Evolution and disappearance of sympatric Coregonus albula in a changing environment - a case study of the only remaining population pair in Sweden

During the past 50 years Fennoscandian populations of spring-spawning Baltic cisco (Coregonus albula), sympatric to common autumn-spawners, have declined or disappeared; e.g., three out of four known spring-spawning populations in Sweden are regarded as extinct. Over the same period, climate has changed and populations have been subject to other anthropogenic stressors. We compared historic (1960s) and recent (1990-2000s) morphological data from the still existent sympatric cisco populations in Lake Fegen, Sweden. Phenotypic changes were found for spring-spawners making them more similar to the sympatric autumn-spawners (that had remained virtually unchanged). Based on results for other salmoniform fishes, a phenotypically plastic response to increased temperature during early development appears unlikely. The recent material was also analysed with microsatellite markers; long-term effective population size in spring-spawners was estimated to be about 20 times lower than autumn-spawners, with signs of long-term gene flow in both directions and a recent genetic bottleneck in spring-spawners. The change towards a less distinct phenotype in spring-spawners is suggested to reflect a recent increase in gene flow from autumn-spawners. Time since divergence was estimated to only c. 1 900 years (95% CI: 400 – 5 900), but still the Fegen populations represent the most morphologically and genetically distinct sympatric populations studied. Consequently, we hypothesise that less distinct population pairs can be even younger, and that spring-spawning may have repeatedly evolved and disappeared in several lakes since the end of the last glaciation, concurrent with changed environmental conditions.

Methods
Please refer to Material and Methods in Delling & Palm (Ecology and Evolution 2019;9:12727-12753).

过去50年间，与普通秋季产卵波罗的海欧白鲑（Coregonus albula）同域分布（sympatric）的芬诺斯坎迪亚（Fennoscandian）春季产卵种群数量持续下降乃至灭绝；例如，瑞典已知的4个春季产卵种群中，已有3个被确认灭绝。同期，区域气候发生显著变化，这些种群还承受了其他人为胁迫因子的影响。

本研究对比了瑞典费根湖（Lake Fegen）现存同域分布白鲑种群的历史（1960年代）与近期（1990-2000年代）形态学数据。结果显示，春季产卵种群出现表型分化改变，使其与几乎未发生显著变化的同域秋季产卵种群愈发相似。结合其他鲑形目鱼类的相关研究结果，春季产卵种群在早期发育阶段对温度升高的表型可塑性（phenotypic plasticity）响应，似乎并非上述表型变化的成因。

研究团队同时利用微卫星标记（microsatellite markers）对近期采集的样本进行遗传分析；结果表明，春季产卵种群的长期有效种群规模（effective population size）约为秋季产卵种群的1/20，双向均存在长期基因交流信号，且春季产卵种群近期出现了遗传瓶颈（genetic bottleneck）效应。本研究推测，春季产卵种群表型分化程度降低的现象，反映了秋季产卵种群向其的基因交流在近期有所增加。

种群分化时间估算仅约1900年（95%置信区间：400–5900年），但费根湖的两个种群仍是目前已研究的同域分布种群中，形态与遗传分化最为显著的类群。据此我们提出假说：分化程度更低的种群其分化时间可能更短，且自末次冰期结束以来，随着环境条件改变，春季产卵习性可能在多个湖泊中反复演化并消失。

方法：具体实验方法请参见Delling与Palm发表于《Ecology and Evolution》2019年第9卷，第12727-12753页的《材料与方法》。