Genomic and Transcriptomic Divergence during Ecological Speciation Driven By Adaptation to Altitude

Even though Darwin's "On the Origin of Species" implied selection being the main driver of species formation, the role of natural selection in speciation remains poorly understood. In particular, it remains unclear how selection at a few genes can lead to genome-wide divergence and the formation of distinct species. To investigate these processes we have been carrying out genomic, transcriptomic and QTL mapping investigations in a pair of plant species that have most likely evolved through ecological speciation.

The transcriptomic analysis identified only 90 genes (out of ca. 18,000) which were significantly differentially expressed between the species. These genes showed significantly elevated species differentiation (F_ST and D_xy), consistent with diversifying selection acting on these genes. Genome-wide genetic differentiation of the species is surprisingly low (F_ST = 0.19), while ca. 200 genes showed significantly higher (FDR < 1%; mean outlier F_ST > 0.6) interspecific differentiation and evidence for local adaptation. Loci showing signatures of adaptive divergence cluster into small ‘speciation islands’ that overlap quantitative trait loci (QTL) controlling morphological differences and differential gene expression between the species.

Hybrid breakdown has been observed in this system and we have started to dissect its genetic bases using transcriptome sequencing and a high density genetic mapping. A single QTL of major effect appears responsible for the hybrid breakdown, and gene expression of over 12% of the loci is significantly disrupted due to hybrid breakdown. This provides support for the idea that initially (sub-) species divergence builds up primarily in the genomic regions responsible for phenotypic traits under divergent selection, even in the face of gene flow. Gradual accumulation of genetic incompatibilities, such as the hybrid breakdown reported here, may lead to wider genomic divergence and eventually to complete separation of gene pools, but even at the early stages of speciation morphological and ecological differences between the species may be surprisingly high despite the fact that the majority of the gene pools are effectively shared by the two species.