Avian plumage polymorphism provides an ideal model for exploring the ecological and genetic bases of phenotypic diversity and adaptive evolution. The Otago Shag (Leucocarbo chalconotus) and Foveaux Shag (Leucocarbo stewarti) are closely related seabird taxa endemic to southern New Zealand. In contrast to their Southern Ocean island sister taxa, which exhibit uniform pied (black-and-white countershading) plumage, these mainland taxa each comprise two distinct adult colour morphs: pied and bronze (fully dark). Colour morph frequencies vary geographically, and the two morphs appear to interbreed freely while showing pronounced ecological differences. Despite this, the genetic basis and evolutionary significance of this polymorphism have remained poorly understood. In this thesis, I investigated the evolutionary and genetic bases of plumage colour polymorphism in Leucocarbo shags using genome-wide sequencing and candidate-gene approaches in a phylogenomic context. The genotyping-by-sequencing (GBS) approach was used to reconstruct phylogenetic relationships within the genus and to test for genome-wide genetic differentiation between colour morphs within species. Nuclear genome analyses largely supported existing taxonomic hypotheses but revealed topological discordance with previous mitochondrial and nuclear DNA studies, particularly in the placement of the New Zealand King Shag (Leucocarbo carunculatus). These results further indicate the likely influence of incomplete lineage sorting and historical introgression among the Chatham Island (Leucocarbo onslowi), Otago, and Foveaux Shags. Nevertheless, analyses consistently supported the Otago and Foveaux Shags as distinct species, and no evidence of genome-wide differentiation was detected between pied and bronze morphs within either species. In parallel, a candidate-gene approach focused on the vertebrate pigmentation gene Melanocortin 1 Receptor (MC1R). Sanger sequencing identified a novel non-synonymous substitution (D119G), a dominant mutation that strongly discriminates between intraspecific colour morphs within this New Zealand seabird clade. In addition, comparative mapping of MC1R variation across the shag phylogeny suggests that an amino acid substitution (R112H) may be associated with interspecific plumage differences in the Spotted Shag (Phalacrocorax punctatus) and its close relatives, highlighting a potential broader evolutionary role of MC1R in plumage diversification among shags. By integrating genetic results with ecological and behavioural data, this study further suggests that the novel melanic inshore ecotype in Otago and Foveaux Shags, which lacks countershading, is an adaptive response to southern New Zealand’s glacial-fed coastal freshwater plumes. Differences in morph frequencies across habitats with contrasting water clarity indicate that variation in ambient light conditions may impose differential selection on plumage colour through effects on camouflage efficiency, potentially mediated by pleiotropic effects of MC1R. Overall, this study demonstrates that intraspecific colour polymorphism in Leucocarbo shags may be largely controlled by a key large-effect gene. Its maintenance and evolutionary significance, however, are shaped by a complex interplay of historical processes and environment-dependent selection on camouflage. These findings highlight the importance of integrating nuclear genomic and ecological data when investigating the adaptive significance of rapid radiations and provide valuable insights for the conservation of New Zealand seabirds and for broader studies of avian plumage evolution.
Shanshan Shen (Thu,) studied this question.