Data: Rapid evolution of an adaptive taste polymorphism disrupts courtship behavior

The evolution of adaptive behavior often requires changes in sensory systems. However, rapid adaptive changes in sensory traits can adversely affect other fitness-related behaviors. In the German cockroach, a gustatory polymorphism, ‘glucose-aversion (GA)’, supports greater survivorship under selection with glucose-containing insecticide baits and promotes the evolution of behavioral resistance. Yet, sugars are prominent components of the male’s nuptial gift and play an essential role in courtship. Behavioral and chemical analyses revealed that the saliva of GA females rapidly degrades nuptial gift sugars into glucose, and the inversion of a tasty nuptial gift to an aversive stimulus often causes GA females to reject courting males. Thus, the rapid emergence of an adaptive change in the gustatory system supports foraging, but it interferes with courtship. The trade-off between natural and sexual selection under human-imposed selection can lead to directional selection on courtship behavior that favors the GA genotype.

适应性行为的演化通常需要感知系统发生相应改变。然而，感知性状的快速适应性改变，可能会对其他与适合度相关的行为产生不利影响。在德国小蠊中，存在一种名为“拒糖（glucose-aversion, GA）”的味觉多态性：该性状在含葡萄糖的杀虫剂诱饵的选择压力下，可提升种群存活率，并推动行为抗性的演化。但糖类是雄性求偶赠礼的核心组成成分，且在求偶过程中发挥关键作用。行为与化学分析结果显示，GA型雌性的唾液可快速将求偶赠礼中的糖类分解为葡萄糖；当原本美味的求偶赠礼转变为厌恶刺激时，GA型雌性常会拒绝前来求偶的雄性。由此可见，味觉系统中适应性改变的快速出现，虽有助于觅食活动，却会干扰求偶过程。在人为施加的选择压力下，自然选择与性选择之间的权衡取舍，可能会对求偶行为产生定向选择，进而青睐GA基因型。