Understanding how landscape features influence the connectivity and genetic variation of natural populations is of central importance in ecology, evolution, and conservation biology. Connectivity remains one of the most difficult parameters to measure, yet it is a critical issue to address in landscape conservation (Tischendorf and Fahrig 2000; Lindenmayer et al. 2008). From a species' perspective, connectivity is a function of the ability of an individual to disperse through the landscape. Characteristics of habitat patches and the intervening landscape matrix can either facilitate or impede dispersal success (e.g., Pérez-Espona et al. 2008). Because landscapes are spatially heterogeneous, and increasingly so as a result of human modifications, it is important to understand how landscape features affect animal movement and subsequent population processes.
Landscape influences on dispersal are determined by species-specific characteristics, including the organism's vagility and specific habitat requirements for dispersal. These factors determine the scale and extent to which specific landscape features influence population connectivity. For example, broadscale dispersal barriers may derive from natural landforms that are impassable, such as mountain ranges (Zalewski et al. 2009) or ocean trenches (Cunningham et al. 2009), and serve to completely separate populations. Local-scale or partial barriers are often formed by smaller landscape elements, such as roads (Coulon et al. 2006) or rivers (Frantz et al. 2010). The effects of these features can vary widely among species. Rivers may completely isolate populations of small mammals (Chambers and Garant 2010), but may be more permeable, at least under some circumstances, to larger mammals (Pérez-Espona et al. 2008; Cullingham et al. 2009) or even provide habitats conducive to dispersal (e.g., riparian corridors; Lowe and McPeek 2012). Similarly, roads, despite their recognized negative effects as barriers (Forman et al. 2003), may serve as movement corridors for some species for which associated habitat is conducive to dispersal (Crooks and Sanjayan 2006; Bissonette and Rosa 2009; Laurence et al. 2013). Linear landscape features may have complex influences on dispersal even within a single species, acting as both barriers and facilitators of dispersal. Anthropogenic changes in land cover can have further consequences for connectivity, as habitat loss and fragmentation can impede dispersal if the intervening matrix is prohibitive to a species' movement (e.g., Keyghobadi et al. 1999; Dixon et al. 2007). These consequences are more pronounced for species with high habitat specificity (Rothermel and Semlitsch 2002).
Disruption of habitat connectivity typically leads to genetic structuring among individuals, as a result of isolation (Segelbacher et al. 2003) and/or physical barriers to dispersal and concomitant gene flow (McRae et al. 2005). Reduced genetic exchange (i.e., fewer dispersing and subsequently reproducing individuals) among populations results in the gradual genetic divergence of populations through genetic drift and local adaptation (Willi et al. 2007) or, in the extreme, leads to population extinction (Bond et al. 2006). The consequences of reduced connectivity are especially relevant for species of conservation concern, which often exist in small, isolated patches and have limited dispersal and small effective population sizes (Ewers and Didham 2006). Small populations are more susceptible to stochastic events, as well as a loss of genetic diversity, which limits the population's ability to cope with environmental change (Templeton et al. 1990, 2001). In such cases, it is important to identify gene flow barriers that can be mitigated to increase effective dispersal. Improving connectivity helps maintain genetic diversity and increases effective population sizes, thereby strengthening the probability of population persistence (Newman and Pilson 1997; Frankham 2005; Bailey 2007). Additionally, recognizing landscape features that facilitate dispersal is necessary for species' recovery, so that those features can be maintained and replicated in habitat restoration efforts to increase connectivity and augment gene flow where needed.
Issues of connectivity are germane for organisms that rely on early successional and shrubland habitats. These ephemeral habitats occur in a landscape mosaic of habitats in varying successional stages, many of which are inhospitable to early successional habitat specialists. Although patchy by nature, the spatial configuration (abundance, patch size, and distribution) of early successional habitats has been modified by a loss of natural disturbance regimes, land use change, and anthropogenic landscape modifications. These habitats are on the decline in the northeastern United States, along with many species that rely on them (Brooks 2003; Litvaitis 2003; Lorimer and White 2003; Sauer et al. 2011). Consequently, early successional habitat specialists may face the consequences of habitat loss and fragmentation, including population isolation and decline, and concomitant reduction in genetic variation (Andren 1994; Fahrig 2003; Keyghobadi 2007).
