Multigenerational hybridisation results in heterosis and facilitates adaptive introgression, with no evidence of outbreeding depression in a pair of marine gastropods

Anthropogenic environmental changes continue to threaten species globally. For example, translocation of species has caused unintentional hybridisation, which has contributed to species declines. On the other hand, hybridisation can be used to increase the evolutionary potential of species vulnerable to rapid environmental change, although the benefits of mixing genetically divergent lineages do not come without risks to individual fitness and the long-term viability of populations. Here, we use a combination of genome-wide Single Nucleotide Polymorphism (SNP) markers, mitochondrial DNA sequencing and measurements of growth rate to determine the genetic consequences of hybridisation between two congeneric marine gastropods across 27 years (~ 18 generations). Multigeneration hybridisation resulted from the introduction of the intertidal periwinkle Bembicium vittatum (a direct developer) into the native range of its congener Bembicium auratum (a species with planktotrophic larval dispersal). Despite significant genetic divergence between the species, we found no direct evidence of outbreeding depression in the admixed population. Instead, we found evidence for heterosis, which dissipated over time. After an initial lag, the frequency of introduced B. vittatum alleles declined dramatically in the hybrid population. However, a few B. vittatum alleles (3.18%) increased significantly in frequency against the overall trend, providing evidence of adaptive introgression. In the context of hybridisation as a conservation management tool, our results provide some evidence of the potential benefits that can be gained, and suggest that the costs due to outbreeding depression can be small.

人为驱动的环境变化正持续威胁全球范围内的物种种群。例如，物种的人为易地迁移引发了无意杂交，这一过程进一步加剧了物种种群的衰退。另一方面，杂交可用于提升易受快速环境变化影响的物种种群的进化潜力，尽管融合遗传分化谱系所能带来的益处，并非不会对个体适合度及种群长期存续能力构成风险。本研究结合全基因组单核苷酸多态性（Single Nucleotide Polymorphism, SNP）标记、线粒体DNA测序技术以及生长速率测定方法，对27年（约18个世代）内两种同属海洋腹足类的杂交事件所产生的遗传后果展开解析。该多世代杂交事件源于潮间带滨螺Bembicium vittatum（直接发育型物种）被引入至同属物种Bembicium auratum（具有浮游营养型幼虫扩散特性）的原生分布区。尽管这两个物种间存在显著的遗传分化，但我们未在混合种群中发现远交衰退（outbreeding depression）的直接证据。相反，我们观测到杂种优势（heterosis）的存在，且该优势随时间推移逐渐消退。在经历初始滞后阶段后，引入的B. vittatum等位基因在杂交种群中的频率出现大幅下降。然而，占比3.18%的少数B. vittatum等位基因却逆势显著提升了频率，这为适应性基因渐渗（adaptive introgression）提供了实证依据。在将杂交作为物种保育管理手段的背景下，本研究结果为其潜在收益提供了一定的实证支持，并表明远交衰退所带来的成本可能较为有限。