Post-glacial colonization of the Fennoscandian coast by a plant parasitic insect with an unusual life history

Species that exhibit very peculiar ecological traits combined with limited dispersal ability pose a challenge to our understanding of ecological and evolutionary mechanisms. This is especially true when they have managed to spread over long distances, overcome physical barriers and colonise large areas. Climate and landscape changes, trophic web relations as well as life history all interact to shape migration routes and present-day species distributions and their population genetic structures. Here we analysed the post-glacial colonization of northern Europe by the gall midge Contarinia vincetoxici, which is a monophagous parasite on the perennial herb White swallowwort (Vincetoxicum hirundinaria). This insect not only has a narrow feeding niche but also limited dispersal ability and an exceptionally long dormancy. Gall midge larvae (n = 329) were collected from 16 sites along its distribution range in Denmark, Sweden, and Finland. Using microsatellite loci and knowledge of the species and the regions’ history, we investigated the role of landscape change, host plant distribution, insect population dynamics, and life history in shaping the population genetic structure of the insect. We devoted particular interest to the role of the insect’s presumed poor dispersal capacity in combination with its exceptionally extended diapause. We found significant levels of local inbreeding (95% highest posterior density interval = 0.42–0.47), low level within-population heterozygosity (mean HE = 0.45, range 0.20–0.61) with private alleles in all populations except two. We also found significant (p < 0.001) regional isolation-by-distance patterns, suggesting regularly recurring mainly short-distance dispersal. According to approximate Bayesian computations, C. vincetoxici appears to have colonized the study area via wind-aided flights from remote areas approximately 4600 to 700 years before present when the land has gradually risen above the sea level. Extremely long dormancy periods have allowed the species to “disperse in time”, thereby aiding population persistence despite generally low census population sizes.

兼具独特生态特征与有限扩散能力的物种，对生态与进化机制的研究构成了挑战。尤其当这类物种能够完成长距离扩散、跨越物理屏障并占据大面积分布区时，这一挑战更为显著。气候与景观变化、食物网关系以及生活史特征共同作用，塑造了物种的迁徙路径、现今分布格局及其种群遗传结构。本研究以寄生于多年生草本植物白鹅绒藤（Vincetoxicum hirundinaria）的单食性寄生瘿蚊（gall midge）康塔瘿蚊（Contarinia vincetoxici）为对象，分析其在北欧的冰后殖民历程。该昆虫不仅取食生态位狭窄，还具备有限的扩散能力与极长的滞育期。研究人员在丹麦、瑞典与芬兰的物种分布范围内的16个采样点，共采集到329头瘿蚊幼虫。本研究利用微卫星位点（microsatellite loci），结合该物种的生物学特性与研究区域的历史背景，探究了景观变化、寄主植物分布、昆虫种群动态以及生活史特征对该昆虫种群遗传结构的塑造作用。我们重点关注了该昆虫被认为较弱的扩散能力与其极长滞育期的协同效应。研究结果显示，该物种存在显著的局部近交现象（95%最高后验密度区间为0.42~0.47）；种群内杂合度水平较低（平均期望杂合度HE=0.45，范围0.20~0.61），除两个种群外其余所有种群均携带私有等位基因。同时，我们检测到显著的区域距离隔离模式（p < 0.001），表明该物种的扩散以频繁发生的短距离扩散为主。基于近似贝叶斯计算（approximate Bayesian computations）结果，康塔瘿蚊（C. vincetoxici）大约在距今4600至700年前，随着陆地逐渐抬升出海面，通过风力辅助的远程飞行从偏远地区殖民至本研究区域。极长的滞育期使得该物种能够实现“时间上的扩散”，即便种群普查数量普遍较低，也有助于种群维持存续。