Abstract
The evolutionary processes that drive rapid species diversification are poorly understood. In particular, it is unclear whether Darwinian adaptation or non-adaptive processes are the primary drivers of explosive species diversifications. Here we show that repeated rapid radiations within New World lupins (Lupinus, Leguminosae) were underpinned by a major increase in the frequency of adaptation acting on coding and regulatory changes genome-wide. This contrasts with far less frequent adaptation in genomes of slowly diversifying lupins and all other plant genera analysed. Furthermore, widespread shifts in optimal gene expression coincided with shifts to high rates of diversification and evolution of perenniality, a putative key adaptation trait thought to have triggered the evolutionary radiations in New World lupins. Our results reconcile long-standing debate about the relative importance of protein-coding and regulatory evolution, and represent the first unambiguous evidence for the rapid onset of lineage- and genome-wide accelerated Darwinian evolution during rapid species diversification.
Highlights
The evolutionary processes that drive rapid species diversification are poorly understood
Taking advantage of the striking among-lineage variation in species diversification rates within this genus, we show that rapid species diversification is underpinned by rapid onset of lineage- and genome-wide accelerated adaptive evolution affecting both coding sequences and expression levels of genes
We identified and analysed coding sequences and normalized expression values for 6,013 orthologous genes present in at least 30 species (Supplementary Fig. 1) including both the rapidly and slowly radiating lineages of lupins
Summary
The evolutionary processes that drive rapid species diversification are poorly understood. We show that repeated rapid radiations within New World lupins (Lupinus, Leguminosae) were underpinned by a major increase in the frequency of adaptation acting on coding and regulatory changes genomewide This contrasts with far less frequent adaptation in genomes of slowly diversifying lupins and all other plant genera analysed. The scarcity of well-sampled comparative studies of genome-wide selective pressures in rapidly and slowly radiating groups of species means that how rapid diversification unfolds at the genetic level remains unclear. It is unclear whether rapid speciation and ecological and morphological evolution are driven by changes in many genes throughout the genome, or in just a few key regulatory genes. Within the New World, Lupinus spp. exhibit very diverse growth forms (ephemeral annuals, prostrate perennial herbs, acaulescent rosettes, stem rosettes, woody shrubs and small trees) and thrive in a very wide array of ecosystems and climates (coastal dunes, chaparral, sagebrush steppe and grasslands, but especially open mountain forests, meadows and disturbed slopes, extending to sub-alpine/alpine elevations) across an exceptionally wide altitudinal range (from sea level to 4,900 m, close to the upper global elevation limit for plant growth), and spanning B100° of latitude from B30°S in the Andes to B70°N in Alaska
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