Gene Flow of a Forest-Dependent Bird across a Fragmented Landscape

Abstract

Habitat loss and fragmentation can affect the persistence of populations by reducing connectivity and restricting the ability of individuals to disperse across landscapes. Dispersal corridors promote population connectivity and therefore play important roles in maintaining gene flow in natural populations inhabiting fragmented landscapes. In the prairies, forests are restricted to riparian areas along river systems which act as important dispersal corridors for forest dependent species across large expanses of unsuitable grassland habitat. However, natural and anthropogenic barriers within riparian systems have fragmented these forested habitats. In this study, we used microsatellite markers to assess the fine-scale genetic structure of a forest-dependent species, the black-capped chickadee (Poecile atricapillus), along 10 different river systems in Southern Alberta. Using a landscape genetic approach, landscape features (e.g., land cover) were found to have a significant effect on patterns of genetic differentiation. Populations are genetically structured as a result of natural breaks in continuous habitat at small spatial scales, but the artificial barriers we tested do not appear to restrict gene flow. Dispersal between rivers is impeded by grasslands, evident from isolation of nearby populations (~ 50 km apart), but also within river systems by large treeless canyons (>100 km). Significant population genetic differentiation within some rivers corresponded with zones of different cottonwood (riparian poplar) tree species and their hybrids. This study illustrates the importance of considering the impacts of habitat fragmentation at small spatial scales as well as other ecological processes to gain a better understanding of how organisms respond to their environmental connectivity. Here, even in a common and widespread songbird with high dispersal potential, small breaks in continuous habitats strongly influenced the spatial patterns of genetic variation.

Fig 1. Map showing sampling locations, barriers and hybrid poplar zones within riparian habitats.

Map of Southern Alberta illustrating riparian woodlands within each river system (shaded dots), sampling locations of the black-capped chickadee Poecile atricapillus (black dots; see Table 1 for abbreviations) and artificial barriers (i.e., river reservoirs represented as stars). Approximate boundaries of pure and hybrid poplar zones (not to scale) are denoted by the dashed lines and corresponding colours (see legend).

Fig 2. Individual assignment to K clusters based on the Bayesian clustering program, STRUCTURE.

Inferred population structure of the black-capped chickadee (Poecile atricapillus) from 12 microsatellite loci. Runs were conducted for two values of K, but the optimal number of clusters to describe the data was unclear. The initial run (a) for all individuals from 28 localities resulted in contrasting values of true K: (i) K = 2 (ΔK) and ii) K = 3 (LnPr (X|K)). After choosing K = 2 as the true value, we removed the genetic cluster containing LE, StM and WO and did a second run (b) which produced contrasting results: (i) K = 2 (ΔK) and ii) K = 3 (LnPr (X|K)). Due to mixed assignment of NSK and BO at K = 3, we chose K = 2 as the true value. No additional structure was identified after removing population SSK. Overall, STRUCTURE identified three genetic clusters (cluster 1: LE, StM and WO; cluster 2: SSK and cluster 3: all remaining populations).

Fig 3. Inferred genetic clusters from STRUCTURE.

Sampling locations (See Table 1 for abbreviations and associated river systems) with inferred clusters from STRUCTURE (coloured circles; K = 3; see Fig 2). Inset illustrates forest cover in the area (dark grey = forest; light grey = grassland).

Fig 4. Genetic similarity inferred by discriminant analysis of principal components (DAPC).

A representation of genetic relatedness between geographical clusters of black-capped chickadee populations (N = 15) obtained by DAPC. The graphs represent individuals as dots and the populations as inertia ellipses (population abbreviations can be found in Table 1) and scatterplots are based on the first two principal components. Populations with N ≤ 5 were excluded.