The Genomic Underpinnings of Convergent Evolution: Repeated Loss of Flight in Island Rails, the Greatest Avian Colonizers

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Convergent evolution—when similar changes occur in independent lineages—may be caused by similar selection pressures resulting in the same adaptations. This is exemplified by the evolution of echolocation in bats and whales, and the evolution of flight in insects, bats, and birds. The phenotypic convergence in major traits is less well-understood at a molecular level, and cases of genomic convergence are rare. In this action, I will focus on rails, a family of birds that is outstanding in two respects: (1) They are extremely successful dispersers and have colonized hundreds or thousands of islands by flight. (2) If island conditions did not require a volant lifestyle, over time the developmental resource investment into the flight apparatus is reduced, and the flight capability often eventually entirely lost. The loss of flight has occurred repeatedly and independently at least 30 times, often over short evolutionary time scales (<125,000 years). I will combine field sampling with historic samples from the unique bird collection of the Natural History Museum of the UK, including six now extinct species. With an extended museomics approach, I will sequence and assemble whole genomes with large-fragment linked-reads, and then employ a novel whole-genome alignment-based annotation method, followed by identification of genes or regulatory elements as targets for selection for flightlessness, replicated over three different lineages of rails. This MSCA action will uncover the genomic underpinnings of recent loss of flight and address the fundamental question whether phenotypic convergent adaption is reflected by convergence at a molecular level. It will also assess the contribution of changes in amino acid sequence vs. changes in gene regulation. Understanding the genomic changes behind loss of flight can also offer unique insights into the original gain of flight in the transitional theropod dinosaurs, ancestors of modern birds.