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DNA fragility in the parallel evolution of pelvic reduction in stickleback fish

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Science  04 Jan 2019:
Vol. 363, Issue 6422, pp. 81-84
DOI: 10.1126/science.aan1425

DNA breakage and adaptation

Adaptation to new environments often occurs in similar ways across different colonization events. Stickleback fish represent a classic example of this, in which repeated colonizations of freshwater have resulted in the loss of pelvic hind fins. Previous work has shown that a pelvic enhancer gene is involved. Xie et al. now show that this gene lies within a region of the genome that is prone to double-stranded DNA breakage owing to a high thymine-guanine content. This enhanced region of breakage could lead to enhanced mutation rates that facilitate repeated adaptations to new environments.

Science, this issue p. 81

Abstract

Evolution generates a remarkable breadth of living forms, but many traits evolve repeatedly, by mechanisms that are still poorly understood. A classic example of repeated evolution is the loss of pelvic hindfins in stickleback fish (Gasterosteus aculeatus). Repeated pelvic loss maps to recurrent deletions of a pelvic enhancer of the Pitx1 gene. Here, we identify molecular features contributing to these recurrent deletions. Pitx1 enhancer sequences form alternative DNA structures in vitro and increase double-strand breaks and deletions in vivo. Enhancer mutability depends on DNA replication direction and is caused by TG-dinucleotide repeats. Modeling shows that elevated mutation rates can influence evolution under demographic conditions relevant for sticklebacks and humans. DNA fragility may thus help explain why the same loci are often used repeatedly during parallel adaptive evolution.

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