Effects of spring temperatures on the strength of selection on timing of reproduction in a long-distance migratory bird

Climate change has differentially affected the timing of seasonal events for interacting trophic levels, and this has often led to increased selection on seasonal timing. Yet, the environmental variables driving this selection have rarely been identified, limiting our ability to predict future ecological impacts of climate change. Using a dataset spanning 31 years from a natural population of pied flycatchers (Ficedula hypoleuca), we show that directional selection on timing of reproduction intensified in the first two decades (1980–2000) but weakened during the last decade (2001–2010). Against expectation, this pattern could not be explained by the temporal variation in the phenological mismatch with food abundance. We therefore explored an alternative hypothesis that selection on timing was affected by conditions individuals experience when arriving in spring at the breeding grounds: arriving early in cold conditions may reduce survival. First, we show that in female recruits, spring arrival date in the first breeding year correlates positively with hatch date; hence, early-hatched individuals experience colder conditions at arrival than late-hatched individuals. Second, we show that when temperatures at arrival in the recruitment year were high, early-hatched young had a higher recruitment probability than when temperatures were low. We interpret this as a potential cost of arriving early in colder years, and climate warming may have reduced this cost. We thus show that higher temperatures in the arrival year of recruits were associated with stronger selection for early reproduction in the years these birds were born. As arrival temperatures in the beginning of the study increased, but recently declined again, directional selection on timing of reproduction showed a nonlinear change. We demonstrate that environmental conditions with a lag of up to two years can alter selection on phenological traits in natural populations, something that has important implications for our understanding of how climate can alter patterns of selection in natural populations.

气候变化对存在互作关系的不同营养级类群的季节事件发生时序产生了差异化影响，且该现象通常会加剧针对季节活动时序的选择压力。然而，驱动这类选择压力的环境变量却鲜有被探明，这限制了我们预测气候变化未来生态影响的能力。本研究基于取自斑姬鹟（Ficedula hypoleuca）自然种群、跨度达31年的数据集开展分析，结果显示：针对繁殖时序的定向选择在1980–2000年的前两个十年间有所增强，但在2001–2010年的最后一个十年间有所减弱。与预期相悖的是，这一模式无法通过与食物丰度相关的物候错配的时间变化来解释。为此我们提出了一项替代性假说：繁殖时序所受的选择压力，取决于个体春季抵达繁殖地时所经历的环境条件——在寒冷条件下提早抵达可能会降低个体存活率。首先，研究发现，雌性补充个体在首个繁殖季的春季抵达日期与其孵化日期呈正相关；因此，早孵化个体抵达繁殖地时所经历的气温要低于晚孵化个体。其次，研究表明，在补充种群当年的抵达气温较高时，早孵化幼鸟的补充概率要高于抵达气温较低时的情况。我们将这一现象解读为寒冷年份提早抵达的潜在代价，而气候变暖或许已降低了这一代价。由此可见，在幼鸟出生的年份里，补充个体抵达繁殖地当年的气温越高，针对提早繁殖的定向选择就越强。随着研究初期的抵达气温有所上升，但近期再度下降，针对繁殖时序的定向选择呈现出非线性变化趋势。本研究证实，存在至多两年滞后效应的环境条件，能够改变自然种群中物候性状所受的选择压力——这一发现对于我们理解气候如何改变自然种群的选择模式具有重要意义。