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.气候变化对存在相互作用的营养级的季节事件发生时序产生了差异化影响，这通常会加剧针对季节发生时序的选择压力。然而，驱动此类选择的环境变量却鲜有被识别，这限制了我们预测气候变化未来生态影响的能力。本研究使用一套覆盖31年时长、源自天然斑姬鹟（Ficedula hypoleuca）种群的数据集，结果显示，繁殖时间所受的定向选择（directional selection）在1980年至2000年的前两个十年间有所增强，但在2001年至2010年的最后一个十年间出现减弱。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不匹配（phenological mismatch）的时间变化来解释。为此我们探索了另一项假说：繁殖时间所受的选择压力，会受到个体春季抵达繁殖地时所经历的环境条件的影响——在低温条件下提早抵达可能会降低个体存活率。其一，我们发现，雌性招募（recruitment）个体在首次繁殖年份的春季抵达日期与出雏日期呈正相关，因此早出雏的个体在抵达繁殖地时，比晚出雏的个体经历更为寒冷的环境条件。其二，我们发现，当招募年春季抵达时的温度较高时，早出雏的幼鸟的招募概率（recruitment probability）要高于抵达温度较低的情况。我们将上述结果解读为寒冷年份提早抵达的潜在代价，而气候变暖可能已经降低了这一代价。由此可见，招募个体抵达年份的更高温度，与这些鸟类出生年份中更强的提早繁殖选择压力相关。随着研究初期的抵达温度有所升高，但近期又再度下降，繁殖时间的定向选择呈现出非线性变化。本研究证明，具有长达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。