Genomic introgression between critically endangered and stable species of Darwin's tree finches on the Galapagos Islands

Abstract

Natural hybridisation among rare or endangered species and stable congenerics is increasingly topical for the conservation of species-level diversity under anthropogenic impacts. Evidence for beneficial genes being introgressed into or selected for in hybrids raises concurrent questions about its evolutionary significance. In Darwins tree finches on the island of Floreana (Galapagos Islands, Ecuador), the Critically Endangered medium tree finch (Camarhynchus pauper) undergoes introgression with the stable small tree finch (Camarhynchus parvulus), and hybrids regularly backcross with C. parvulus. Earlier studies in 2005-2013 documented an increase in the frequency of Camarhynchus hybridisation on Floreana using field-based and microsatellite data. With single nucleotide polymorphism (SNP) data from the same Floreana tree finches sampled in 2005 and 2013 (n = 95), we examine genome-wide divergence across parental and hybrid birds and evidence for selection in hybrids. In assessing previous estimates of introgression we found that just 18% of previously assigned hybrid birds based on microsatellites were assigned to hybrids using SNPs. Over half of the previously assigned hybrids (63%) were reassigned to C. parvulus, though parental species showed concordance with prior assignments. Of 4869 private alleles found in hybrid birds, 348 were at a high frequency ([≥]0.30) that exceeded their parental species of origin 89-96% of the time. Across the two years, 3436 (70.6%) private alleles underwent a substantial ([≥]0.30) allele frequency increase or decrease. Of these, 28 private alleles were identified as candidate loci under selection via local PCA genome scans and outlier tests. Alleles were annotated to genes associated with inflammation, immunity, brain function and development. We provide evidence that introgression among a critically endangered and stable species of Darwins tree finch is being retained by selection across years and may aid in the retention of genetic diversity in birds threatened with extinction.