Behavioural foundation of a massive mitochondrial introgression in the fire salamander, Salamandra salamandra

Patterns of mito-nuclear discordance across secondary contact zones have been reported in a wide range of organisms. They consist of a spatial mismatch between nuclear and mitochondrial genomes, in terms of geographic location and/or extension of the contact zone between distinct evolutionary lineages. Several theoretical and empirical studies have identified massive mitochondrial introgression as putative source of these mismatches. Yet, we still lack a clear understanding of the phenotypic underpinnings of such massive introgression. We hypothesised that mtDNA variation across a contact zone could be associated with variation in phenotypic traits affecting dispersal propensity. We analysed patterns of behavioural and genetic variation across a mtDNA secondary contact zone of the fire salamander Salamandra salamandra in central Italy, which is over 600 km displaced from its nuclear counterpart. We found distinct behavioural profiles associated with the two co-occurring mitotypes. Counterintuitively, the introgressed mitotype was associated to a ‘slow-thorough’ dispersal profile, characterized by shy, less active and less exploratory personality traits. This pattern was consistent across life-stages and contexts, i.e., aquatic larvae and terrestrial juveniles. These results provide for the first time robust evidence that personality traits associated with distinct mitotypes could promote differential mitochondrial introgression within alternative nuclear backgrounds.诸多生物类群的次生接触带中均已报道有线粒体-核基因组不协调（mito-nuclear discordance）模式。此类模式体现为核基因组与线粒体基因组之间的空间错配，具体表现为不同演化支间的接触带在地理位置与/或分布范围上存在差异。多项理论与实证研究已将大规模线粒体基因渐渗（mitochondrial introgression）认定为这类错配现象的推测成因。然而，学界目前仍未明确此类大规模基因渐渗背后的表型基础。本研究提出假说：接触带内的线粒体DNA（mtDNA）变异，可能与影响个体扩散倾向的表型性状变异存在关联。我们以意大利中部的火蝾螈（Salamandra salamandra）线粒体次生接触带为研究对象，分析了其行为与遗传变异模式——该接触带的分布范围较其核基因组对应的接触带偏移了600余公里。我们发现，与两种共存的线粒体型（mitotypes）相对应的行为特征存在显著差异。与直觉相悖的是，发生渐渗的线粒体型与“慢-审慎”型扩散策略相关联，该策略的个性特征表现为羞怯、活动量较低且探索性较弱。该模式在不同生活史阶段与环境背景下均保持一致，涵盖水生幼体与陆生幼体两类群体。本研究结果首次提供了可靠证据，表明与不同线粒体型相关联的个性特征，可在不同核基因组背景下推动差异化的线粒体基因渐渗过程。