Abstract
Background“Explosive” adaptive radiations on islands remain one of the most puzzling evolutionary phenomena. The rate of phenotypic and ecological adaptations is extremely fast during such events, suggesting that many genes may be under fairly strong selection. However, no evidence for adaptation at the level of protein coding genes was found, so it has been suggested that selection may work mainly on regulatory elements. Here we report the first evidence that positive selection does operate at the level of protein coding genes during rapid adaptive radiations. We studied molecular adaptation in Hawaiian endemic plant genus Schiedea (Caryophyllaceae), which includes closely related species with a striking range of morphological and ecological forms, varying from rainforest vines to woody shrubs growing in desert-like conditions on cliffs. Given the remarkable difference in photosynthetic performance between Schiedea species from different habitats, we focused on the “photosynthetic” Rubisco enzyme, the efficiency of which is known to be a limiting step in plant photosynthesis.ResultsWe demonstrate that the chloroplast rbcL gene, encoding the large subunit of Rubisco enzyme, evolved under strong positive selection in Schiedea. Adaptive amino acid changes occurred in functionally important regions of Rubisco that interact with Rubisco activase, a chaperone which promotes and maintains the catalytic activity of Rubisco. Interestingly, positive selection acting on the rbcL might have caused favorable cytotypes to spread across several Schiedea species.SignificanceWe report the first evidence for adaptive changes at the DNA and protein sequence level that may have been associated with the evolution of photosynthetic performance and colonization of new habitats during a recent adaptive radiation in an island plant genus. This illustrates how small changes at the molecular level may change ecological species performance and helps us to understand the molecular bases of extremely fast rate of adaptation during island adaptive radiations.
Highlights
The most dramatic ‘‘bursts’’ of adaptive radiation often occur within confined geographical regions
As the efficacy of selection is proportional to the product of the selective coefficient and the effective population size [4], the relatively small effective population size of island species should result in a reduced efficacy of natural selection
We demonstrated that the rbcL gene, encoding the large subunit of Rubisco enzyme, might have been under strong positive selection during recent adaptive radiation in Hawaiian Schiedea
Summary
The most dramatic ‘‘bursts’’ of adaptive radiation often occur within confined geographical regions (e.g. oceanic islands or inland freshwater lakes; e.g. [1]). Many island species are thought to evolve via colonization of new islands or habitats (‘‘island hopping speciation’’, [3]). Such colonization events should lead to a drastic reduction in population size. Few studies have investigated the action of selection at the molecular level during island adaptive radiations [6,7] These studies indicated some increase in non-synonymous (dN) to synonymous (dS) substitution rates in the Hawaiian silversword alliance, which may reflect slight relaxation of purifying selection in small island populations, but no convincing evidence of positive selection has been reported
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