Seascape genomics of red abalone: Limited range-wide population structure and evidence for local adaptation

Characterizing patterns of genetic diversity including evidence of local adaptation is relevant for predicting and managing species recovering from over-exploitation in the face of climate change. Red abalone (Haliotis rufescens) is a species of conservation concern due to recent declines from over-harvesting, disease, and climate change, resulting in the closure of commercial and recreational fisheries. We hypothesized that the environmental mosaic that defines nearshore habitats in the California current ecosystem, including variable pH and temperature, has enriched some regions for locally adapted genotypes that may be important for species persistence in changing environments. Using whole genome re-sequencing data from 23 populations spanning their entire range (southern Oregon, USA, to Baja California, MEX) we investigated patterns of population connectivity and local adaptation. We discovered high genetic diversity that is shared within and among populations, suggesting high historical range-wide gene flow. Using multiple layers of environmental metadata, we tested for genotype-environment associations that would reveal local adaptation across the mosaic of coastal environments that define the California Current ecosystem. We found little evidence for large selective sweeps between populations that occupy local habitats that vary by pH, strength of upwelling, chlorophyll, salinity, and sea surface temperature. This is consistent with a broad range of species with similar life histories that show limited neutral or adaptive genetic variation across the same region and the same environments, suggesting that the mosaic of environmental variation across the CCS is insufficient to drive local adaptation in the face of high gene flow. Given the high genetic connectivity across their range, state-mandated regulatory actions would be most effective if aligned across jurisdictional boundaries (i.e., Mexico, California, and Oregon).

解析遗传多样性模式（包括本地适应相关证据），对于预测并管理在气候变化背景下因过度开发而复苏的物种种群具有重要意义。红鲍（Haliotis rufescens）因过度捕捞、病害与气候变化导致种群数量近期下降，商业与休闲渔业均已关停，因此该物种已被纳入保护关注名录。本研究提出假说：塑造加州海流生态系统（California Current Ecosystem, CCS）近岸生境的环境镶嵌体（包含pH与温度的波动），使得部分区域富集了本地适应型基因型，这类基因型对物种在变化环境中的存续至关重要。我们利用覆盖其整个分布范围（美国俄勒冈州南部至墨西哥下加利福尼亚州）的23个种群的全基因组重测序（whole genome re-sequencing）数据，解析了种群连通性与本地适应的模式。研究发现种群内部与种群间共享高水平的遗传多样性，这暗示历史上整个分布范围内存在高强度的基因流。我们借助多层环境元数据，开展了基因型-环境关联分析，以揭示加州海流生态系统所涵盖的沿海环境镶嵌体中的本地适应信号。我们未发现显著证据表明，在pH、上升流强度、叶绿素含量、盐度与海表面温度存在差异的本地生境的种群之间存在大规模选择性清除。这与众多具有相似生活史的物种的研究结果一致：这类物种在同一区域与相同环境中的中性或适应性遗传变异水平有限。这表明，在高基因流的背景下，加州海流生态系统的环境镶嵌变异不足以驱动本地适应。鉴于该物种整个分布范围内存在高强度的遗传连通性，若跨司法管辖区（即墨西哥、加利福尼亚州与俄勒冈州）协调实施州级法定监管措施，将能取得最佳管控效果。