Habitat and climate influence hybridization among three genetically distinct Canada jay (Perisoreus canadensis) morphotypes in an avian hybrid zone complex

Abstract

Examining the frequency and distribution of hybrids across contact zones provide insights into the factors mediating hybridization. In this study, we examined the effect of habitat and climate on hybridization patterns for three phenotypically, genetically, and ecologically distinct groups of the Canada jay (Perisoreus canadensis) in a secondary contact zone in western North America. Additionally, we tested whether the frequency of hybridization involving the three groups (referred to as Boreal, Pacific and Rocky Mountain morphotypes) is similar across the hybrid zones or whether some pairs have hybridized more frequently than others. We reanalyzed microsatellite, mtDNA and plumage data, and new microsatellite and plumage data for 526 individuals to identify putative genetic and phenotypic hybrids. The genetically and phenotypically distinct groups are associated with different habitats and occupy distinct climate niches across the contact zone. Most putative genetic hybrids (86%) had Rocky Mountain ancestry. Hybrids were observed most commonly in intermediate climate niches and in habitats where Engelmann spruce (Picea engelmannii) overlaps broadly with boreal and subalpine tree species. Our finding that hybrids occupy intermediate climate niches relative to parental morphotypes matches patterns for other plant and animal species found in this region. This study demonstrates how habitat and climate influence hybridization patterns in areas of secondary contact and adds to the growing body of research on tri-species hybrid zones.

Fig. 1. Sketches show the plumage differences of the three Canada jay (Perisoreus canadensis) morphotypes (Boreal, Rocky Mountain, and Pacific) and the key tree species they are associated with (illustrations by Howard Coneybeare).

Boreal morphotypes are strongly associated with white spruce (Picea glauca), Rocky Mountain morphotypes are associated with Engelmann spruce (P. engelmanni), and Pacific morphotypes are not associated with any particular spruce species but are found in coniferous forests of the western subalpine. Map shows the distributions of the three Canada jay morphotypes across the contact in southwestern Canada and northwestern United States: Boreal (red), Rocky Mountain (yellow), and Pacific (green). Inset I) shows populations from further north in northern British Columbia and the Northwest Territories Canada. Pie charts show the nuclear genetic group that individuals were assigned to with STRUCTURE and GENODIVE (as found in Fig. 3): Boreal (red), Rocky Mountain (yellow), Pacific (green), and putative hybrids (purple). For information on the individuals included in each group, please see Table S1. Inset II) Map showing the distribution of white spruce (Picea glauca; light brown), Engelmann spruce (P. engelmanni; white), and western subalpine (dark gray), and the areas of overlap between white and Engelmann spruce (light purple), and western subalpine and Engelmann spruce (light blue) across the contact zone.

Fig. 2. Statistical parsimony network showing the relationship between the three Canada jay (Perisoreus canadensis) morphotypes and putative phenotypic hybrids (intergrades) for 190 individuals using a 506 bp fragment of the mtDNA control region.

Colors correspond with the morphotype (Boreal = red; Rocky Mountain = yellow; Pacific = green; intergrade = purple) assigned to each individual, while small black circles represent inferred haplotypes. Canada jay morphotype illustrations by Howard Coneybeare.

Fig. 3. Histogram showing genetic assignment of the three Canada jay (Perisoreus canadensis) morphotypes (Boreal, Rocky Mountain, and Pacific) and putative phenotypic hybrids (referred to as intergrade morphotypes) using mtDNA (mt), GENODIVE (HI) and Structure (Q).

For microsatellite data, individuals were first assigned to a genetic cluster (red = Boreal, yellow = Rocky Mountain, Pacific = green) with STRUCTURE. Following this STRUCTURE run, individuals with admixed ancestry (i.e., those individuals with a Q < 0.70) were assigned to a genetic group or identified as a putative genetic hybrid type (olive = Boreal × Rocky Mountain, light gray = Pacific × Rocky Mountain, dark gray = Pacific × Boreal) with GENODIVE. For mtDNA the colors correspond with the three mtDNA clades (red = Boreal, yellow = Rocky Mountain, Pacific = green, white = not genotyped for mtDNA).

Fig. 4. Summary figure showing the distribution of Canada jay (Perisoreus canadensis) phenotypes and genotypes across forest types.

a Phenotypic patterns based on morphotype assignment by observers; b MtDNA clade; c Genotype assignment of microsatellite data based on hybrid index scores; d Distribution of putative hybrids across forest type (olive = Boreal × Rocky Mountain, dark gray = Pacific × Boreal, light gray = Pacific × Rocky Mountain). Colors in a-c represent Boreal (red), Rocky Mountain (yellow), Pacific (green), and intergrades (purple).

Fig. 5. Summary figure showing the distribution of Canada jay (Perisoreus canadensis) phenotypes and genotypes across an environmental gradient.

a Phenotypic patterns based on morphotype assignment by observers; b MtDNA clade distribution across forest type; c Genotype assignment of microsatellite data based on hybrid index scores; d Distribution of putative hybrids across forest type (olive = Boreal × Rocky Mountain, dark gray = Pacific × Boreal, light gray = Pacific × Rocky Mountain). Colors across a–d represent Boreal (red), Rocky Mountain (yellow), Pacific (green), and intergrade morphotypes (purple). For the mtDNA patterns, Rocky Mountain refers to the Intermountain West clade described in Dohms et al. (2017).

Fig. 6. Violin plots examining the relationship between environmental variation and phenotypic and genetic variation.

a morphotypes, b mtDNA lineages, and c microsatellite genotypes in Canada jays (Perisoreus canadensis). Plots with different letters indicate comparisons that were significantly different at p < 0.05 following least squares differences tests.

Fig. 7. Box plots of hybrid index scores for Canada jay (Perisoreus canadensis) Boreal and Pacific morphotypes in the presence and absence of Engelmann spruce.

For Rocky Mountain morphotypes which are associated with Engelmann spruce, we compared hybrid indices in forests where only Engelmann spruce was found and where Engelmann spruce overlapped with coastal and boreal tree species. Dark lines represent the median and the bottom and top of box represent the 25th and 75th quartiles, respectively, while the whiskers extend to the highest and lowest values. Asterisk above paired plots show comparisons significant at p < 0.05.