Evolution and plasticity: divergence of song discrimination is faster in birds with innate song than in song learners in Neotropical passerine birds

Plasticity is often thought to accelerate trait evolution and speciation. For example, plasticity in birdsong may partially explain why clades of song learners are more diverse than related clades with innate song. This “song learning” hypothesis predicts that 1) differences in song traits evolve faster in song learners, and 2) behavioral discrimination against allopatric song (a proxy for premating reproductive isolation) evolves faster in song learners. We tested these predictions by analyzing acoustic traits and conducting playback experiments in allopatric Central American sister pairs of song learning oscines (N = 42) and non-learning suboscines (N = 27). We found that non-learners evolved mean acoustic differences slightly faster than did leaners, and that the mean evolutionary rate of song discrimination was 4.3 times faster in non-learners than in learners. This unexpected result may be a consequence of significantly greater variability in song traits in song learners (by 54–79%) that requires song-learning oscines to evolve greater absolute differences in song before achieving the same level of behavioral song discrimination as non-learning suboscines. This points to “a downside of learning” for the evolution of species discrimination, and represents an important example of plasticity reducing the rate of evolution and diversification by increasing variability.

表型可塑性 (Plasticity) 通常被认为可加速性状进化 (trait evolution) 与物种形成 (speciation)。例如，鸟类鸣啭的可塑性或许可部分解释为何鸣啭学习者 (song learners) 支系 (clades) 的多样性高于具有先天鸣啭 (innate song) 的近缘支系。这一“鸣啭学习假说 (song learning hypothesis)”可推导出两项预测：其一，鸣啭学习者的鸣啭性状 (song traits) 差异演化速率更快；其二，鸣啭学习者针对异域鸣啭 (allopatric song)——交配前生殖隔离 (premating reproductive isolation) 的替代指标——的行为识别 (behavioral discrimination) 演化速率更快。

我们通过分析声学性状 (acoustic traits) 并开展回放实验 (playback experiments)，对上述预测展开检验。研究对象为中美洲的异域姊妹类群，涵盖鸣啭学习鸣禽（鸣禽亚目 (Oscines)，N=42）与非学习鸣禽（霸鹟亚目 (Suboscines)，N=27）两类。

研究结果出乎意料：非学习鸣禽的平均声学性状差异演化速率略快于鸣啭学习者；而鸣啭辨别的平均演化速率在非学习鸣禽中是鸣啭学习者的4.3倍。这一意外结果或源于鸣啭学习者的鸣啭性状变异程度显著更高（较非学习鸣禽高出54%~79%），使得鸣啭学习鸣禽需演化出更大的鸣啭绝对差异，才能达到与非学习鸣禽同等的鸣啭行为辨别水平。

该发现揭示了“学习对物种辨别演化的不利一面”，同时也是可塑性通过增加变异降低演化速率与物种多样化速率的重要例证。