes or pathways that are adapted to the interslope microclimatic divergence induce the differentiation of flowering time between the two ecotypes? The investigation on both phenotypic and transcriptomic divergence of these two ecotypes of R. lunaria, will shed light on our better understanding of the molecular basis of sympatric speciation in plants in ecologically divergent microsites
To further explore whether the constitute expression were divergent between the two ecotypes, differential expression analysis was first performed with EBSeq (Leng et al, 2013) under 1% false discover cutoff and at least twofold change
Summary
First proposed by Darwin as speciation occurring in contiguous populations with ongoing gene flow, was considered as one of the important models of biodiversity origin (Darwin, 1859). Compared to other geographic models of speciation, such as the allopatric and parapatric speciation models, sympatric speciation attracts particular interests for the reproductive barriers must evolve in situ to prevent homogenization, which was challenging to be proved between contiguous populations (Mayr, 1947, 1963; Fitzpatrick et al, 2008; Bird et al, 2012). Previous empirical studies and theoretical modeling supported that sympatric speciation was possible (Smith, 1966; Gavriletz, 2004; Bolnick and Fitzpatrick, 2007). It required the conditions of primary divergence with gene flow between populations, with complete absence of geographic barriers, which could be uncommon in nature. There is currently very little evidence to prove that natural selection in plants could induce sympatric speciation, partially due to the fact that flowering time hardly diverged between contiguous populations
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