Genome-wide signals of drift and local adaptation during rapid lineage divergence in a songbird

Abstract

The formation of independent evolutionary lineages involves neutral and selective factors, and understanding their relative roles in population divergence is a fundamental goal of speciation research. Correlations between allele frequencies and environmental variability can reveal the role of selection, yet the relative contribution of drift can be difficult to establish. Recently diversified systems such as that of the Oregon junco (Aves: Emberizidae) of western North America provide ideal scenarios to apply genetic-environment association analyses (GEA) while controlling for population structure. Genome-wide SNP loci analyses revealed marked genetic structure consisting of differentiated populations in isolated, dry southern mountain ranges, and more admixed recently expanded populations in humid northern latitudes. We used correlations between genomic and environmental variance to test for three specific modes of evolutionary divergence: (i) drift in geographic isolation, (ii) differentiation along continuous selective gradients, and (iii) isolation by adaptation. We found evidence of strong drift in southern mountains, but also signals of local adaptation in several populations, driven by temperature, precipitation, elevation and vegetation, especially when controlling for population history. We identified numerous variants under selection scattered across the genome, suggesting that local adaptation can promote rapid differentiation over short periods when acting over multiple independent loci.

Population assignment reveals low migratory connectivity in a weakly structured songbird

“…Additionally, the observed genetic variation associated with environment may be indicative of local adaptation, given that breeding sites varied in environmental conditions. The amount of total variance explained, as well as the individual contributions of geography and environment, was generally higher than reported in other avian studies using RDA (Friis et al, ; Szulkin, Gagnaire, Bierne, & Charmantier, ). This may be due to our use of a much smaller subset of 600 SNPs data filtered by F ST than random sets of more than 10,000 SNPs.…”

“…Environmental association analyses of avian species have found ecological factors such as temperature (Andrew, Jensen, Hagen, Lundregan, & Griffith, ; Friis et al, ; Seeholzer & Brumfield, ; Termignoni‐Garcia et al, ; Zhen et al, ), precipitation (Bay et al, ; Friis et al, ; Zhen et al, ) and habitat (Szulkin et al, ) to be associated with spatial patterns of genomic variation. In our study, the relation of ENV_PC1 with temperature may be indicative of local adaptation associated with temperature differences, including seasonality, among the breeding sites.…”

Change in sexual signalling traits outruns morphological divergence across an ecological gradient in the post‐glacial radiation of the songbird genusJunco

“…palliatus, and at least six distinct and geographically structured forms currently grouped within the dark-eyed junco (Junco hyemalis) complex: the red-backed junco (J. h. dorsalis) from south-western USA; the greyheaded junco (J. h. caniceps) in the Rocky Mountains; the Oregon junco complex (J. h. oreganus) across the West, composed in turn of several distinct forms from northern Baja California to Alaska, including townsendi, pontilis, thurberi, pinosus, montanus, shufeldti and oreganus; the pink-sided junco (J. h. mearnsi) in the northern Rocky Mountains; the white-winged junco (J. h. aikeni) in the Black Hills of South Dakota; and the slate-coloured junco in eastern and boreal North America, comprising J. h. hyemalis, J. h. carolinensis and J. h. cismontanus ( Figure 1; Table 1; Miller, 1941;Nolan et al, 2002;Sullivan, 1999). These recently radiated dark-eyed junco forms represent independent evolutionary lineages according to genome-wide data (Friis et al, 2016(Friis et al, , 2018 and are characterized by a stunning diversity of plumage patterns and colours (Figure 1a), suggesting that sexual selection may have played a relevant role in the phenotypic diversification of the young forms of junco. However, the fact that the radiation took place across a wide latitudinal axis of pronounced ecological variability also suggests the involvement of ecological selective pressures in the diversification process, a hypothesis that has recently received experimental support for the case of the Oregon junco complex (Friis et al, 2018).…”

“…These recently radiated dark-eyed junco forms represent independent evolutionary lineages according to genome-wide data (Friis et al, 2016(Friis et al, , 2018 and are characterized by a stunning diversity of plumage patterns and colours (Figure 1a), suggesting that sexual selection may have played a relevant role in the phenotypic diversification of the young forms of junco. However, the fact that the radiation took place across a wide latitudinal axis of pronounced ecological variability also suggests the involvement of ecological selective pressures in the diversification process, a hypothesis that has recently received experimental support for the case of the Oregon junco complex (Friis et al, 2018).…”

A High-Quality Genome Assembly of the North American Song Sparrow, Melospiza melodia

“…The lower genetic variability in this naturally inbred population makes song sparrows from the Aleutian islands a favorable resource for generating a reference genome assembly, because lower levels of polymorphism between both copies of a diploid genome can improve assembly quality. Previous work has also been done on the song sparrow transcriptome, developing genomic markers to screen at population levels (Srivastava et al 2012 Friis et al 2018). In this study, we provide the genome assembly of Melospiza melodia, a member of the family Passerellidae.…”