Genomic variation, population history and within-archipelago adaptation between island bird populations

Abstract

Oceanic island archipelagos provide excellent models to understand evolutionary processes. Colonization events and gene flow can interact with selection to shape genetic variation at different spatial scales. Landscape-scale variation in biotic and abiotic factors may drive fine-scale selection within islands, while long-term evolutionary processes may drive divergence between distantly related populations. Here, we examine patterns of population history and selection between recently diverged populations of the Berthelot's pipit (Anthus berthelotii), a passerine endemic to three North Atlantic archipelagos. First, we use demographic trees and f₃ statistics to show that genome-wide divergence across the species range is largely shaped by colonization and bottlenecks, with evidence of very weak gene flow between populations. Then, using a genome scan approach, we identify signatures of divergent selection within archipelagos at single nucleotide polymorphisms (SNPs) in genes potentially associated with craniofacial development and DNA repair. We did not detect within-archipelago selection at the same SNPs as were detected previously at broader spatial scales between archipelagos, but did identify signatures of selection at loci associated with similar biological functions. These findings suggest that similar ecological factors may repeatedly drive selection between recently separated populations, as well as at broad spatial scales across varied landscapes.

Keywords: adaptation; birds; colonization history; genome scan; population genetics; spatial scales.

Figure 1.

Locations of Berthelot's pipit populations used in the current study. Canary Island populations: El Hierro (EH), La Palma (LP), La Gomera (GOM), El Teide (TEID) mountain population of Tenerife, lowland Tenerife (TF), Gran Canaria (GC), Fuerteventura (FV), Lanzarote (LZ) and La Graciosa (GRA). Madeiran populations: Madeira (M), Porto Santo (PS) and Deserta Grande (DG). Selvagem Grande (SG), Selvagens archipelago.

Figure 2.

Evolutionary relationships between island populations of the Berthelot's pipit. (a) Maximum-likelihood bifurcating tree of population history—without subsequent gene flow—across the pipit colonization range as inferred by TreeMix. The branch length-scale bar shows 10 times the average standard error in the covariance matrix of ancestry. (b) The relationship between LD and base-pair distance for SNPs across each Madeiran Island (green), three Canary Island populations (purple), and the Selvagens (orange); Tenerife, a central island assumed to be a large outbred population with low within-archipelago divergence (figure 3a), and El Hierro and La Graciosa populations which have long branch lengths and strongest within-archipelago genome-wide divergence. The fit lines show a local regression model, with a shaded band indicating 95% confidence intervals.

Figure 3.

Population structure based on genome-wide ddRAD SNPs among Berthelot's pipit populations separately across the Canary Islands and Madeiran archipelago. (a) PCA across the Canary Island populations. PC1 and PC2 explained 2.7% and 2.3% of genomic variation, respectively. (b) PCA of Madeiran archipelago populations; PC1 = 3.5%, PC2 = 1.6% of genomic variation explained. Canary Island populations: El Hierro (EH), La Palma (LP), La Gomera (GOM), El Teide (TEID), lowland Tenerife (TF), Gran Canaria (GC), Fuerteventura (FV), Lanzarote (LZ) and La Graciosa (GRA). Madeiran populations: Madeira (M), Porto Santo (PS) and Deserta Grande (DG).

Figure 4.

Manhattan plots of EigenGWAS analyses based on genome-wide ddRAD SNPs among Berthelot's pipit populations within archipelagos. (a) Canary Islands PC1, clustering east–west geographical gradient, as seen in figure 3a. Horizontal red line indicates Bonferroni-corrected significance of p < 1.12 × 10⁻⁵ based on 4470 genome-wide ddRAD SNPs. (b) Madeiran archipelago PC1, separating Deserta Grande from Madeira and Porto Santo islands, as seen in figure 3b. Horizontal red line indicates Bonferroni-corrected significance of p < 1.70 × 10⁻⁵ based on 2938 genome-wide ddRAD SNPs. Unmapped SNPs are recorded as ‘Un’, and alternate black-grey colouring indicates chromosomal limits.

Figure 5.

Within-archipelago genetic differentiation of genome-wide ddRAD SNPs among Berthelot's pipit populations. Points represent F_ST of 3531 mapped genome-wide ddRAD SNPs between populations, across the Canary Islands and the Madeiran archipelago. SNPs identified by the EigenGWAS analysis for the Canary Islands archipelago (y-axis) and Madeiran archipelago (x-axis) are highlighted in red and labelled with their SNP code. Please note: no unmapped SNPs had F_ST > 0.16 or greater than 0.40 for the Canary Islands and Madeiran archipelago, respectively.