Rapid genetic restoration of a keystone species exhibiting delayed demographic response

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. D. 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 yrs (≥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.

在破碎化景观中，动物定植于恢复生境时通常会出现遗传奠基者效应（genetic founder effects），但有关生境恢复的遗传响应的实证数据仍较为匮乏。本研究以美国新墨西哥州奇瓦瓦沙漠中的旗尾更格卢鼠（Dipodomys spectabilis）为研究对象，探究其对景观尺度草原恢复的遗传响应。该物种为草原特化种，同时也是关键物种。在喷施除草剂以清除灌木的处理样地中，旗尾更格卢鼠的定植过程较为缓慢，种群以低密度持续存在至少10年（即至少6个世代）。低密度持续存续与低基因流可能引发强烈的遗传奠基者效应。本研究对比了处理样地与原生草原中旗尾更格卢鼠种群的遗传结构，并探究了生境恢复的遗传响应如何受处理年限、样地面积以及与源种群连通性的影响。结果显示，处理样地与原生草原的等位基因丰富度与杂合度均无显著差异。处理样地的等位基因丰富度在恢复进程早期达到峰值，且新近定植种群与已存续种群间的遗传分化并无差异。上述结果表明，在处理样地定植过程中，遗传奠基者效应较弱甚至未出现。此外，本研究结果显示，样地面积与连通性并未缓解遗传奠基者效应的发生。旗尾更格卢鼠的扩散行为具有负密度依赖特征，据此我们推测，在恢复进程早期种群密度较低时，可能会出现较高的基因流。本研究表明，生境恢复后，种群遗传多样性的恢复速度快于种群统计组分，且在破碎化景观中，动物定植恢复生境时并非必然会出现遗传奠基者效应。