Mitogenomics clarifies the position of the Nearctic magpies (Pica hudsonia and Pica nuttalli) within the Holarctic magpie radiation

Abstract

Partial separation of a peripheral population may lead to its divergence and, potentially, speciation due to genetic drift followed by selection and geographic isolation. This process may cause taxonomic uncertainty because reproductive isolation in allopatry cannot be verified directly. The two Nearctic allopatric species of magpies (Aves, Corvidae: Pica) serve as a good example of these problems. The Black-billed magpie Pica hudsonia is widely distributed in North America, whereas the Yellow-billed Magpie Pica nuttalli is endemic to restricted range in California. Their relationships with Palearctic species have been little studied. We obtained complete mitochondrial genomes of both Nearctic magpie species, along with the Eurasian Magpie (Pica pica) and the Oriental Magpie (Pica serica), 20 mitogenomes in total. Phylogenetic analysis reveals a basal position of P. serica, and P. pica as a sister clade to the two Nearctic species. P. hudsonia and P. nuttalli form reciprocal monophyletic subclades, showing recent divergence between and within them. Our data show that the Nearctic magpie lineage diverged from the common ancestor with P. pica, with a single migration wave via the Beringia. Within the Nearctic, we hypothesize a peripatric mode of speciation among Pica taxa due to divergence and separation of the small marginal population in California below the Sierra-Nevada mountains. Diversifying amino acid substitutions in ND4-ND5-ND6 genes along the branch leading to the New World clade may indicate selection for heat-tolerance. Considering the clear phenotypic differences between P. hudsonia and P. nuttalli, our data, showing their reciprocal monophylies and genetic distinctness, is consistent with the two-species taxonomy.