Data from: Recurrent evolution of melanism in South American felids

Morphological variation in natural populations is a genomic test bed for studying the interface between molecular evolution and population genetics, but some of the most interesting questions involve non-model organisms that lack well annotated reference genomes. Many felid species exhibit polymorphism for melanism but the relative roles played by genetic drift, natural selection, and interspecies hybridization remain uncertain. We identify mutations of Agouti signaling protein (ASIP) or the Melanocortin 1 receptor (MC1R) as independent causes of melanism in three closely related South American species: the pampas cat (Leopardus colocolo), the kodkod (Leopardus guigna), and Geoffroy's cat (Leopardus geoffroyi). To assess population level variation in the regions surrounding the causative mutations we apply genomic resources from the domestic cat to carry out clone-based capture and targeted resequencing of 299 kb and 251 kb segments that contain ASIP and MC1R, respectively, from 54 individuals (13–21 per species), achieving enrichment of ~500–2500-fold and ~150x coverage. Our analysis points to unique evolutionary histories for each of the three species, with a strong selective sweep in the pampas cat, a distinctive but short melanism-specific haplotype in the Geoffroy's cat, and reduced nucleotide diversity for both ancestral and melanism-bearing chromosomes in the kodkod. These results reveal an important role for natural selection in a trait of longstanding interest to ecologists, geneticists, and the lay community, and provide a platform for comparative studies of morphological variation in other natural populations.

自然种群中的形态变异是研究分子进化与群体遗传学交叉领域的基因组测试平台（genomic test bed），但其中部分最具研究价值的问题聚焦于缺乏完善注释参考基因组的非模式生物。诸多猫科（felid）物种均存在黑化多态性，但遗传漂变、自然选择以及种间杂交各自所扮演的相对角色仍未明确。我们鉴定发现，刺豚鼠信号蛋白（Agouti signaling protein, ASIP）或黑皮质素1受体（Melanocortin 1 receptor, MC1R）的突变，是三种近缘南美物种黑化现象的独立诱因：潘帕斯猫（Leopardus colocolo）、南美林猫（Leopardus guigna）以及乔氏猫（Leopardus geoffroyi，又称Geoffroy's cat）。为评估致病突变侧翼区域的种群水平变异，我们借助家猫的基因组资源，对54个个体（每个物种13至21个）中分别包含ASIP与MC1R的299kb和251kb片段开展基于克隆的捕获及靶向重测序，分别实现了约500至2500倍的富集倍数与约150倍的测序覆盖度。我们的分析显示，这三个物种各自拥有独特的进化历程：潘帕斯猫经历了强烈的选择性清除（selective sweep），乔氏猫存在独特但长度较短的黑化特异性单倍型（haplotype），而南美林猫的祖先染色体与携带黑化性状的染色体均呈现核苷酸多样性降低的特征。上述研究结果揭示了自然选择在这一长期受到生态学家、遗传学家以及普通大众关注的性状中的重要作用，并为其他自然种群形态变异的比较研究提供了研究平台。