Behavioral changes in a new environment are often assumed to precede the origins of evolutionary novelties. Here, we examined whether an increase in aggression is associated with a novel scale-eating trophic niche within a recent radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. We measured aggression using multiple behavioral assays and used transcriptomic analyses to identify differentially expressed genes in aggression and other behavioral pathways across 3 sympatric species in the San Salvador radiation (generalist, snail-eating specialist, and scale-eating specialist) and 2 generalist outgroups. Surprisingly, we found increased behavioral aggression and differential expression of aggression-related pathways in both the scale-eating and snail-eating specialists, despite their independent evolutionary origins. Increased behavioral aggression varied across both sex and stimulus context in both species. Our results indicate that aggression is not unique to scale-eating specialists. Instead, selection may increase aggression in other contexts such as niche specialization in general or mate competition. Alternatively, increased aggression may result from indirect selection on craniofacial traits, pigmentation, or metabolism-all traits which are highly divergent, exhibit signs of selective sweeps, and are affected by aggression-related genetic pathways which are differentially expressed in this system. In conclusion, the evolution of a novel predatory trophic niche within a recent adaptive radiation does not have clear-cut behavioral origins as previously assumed, highlighting the multivariate nature of adaptation and the complex integration of behavior with other phenotypic traits.

中文翻译：

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新奇的行为起源：攻击性的增加是否会导致鳉鱼吃鳞？

人们通常认为新环境中的行为变化先于进化新颖性的起源。在这里，我们研究了巴哈马圣萨尔瓦多岛特有的鲤鱼最近辐射中的攻击性增加是否与新的食鳞营养位有关。我们使用多种行为测定来测量攻击性，并使用转录组分析来识别圣萨尔瓦多辐射区 3 个同域物种（通才、吃蜗牛专家和吃鳞片专家）和 2 个通才外群的攻击性和其他行为途径的差异表达基因。令人惊讶的是，我们发现食鳞专家和食蜗牛专家的行为攻击性和攻击相关途径的差异表达有所增加，尽管它们具有独立的进化起源。在这两个物种中，攻击性行为的增加在性别和刺激环境中都存在差异。我们的研究结果表明，攻击性并不是食鳞专家所独有的。相反，选择可能会增加其他情况下的攻击性，例如一般情况下的利基专业化或配偶竞争。或者，攻击性的增加可能是由于对颅面特征、色素沉着或新陈代谢的间接选择造成的——所有这些特征都高度不同，表现出选择性清除的迹象，并受到该系统中差异表达的攻击性相关遗传途径的影响。总之，最近适应性辐射中新型捕食性营养生态位的进化并不像之前假设的那样具有明确的行为起源，凸显了适应的多元性质以及行为与其他表型特征的复杂整合。