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 Darwin's 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. We found that just 18% of previously assigned hybrid birds based on microsatellites could be 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. For private alleles detected in both years (N = 536) between 11%-76% of alleles underwent a frequency increase and 13%-61% a frequency decrease between 2005 and 2013, which was sensitive to sampling effort. We identified 28 private alleles that were candidates under selection via local PCA 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 Darwin's tree finch across years may aid in the retention of adaptive alleles and genetic diversity in birds threatened with extinction.

Keywords: Camarynchus; Darwin's finches; RAD sequencing; hybridization; introgression; private alleles.

FIGURE 1

(a) PCA plot from pcadapt with genetic groups labelled according to microsatellite‐based genetic assignments; (b) PCA plot from pcadapt with genetic groups labelled following SNP‐based genetic assignment analysis (using snmf); (c) Admixture coefficients (q‐value). From genetic structure analysis using snmf showing two distinct genetic clusters, C. parvulus and C. pauper , with a third group with increased admixture (hybrid). Samples in (c) are shown re‐labelled after comparison with initial microsatellite identifications.

FIGURE 2

Numbers of birds assigned to each genetic group ( C. parvulus , C. pauper or hybrid) using 10 microsatellites (Kleindorfer et al. ; Peters et al. 2017) versus 6637 SNPs used in the current study. Microsatellite assignments were based on Structure (Pritchard, Stephens, and Donnelly 2000), SNP assignments were based on snmf (Frichot et al. 2014), both using a 0.80 assignment threshold value.

FIGURE 3

Co‐ancestry matrix visualised as a heat map fineRADstructure and RADpainter. The colour of each cell in the matrix (estimated co‐ancestry) shows the number of expected shared genetic markers copied from a donor genome (column) to a recipient genome (row). Support for the branches on the clustering dendrogram (co‐ancestry tree) is shown on the plot. Yellow highlighted samples are C. parvulus , blue is C. pauper and individuals with green highlighted are hybrids, as assigned by genetic clustering analysis using snmf.

FIGURE 4

Pairwise AMOVA F _st for the 69 outlier loci identified using pcadapt for (a) C. parvulus versus C. pauper , (b) C. pauper versus hybrid and (c) C. parvulus versus hybrid.

FIGURE 5

Results of multidimensional scaling (MDS) analysis (localPCA in lostruct). In (a), three extreme clusters of windows are colour‐coded in an aggregated PCA of MDS 1 and MDS 2 coordinates. Group 1 (green points) corresponds with C. parvulus , group 2 (orange) corresponds with C. pauper and group 3 (purple) corresponds with the hybrid group. In (b), MDS coordinates of outlier (colour‐coded clusters) and nonoutlier (black points) windows are shown mapped on to chromosomes of the C. parvulus genome (N = 30 chromosomes).