A multi-scale analysis of gene flow for the New England cottontail, an imperiled habitat specialist in a fragmented landscape

Landscape features of anthropogenic or natural origin can influence organisms’ dispersal patterns and the connectivity of populations. Understanding these relationships is of broad interest in ecology and evolutionary biology and provides key insights for habitat conservation planning at the landscape scale. This knowledge is germane to restoration efforts for the New England cottontail (Sylvilagus transitionalis), an early-successional habitat specialist of conservation concern. We evaluated local population structure and measures of genetic diversity of a geographically isolated population of cottontails in the northeastern United States. We also conducted a multi-scale landscape genetic analysis, in which we assessed genetic discontinuities relative to the landscape and developed several resistance models to test hypotheses about landscape features that promote or inhibit cottontail dispersal within and across the local populations. Bayesian clustering identified four genetically distinct populations, with very little migration among them, and additional substructure within one of those populations. These populations had private alleles, low genetic diversity, critically low effective population sizes (3.2 -36.7), and evidence of recent genetic bottlenecks. Major highways and a river were found to limit cottontail dispersal and to separate populations. The habitat along roadsides, railroad beds and utility corridors, on the other hand, was found to facilitate cottontail movement among patches. The relative importance of dispersal barriers and facilitators on gene flow varied among populations in relation to landscape composition, demonstrating the complexity and context dependency of factors influencing gene flow and highlighting the importance of replication and scale in landscape genetic studies. Our findings provide information for the design of restoration landscapes for the New England cottontail and also highlight the dual influence of roads, as both barriers and facilitators of dispersal for an early-successional habitat specialist in a fragmented landscape.

人为或自然起源的景观特征，可影响生物的扩散模式与种群连通性。厘清此类关联是生态学与进化生物学领域的核心研究方向之一，同时可为景观尺度下的栖息地保护规划提供关键洞见。此类研究认知与受保护关注的早期演替栖息地特化物种——新英格兰棉尾兔（Sylvilagus transitionalis）的修复工作密切相关。本研究针对美国东北部一处地理隔离的棉尾兔种群，评估了其局域种群结构与多项遗传多样性指标。本研究同时开展了多尺度景观遗传学（landscape genetics）分析：首先评估了与景观格局相关的遗传不连续性，随后构建了多组抗性模型，用以检验关于调控棉尾兔在局域种群内部及跨种群间扩散的景观特征的相关假说。贝叶斯聚类（Bayesian clustering）分析共识别出4个遗传分化显著的种群，种群间迁移水平极低，且其中一个种群内部还存在额外的亚结构。这些种群均携带私有等位基因，遗传多样性水平偏低，有效种群大小极低（3.2~36.7），且存在近期发生遗传瓶颈的证据。研究发现，主要公路与一条河流会限制棉尾兔的扩散，并成为种群间的隔离屏障。而公路旁、铁路路基及公用设施廊道周边的栖息地，则被证实可促进棉尾兔在不同栖息地斑块间的移动。扩散屏障与促进因子对基因流的相对重要性会随种群所处的景观组成不同而发生变化，这既体现了调控基因流的各类因素的复杂性与情境依赖性，也凸显了重复研究与尺度选择在景观遗传学研究中的重要性。本研究结果可为新英格兰棉尾兔的修复性景观设计提供参考，同时也揭示了道路的双重作用：在破碎化景观中，道路既是早期演替栖息地特化物种扩散的屏障，亦是其扩散的促进通道。