Barn swallow pangenomics provides insights into the evolution of synanthropy

Insights into the genomic evolution of non-model organisms are often limited by the lack of reference genomes. The barn swallow (Hirundo rustica) is a well-studied migratory passerine bird with six recognized subspecies in Europe, Asia, Africa and the Americas. While recent studies have started to shed light on its genetics, the absence of a high quality reference genome has hindered the understanding of the genetic bases of behavioural phenotypes and evolutionary adaptations. As part of the Vertebrate Genomes Project’s effort to generate complete, accurate and fully annotated genome assemblies, we present here a new chromosome-level reference genome for the barn swallow and the first pangenome for the species, produced using High-Fidelity long reads. We generated a reference-free whole-genome alignment with other bird species and a comprehensive catalogue of genetic markers. We used these genomic resources to identify genetic loci potentially under selective pressures. Conservation analyses performed on the multialignment pointed at genes enriched for DNA-binding, transcriptional regulation and neurodevelopment. The top candidate was CAMK2N2, encoding a protein that acts as inhibitor of CAMKII, involved in the glutamatergic system. Genome-wide linkage disequilibrium scans and extended haplotype statistics analyses using the genetic markers identified from all publicly available genomic data detected signatures of selection at a locus harbouring BDNF, a neurotrophin involved in the response to stress, fear memory formation and neural crest cells development. All these processes have been previously linked with tameness and domestication in animals, suggesting the possibility that selective pressures acting on genes involved in mechanisms regulating fear and stress response played a role in the evolution of the synanthropic habits of the barn swallow.