Phylogenomics Reveals Three Sources of Adaptive Variation during a Rapid Radiation

Abstract

Speciation events often occur in rapid bursts of diversification, but the ecological and genetic factors that promote these radiations are still much debated. Using whole transcriptomes from all 13 species in the ecologically and reproductively diverse wild tomato clade (Solanum sect. Lycopersicon), we infer the species phylogeny and patterns of genetic diversity in this group. Despite widespread phylogenetic discordance due to the sorting of ancestral variation, we date the origin of this radiation to approximately 2.5 million years ago and find evidence for at least three sources of adaptive genetic variation that fuel diversification. First, we detect introgression both historically between early-branching lineages and recently between individual populations, at specific loci whose functions indicate likely adaptive benefits. Second, we find evidence of lineage-specific de novo evolution for many genes, including loci involved in the production of red fruit color. Finally, using a “PhyloGWAS” approach, we detect environment-specific sorting of ancestral variation among populations that come from different species but share common environmental conditions. Estimated across the whole clade, small but substantial and approximately equal fractions of the euchromatic portion of the genome are inferred to contribute to each of these three sources of adaptive genetic variation. These results indicate that multiple genetic sources can promote rapid diversification and speciation in response to new ecological opportunity, in agreement with our emerging phylogenomic understanding of the complexity of both ancient and recent species radiations.

Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

“…Over this time period, the Oryzeae have maintained a base chromosome number of 12, despite having adapted to different ecological conditions associated with their global distribution and withstanding bursts of TE diversification that, in some cases, led to doubling of genome sizes, as in O. australiensis 20 and O. granulata 21 . Our phylogenomic work illustrates both the challenges of inferring species phylogenies in closely related plant taxa-incomplete lineage sorting 89 , hybridization and introgression 90 -and the power of whole-genome sequences to untangle the resulting phylogenetic discordance. Combining recent tools for species tree inference with this massive dataset permitted us to construct a much more nuanced view of the species phylogeny in Oryza that reflects the mosaic history of different parts of the genome 91 .…”

De Novo Assembly of a New Solanum pennellii Accession Using Nanopore Sequencing

“…Gene calling was performed with Augustus with external homology evidence from Arabidopsis thaliana, Solanum lycopersicum, and S. pennellii LA716 and with external RNaseq evidence from public S. pennellii samples in SRP068871 (Pease et al, 2016b), ERP005244 (Bolger et al, 2014a), and SRP067562 (Pease et al, 2016a). Putative missing genes were identified as orthogroups produced by OrthoFinder that had zero members in just one species.…”

Targeted Sequencing of Venom Genes from Cone Snail Genomes Improves Understanding of Conotoxin Molecular Evolution

“…Past studies have described several genetic characteristics that seem to be associated with rapidly radiating clades or the evolution of novel phenotypes, including evidence for diversifying selection, gene gains and losses, and accelerated rates of sequence evolution (Floudas et al 2012;Brawand et al 2014;Guill en et al 2014;Cornetti et al 2015;Malmstrøm et al 2016;Pease et al 2016). Although large-scale comparative genomic studies have vastly increased our knowledge of the genetic changes associated with diversification, the link between genotype and ecologically relevant phenotypes frequently remains unclear.…”

“…Although large-scale comparative genomic studies have vastly increased our knowledge of the genetic changes associated with diversification, the link between genotype and ecologically relevant phenotypes frequently remains unclear. Often, the functional consequences of genetic patterns such as an excess of gene duplicates or regions under positive selection are unknown (Brawand et al 2014;Cornetti et al 2015;Pease et al 2016), limiting our ability to understand how genetic changes shape the evolutionary trajectory of species.…”