Program in Ecology, Department of Zoology and Physiology, University of Wyoming, 1000 East University Avenue, Laramie, WY 82071, USA.
Proc Biol Sci. 2019 Aug 14;286(1908):20190761. doi: 10.1098/rspb.2019.0761. Epub 2019 Jul 31.
Cultural evolution may accelerate population divergence and speciation, though most support for this hypothesis is restricted to scenarios of allopatric speciation driven by random cultural drift. By contrast, the role of cultural evolution in non-allopatric speciation (i.e. speciation with gene flow) has received much less attention. One clade in which cultural evolution may have figured prominently in speciation with gene flow includes the conifer-seed-eating finches in the red crossbill (Loxia curvirostra) complex. Here we focus on Cassia crossbills (Loxia sinesciuris; an ecotype recently split taxonomically from red crossbills) that learn social contact calls from their parents. Previous work found that individuals modify their calls throughout life such that they become increasingly divergent from a closely related, sympatric red crossbill ecotype. This open-ended modification of calls could lead to character displacement if it causes population-level divergence in call structure that, in turn, reduces (maladaptive) heterospecific flocking. Heterospecific flocking is maladaptive because crossbills use public information from flockmates to assess resource quality, and feeding rates are depressed when flockmates differ in their ability to exploit a shared resource (i.e. when flockmates are heterospecifics). We confirm the predictions of character displacement by documenting substantial population-level divergence in Cassia crossbill call structure over just two decades and by using field experiments to demonstrate that Cassia and red crossbills differentially respond to these evolved differences in call structure, reducing heterospecific flock formation. Moreover, because crossbills choose mates from within flocks, a reduction in heterospecific flocking should increase assortative mating and may have been critical for speciation of Cassia crossbills in the face of ongoing gene flow in as few as 5000 years. Our results provide evidence for a largely neglected yet potentially widespread mechanism by which reproductive isolation can evolve between sympatric lineages as a byproduct of adaptive cultural evolution.
文化进化可能会加速种群的分歧和物种形成，但大多数对该假说的支持仅限于由随机文化漂移驱动的异域物种形成情景。相比之下，文化进化在非异域物种形成（即有基因流动的物种形成）中的作用受到的关注要少得多。一个文化进化可能在有基因流动的物种形成中起重要作用的分支包括红交嘴雀（Loxia curvirostra）复合体中的针叶树种子食雀。在这里，我们关注的是相思交嘴雀（Loxia sinesciuris；一个最近在分类上从红交嘴雀中分离出来的生态型），它们从父母那里学习社交联系叫声。以前的研究发现，个体在一生中会不断改变叫声，使它们与亲缘关系密切、同域的红交嘴雀生态型越来越不同。如果这种叫声的无限修改导致了叫声结构上的种群水平分歧，从而减少（适应不良的）异种种群聚集，那么这种修改就会导致性状替换。异种种群聚集是适应不良的，因为交嘴雀利用来自同伴的公共信息来评估资源质量，当同伴在利用共享资源的能力上存在差异时（即当同伴是异种种群时），觅食率会下降。我们通过记录在短短二十年内相思交嘴雀叫声结构的大量种群水平分歧，以及通过野外实验证明相思交嘴雀和红交嘴雀对这些叫声结构的进化差异有不同的反应，从而减少了异种种群的聚集，证实了性状替换的预测。此外，由于交嘴雀从群体中选择配偶，减少异种种群聚集应该会增加交配的选择性，并且在面对仅有 5000 年的持续基因流动时，可能对相思交嘴雀的物种形成至关重要。我们的研究结果为生殖隔离如何作为适应性文化进化的副产品在同域谱系之间进化提供了一个很大程度上被忽视但可能广泛存在的机制的证据。
