The evolution of eye size in response to increased fish predation in Daphnia

Variation in eye size is ubiquitous across taxa. Increased eye size is correlated with improved vision and increased fitness via shifts in behavior. Tests of the drivers of eye size evolution have focused on macroevolutionary studies evaluating the importance of light availability. Predator-induced mortality has recently been identified as a potential driver of eye size variation. Here we tested the influence of increased predation by the fish predator, the alewife (Alosa pseudoharengus) on eye size evolution in waterfleas (Daphnia ambigua) from lakes in Connecticut. We quantified the relative eye size of Daphnia from lakes with and without alewife using wild-caught and third generation laboratory reared specimens. This includes comparisons between lakes where alewife are present seasonally (anadromous) or permanently (landlocked). Wild-caught specimens did not differ in eye size across all lakes. However, third generation lab reared Daphnia from lakes with alewife, irrespective of the form of alewife predation, exhibited significantly larger eyes than Daphnia from lakes without alewife. This genetically based increase in eye size may enhance the ability of Daphnia to detect predators. Alternatively, such shifts in eye size may be an indirect response to Daphnia aggregating at the bottom of lakes. To test these mechanisms, we collected Daphnia as a function of depth and found that eye size differed in Daphnia found at the surface versus the bottom of the water column between anadromous alewife and no alewife lakes. However, we found no evidence of Daphnia aggregating at the bottom of lakes. Such results indicate that the evolution of a larger eye may be explained by a connection between eyes and enhanced survival. We discuss the cause of the lack of concordance in eye size variation between our phenotypic and genetic specimens and the ultimate drivers of eye size.

不同类群生物的眼大小变异普遍存在。眼体积增大与视觉功能提升及通过行为模式改变带来的适合度（fitness）提高呈正相关。以往针对眼大小进化驱动因素的研究，多聚焦于评估光照可获得性重要性的宏观进化研究（macroevolutionary studies）。近年来，捕食者诱导死亡率（predator-induced mortality）被认定为眼大小变异的潜在驱动因素之一。本研究以康涅狄格州湖泊中的歧义溞（Daphnia ambigua）为对象，检验了其捕食者西鲱（Alosa pseudoharengus）种群捕食压力增加对其眼大小进化的影响。我们分别利用野生捕获个体与实验室繁育三代的实验个体，量化了有西鲱与无西鲱湖泊中水蚤的相对眼大小，同时涵盖了西鲱为季节性溯河洄游型（anadromous）与永久性陆封型（landlocked）两类湖泊的对比。野生捕获个体的眼大小在所有调查湖泊中均无显著差异。但实验室繁育三代的个体中，来自有西鲱湖泊的水蚤，无论西鲱的捕食类型如何，其眼大小均显著大于来自无西鲱湖泊的个体。这种基于遗传基础的眼体积增大，或可提升歧义溞侦测捕食者的能力；此外，眼大小的这类变化也可能是水蚤聚集于湖底所产生的间接响应。为验证这两种潜在机制，我们按水深梯度采集水蚤，并对比了溯河洄游西鲱湖泊与无西鲱湖泊中，表层水体与湖底水体中水蚤的眼大小差异。但我们并未发现水蚤聚集于湖底的相关证据。上述结果表明，眼体积增大的进化现象，可通过眼睛功能与生存能力提升之间的关联得到解释。最后，我们讨论了本研究中表型个体与遗传繁育个体眼大小变异不一致的原因，以及眼大小进化的终极驱动因素。