Fixation of genetic variation and optimization of gene expression: The speed of evolution in isolated lizard populations undergoing Reverse Island Syndrome

The ecological theory of island biogeography suggests that mainland populations should be more genetically divergent from those on large and distant islands rather than from those on small and close islets. Some island populations do not evolve in a linear way, but the process of divergence occurs more rapidly because they undergo a series of phenotypic changes, jointly known as the Island Syndrome. A special case is Reversed Island Syndrome (RIS), in which populations show drastic phenotypic changes both in body shape, skin colouration, age of sexual maturity, aggressiveness, and food intake rates. The populations showing the RIS were observed on islets nearby mainland and recently raised, and for this they are useful models to study the occurrence of rapid evolutionary change. We investigated the timing and mode of evolution of lizard populations adapted through selection on small islets. For our analyses, we used an ad hoc model system of three populations: wild-type lizards from the mainland and insular lizards from a big island (Capri, Italy), both Podarcis siculus siculus not affected by the syndrome, and a lizard population from islet (Scopolo) undergoing the RIS (called P. s. coerulea because of their melanism). The split time of the big (Capri) and small (Scopolo) islands was determined using geological events, like sea-level rises. To infer molecular evolution, we compared five complete mitochondrial genomes for each population to reconstruct the phylogeography and estimate the divergence time between island and mainland lizards. We found a lower mitochondrial mutation rate in Scopolo lizards despite the phenotypic changes achieved in approximately 8,000 years. Furthermore, transcriptome analyses showed significant differential gene expression between islet and mainland lizard populations, suggesting the key role of plasticity in these unpredictable environments.

岛屿生物地理学（island biogeography）理论指出，大陆种群与大型偏远岛屿种群的遗传分化程度，应高于其与小型近岸小岛种群的遗传分化程度。部分岛屿种群的演化并非呈线性模式，其分化进程反而更为迅速——这是由于它们经历了一系列表型变化，这类变化被统称为岛屿综合征（Island Syndrome）。其中一类特殊亚型为反转岛屿综合征（Reversed Island Syndrome, RIS），罹患该综合征的种群会在体型、皮肤着色、性成熟年龄、攻击性以及食物摄入速率等多方面出现显著的表型改变。目前已观测到的呈现反转岛屿综合征的种群，均分布于大陆附近的新近形成小岛，因此这类种群可作为研究快速演化发生机制的理想模型。本研究针对小型岛屿上经自然选择适应的蜥蜴种群的演化时序与模式展开探究。本次分析采用了一套特设模型系统，包含三组种群：分别为源自大陆的野生型蜥蜴、来自大型岛屿（意大利卡普里岛，Capri）的岛屿蜥蜴，二者均为未受岛屿综合征影响的意大利壁蜥指名亚种（Podarcis siculus siculus）；以及来自小岛斯科波洛（Scopolo）、表现出反转岛屿综合征的蜥蜴种群——该种群因黑化现象被命名为P. s. coerulea。研究通过海平面上升等地质事件，确定了大型岛屿卡普里（Capri）与小型岛屿斯科波洛（Scopolo）的分化时间。为推断分子演化历程，我们对每个种群的5套完整线粒体基因组（mitochondrial genome）进行比对，以重建系统地理学格局并估算岛屿蜥蜴与大陆蜥蜴的分化时间。研究发现，尽管斯科波洛蜥蜴仅用约8000年便完成了表型适应性演化，但其线粒体突变率却更低。此外，转录组（transcriptome）分析显示，小岛种群与大陆蜥蜴种群间存在显著的差异基因表达（differential gene expression），这表明表型可塑性在这类多变环境中发挥了关键作用。