Rapid genetic restoration of a keystone species exhibiting delayed demographic response

Abstract

Genetic founder effects are often expected when animals colonize restored habitat in fragmented landscapes, but empirical data on genetic responses to restoration are limited. We examined the genetic response of banner-tailed kangaroo rats (Dipodomys spectabilis) to landscape-scale grassland restoration in the Chihuahuan Desert of New Mexico, USA. Dipodomys spectabilis is a grassland specialist and keystone species. At sites treated with herbicide to remove shrubs, colonization by D. spectabilis is slow and populations persist at low density for ≥10 years (≥6 generations). Persistence at low density and low gene flow may cause strong founder effects. We compared genetic structure of D. spectabilis populations between treated sites and remnant grasslands, and we examined how the genetic response to restoration depended on treatment age, area, and connectivity to source populations. Allelic richness and heterozygosity were similar between treated sites and remnant grasslands. Allelic richness at treated sites was greatest early in the restoration trajectory, and genetic divergence did not differ between recently colonized and established populations. These results indicated that founder effects during colonization of treated sites were weak or absent. Moreover, our results suggested founder effects were not mitigated by treatment area or connectivity. Dispersal is negatively density-dependent in D. spectabilis, and we hypothesize that high gene flow may occur early in the restoration trajectory when density is low. Our study shows genetic diversity can be recovered more rapidly than demographic components of populations after habitat restoration and that founder effects are not inevitable for animals colonizing restored habitat in fragmented landscapes.

Functional connectivity and home range inferred at a microgeographic landscape genetics scale in a desert‐dwelling rodent

“…However, desert landscapes are truly heterogeneous ecosystems where, among others, vegetation patches retain rainfall, resulting in a banded vegetation pattern tightly linked to topography and soil type (Grünberger, 2004;Ludwig, Wilcox, Breshears, Tongway, & Imeson, 2005). Notably, of the few LG studies done on desert ecosystems, fewer have been performed for mammal species, including big-sized and long dispersing mammals such as the bighorn sheep (Ovis canadensis nelsoni; Creech, Epps, Monello, & Wehausen, 2014a, 2014b), a small carnivore (Bassariscus astutus; Lonsinger, Schweizer, Pollinger, Wayne, & Roemer, 2015), and a desert rodent (Dipodomys spectabilis; Cosentino, Schooley, Bestelmeyer, McCarthy, & Sierzega, 2015), in which some landscape features like vegetation and elevation influenced gene flow.…”

Making the connection: expanding the role of restoration genetics in restoring and evaluating connectivity

“…To better integrate connectivity into restoration practice, it is also important to explicitly evaluate the impacts of restoration projects on genetic connectivity, not only during translocations (Aavik et al ; Reynolds et al ), but also in species that naturally recolonize restored habitat (Cosentino et al ; Isselin‐Nondedeu et al ; Mijangos et al ). When evaluating the restoration of habitat for connectivity, it is important to note that “gene flow” should be considered as the incorporation via reproduction of genes into another population; “movement” of genes alone is insufficient to realize the fitness benefits of gene flow.…”

“…These include identifying barriers to gene flow (McRae et al ) or spread of adaptive genetic variation (Apgar et al ); mapping gradients of adaptive variation in species (Shryock et al ); and setting genetic targets for restored populations that reflect diversity and connectivity in reference populations (Drury et al ). Connectivity of restored populations to the surrounding landscape is also becoming an important metric of restoration success, both for translocated (Aavik et al ; Reynolds et al ) and naturally recolonizing species (Cosentino et al ; Isselin‐Nondedeu et al ; Mijangos et al ). Given the rapid development of sequencing technology and analytical approaches to assessing genetic connectivity, and increasing interest in incorporating this into restoration genetics, we feel that it is timely to synthesize current and emerging genetic techniques that can support decision‐making in ecological restoration.…”