Genomic Architecture, Differentiation, and Adaptation in Three Large Falcons

Abstract

Recent chromosomal rearrangements and divergence in large falcon species make them excellent foci for studies on evolution and genomic architecture. Here, we use high-coverage (44-74X) whole genome resequencing with 10X Genomics Linked-Reads to assess patterns of genomic divergence in peregrine, saker, and gyrfalcons and we link these to chromosomal type and chromosomal rearrangements. We first use admixture analysis and cross-coalescent MSMC2 to demonstrate distinct species boundaries between the large falcons and retrace their demography. We assessed genomic landscapes in terms of recombination rate, nucleotide diversity ({pi}), Tajimas D, autozygosity and Fst between saker and gyrfalcons: {pi} had higher values on smaller chromosomes and Fst had higher values on larger chromosomes. Recombination rate concealed other chromosome type effects on {pi} and Tajimas D but largely explained variation in Fst. We find 39 selective sweeps--some shared--across the falcons. However, only five candidate genes--mostly housekeeping genes--were implicated as targets of balancing selection across all falcons, with 4 of these shared between Hierofalco and three shared across all the falcons. Occurrence of selective sweeps and balancing selection were not enriched by chromosome type or in the context of chromosome fusions. Overall, our findings provide insights into divergence and adaptation in large falcons, and demonstrate an association of genomic architecture and chromosomal fusions with all population genomic indicators and metrics of differentiation between species. Significance StatementFalcons are culturally and commercially important birds that have undergone recent chromosomal rearrangement, providing a natural system for studies on chromosomal heterogeneities and evolution. By analyzing genomic variation across three large falcon species, we show that chromosome type and chromosomal fusions structure patterns of recombination, diversity, and divergence. Our findings highlight the importance of underlying genomic architecture to common forms of evolutionary inference and call attention to the role of chromosomal fusions in shaping falcon evolution.