One of the many shrubland obligate species of high conservation priority in the northeastern United States is the New England cottontail (Sylvilagus transitionalis; Fig. 1), which requires dense, brushy vegetation for food and escape cover (Litvaitis et al. 2003). Widespread habitat loss has resulted in rapid population decline for this species, and it now occupies less than 14% of its historical range (all New England states and eastern New York; Litvaitis et al. 2006). As a result, the New England cottontail is listed as endangered in Maine (MDIFW 2007) and New Hampshire (NHFG 2008), and it is a candidate for federal listing under the Endangered Species Act (USFWS 2006, 2012). Remnant populations of New England cottontail currently occur in five geographically (Litvaitis et al. 2006) and genetically (Fenderson et al. 2011) isolated regions: (1) southern Maine and Seacoast (southeastern) New Hampshire; (2) central New Hampshire; (3) Cape Cod, Massachusetts; (4) eastern Connecticut and Rhode Island; and (5) western Connecticut, western Massachusetts, and eastern New York. The current population structure is a result of recent habitat fragmentation (within the last several decades) and genetic stochasticity, as the populations have experienced genetic drift in isolation (Fenderson et al. 2011).
Given the lack of gene flow among the remaining populations of New England cottontails, conservation efforts must begin within each of these regions to ensure connectivity, stability, and population persistence on a local scale. New England cottontails in southern Maine and the Seacoast region of New Hampshire are in immediate need of restoration management. This region is at the northern extent of the species' range and is experiencing ongoing decline, with an estimated 50% reduction in effective population size occurring within the past two decades (Fenderson 2010) and reduced genetic diversity relative to other remnant populations (Fenderson et al. 2011). A census population size of roughly 300 individuals has been estimated to occur in southern Maine (Litvaitis and Jakubas 2004), and an effective population size of 75–150 has been estimated for the Maine and New Hampshire region (Fenderson et al. 2011). Extensive habitat loss and fragmentation have reduced the availability of suitable (thicket) habitat in this region, such that fewer and smaller habitat patches exist, separated by increasingly large geographic distances. Remaining habitat patches are typically small (2–35 ha, with most <5 ha) and fragmented by development and inhospitable habitat. Recovery of the New England cottontail in the Maine and Seacoast New Hampshire region will require increasing available suitable habitat to support patch occupancy, as well as increasing connectivity among remaining patches. These efforts require an understanding of current landscape influences on gene flow.
The objectives of our study were threefold: (1) to assess local population genetic structure and diversity of New England cottontails in southern Maine and coastal New Hampshire; (2) to identify landscape features that are influential in structuring populations through promoting or inhibiting connectivity within and among these populations; and (3) to test hypotheses about the influence of landscape features (identified in #2) on gene flow. Specifically, we evaluated the effects of geographic distance, roads, waterbodies, and linear features comprised of early successional habitat, such as utility lines and roadsides, on gene flow. We expected to find fine-scale population structure resulting from the separation of populations by fragmentation and/or dispersal barriers. We hypothesized that landscape features have a stronger influence on genetic variation within and among populations than geographic distance alone. We also predicted that roads and waterbodies would function as dispersal barriers, while linear shrubby habitat features (railroads, powerline rights-of-way, and roadsides) would facilitate gene flow. Our results provide key information for the design of restoration landscapes that enhance connectivity for the New England cottontail and thereby likely also benefit other species that rely on early successional habitats. Our findings also illustrate the complexity of natural and anthropogenic factors influencing gene flow of a habitat specialist in a fragmented landscape.