The passenger pigeon (Ectopistes migratorius) numbered between 3 billion and 5 billion individuals before its 19th-century decline and eventual extinction (1). Passenger pigeons were highly mobile and bred in large social colonies, and their population lacked clear geographic structure (2). Few vertebrates have populations this large and cohesive, and the neutral model of molecular evolution predicts that effective population size (Ne) and genetic diversity will increase in proportion to population size (3). Preliminary analyses of passenger pigeon genomes have, however, revealed surprisingly low genetic diversity (4). This finding has been interpreted within the framework of the neutral theory of molecular evolution as the result of a history of large demographic fluctuations (4). However, in large populations, natural selection may be particularly important in shaping genetic diversity: Population genetic theory predicts that selection will be more effective in large populations (3), and selection on one locus can cause a loss of diversity at other loci, particularly those that are closely linked (5–8). It has been suggested that this could explain why the genetic diversity of a species is poorly predicted by its population size (9–11).
We investigated the impact of natural selection on passenger pigeon genomes through comparative genomic analyses of both passenger pigeons and band-tailed pigeons (Patagioenas fasciata). Although ecologically and physiologically similar to passenger pigeons, band-tailed pigeons have a present-day population size three orders of magnitude smaller than that of their close relative, the passenger pigeon (2, 12, 13).
We applied a Bayesian skyline model of ancestral population dynamics to the mitochondrial genomes of 41 passenger pigeons from across their former breeding range (Fig. 1A and table S1) (14). This returned a most recent effective population size (Ne) of 13 million [95% highest posterior density (HPD) interval: 2 million to 58 million] and a similar, stable Ne for the previous 20,000 years (Fig. 1B). Although this Ne is much lower than the (census) population size (Nc), it is greater than previous estimates from analyses of nuclear genomes (4) and is likely to be conservative (14).
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