Urbanization impacts apex predator gene flow but not genetic diversity across an urban-rural divide

Apex predators are important indicators of intact natural ecosystems. They
are also sensitive to urbanization because they require broad home ranges
and extensive contiguous habitat to support their prey base. Pumas (Puma
concolor) can persist near human developed areas, but urbanization may be
detrimental to their movement ecology, population structure, and genetic
diversity. To investigate potential effects of urbanization in population
connectivity of pumas, we performed a landscape genomics study of 130
pumas on the rural Western Slope and more urbanized Front Range of
Colorado, USA. Over 12,000 single nucleotide polymorphisms were genotyped
using double-digest, restriction site-associated DNA sequencing
(ddRADseq). We investigated patterns of gene flow and genetic diversity,
and tested for correlations between key landscape variables and genetic
distance to assess the effects of urbanization and other landscape factors
on gene flow. Levels of genetic diversity were similar for the Western
Slope and Front Range, but effective population sizes were smaller,
genetic distances were higher, and there was more admixture in the more
urbanized Front Range. Forest cover was strongly positively associated
with puma gene flow on the Western Slope, while impervious surfaces
restricted gene flow and more open, natural habitats enhanced gene flow on
the Front Range. Landscape genomic analyses revealed differences in puma
movement and gene flow patterns in rural versus urban settings. Our
results highlight the utility of dense, genome-scale markers to document
subtle impacts of urbanization on a wide-ranging carnivore living near a
large urban center.

顶级捕食者（Apex predators）是完整自然生态系统的重要指示物种。它们对城市化也较为敏感，因为其需要广阔的家域与连续延展的栖息地以支撑自身的猎物种群。美洲狮（Puma concolor）能够在人类开发区域附近存续，但城市化可能会对其移动生态学、种群结构以及遗传多样性产生不利影响。为探究城市化对美洲狮种群连通性的潜在影响，我们针对美国科罗拉多州西部乡村坡地与城市化程度更高的前岭（Front Range）区域的130只美洲狮开展了景观基因组学研究。我们采用双酶切限制性位点相关DNA测序（double-digest, restriction site-associated DNA sequencing, ddRADseq）技术，对超过12000个单核苷酸多态性（single nucleotide polymorphisms）位点进行了基因分型。本研究分析了基因流与遗传多样性的分布模式，并检验了关键景观变量与遗传距离之间的相关性，以评估城市化及其他景观因子对基因流的影响。西部坡地与前岭区域的遗传多样性水平相近，但在城市化程度更高的前岭区域，有效种群规模更小、遗传距离更高，且遗传混合程度更强。在西部坡地，森林覆盖度与美洲狮的基因流呈显著正相关；而在前岭区域，不透水面会限制基因流，更为开阔的自然生境则会促进基因流。景观基因组学分析揭示了乡村与城市环境中美洲狮移动模式与基因流模式的差异。本研究结果证实了高密度基因组尺度标记在记录栖息于大型城市中心附近的活动范围广阔的食肉动物所受城市化细微影响方面的应用价值。