Neurobiology Section, Division of Biological Sciences, University of California, San Diego, La Jolla, CA 92093, USA.
Department of Biology, Duke University, Durham, NC 27708, USA; Department of Neurobiology, Duke University, Durham, NC 27708, USA.
Curr Biol. 2019 Nov 18;29(22):3887-3898.e4. doi: 10.1016/j.cub.2019.09.045. Epub 2019 Oct 31.
Critical to evolutionary fitness, animals regulate social behaviors by integrating signals from both their external environments and internal states. Here, we find that population density modulates the courtship behavior of male Drosophila melanogaster in an age-dependent manner. In a competitive mating assay, males reared in a social environment have a marked advantage in courting females when pitted against males reared in isolation. Group housing promotes courtship in mature (7-day) but not immature (2-day) males; this behavioral plasticity requires the Or47b pheromone receptor. Using single-sensillum recordings, we find that group housing increases the response of Or47b olfactory receptor neurons (ORNs) only in mature males. The effect of group housing on olfactory response and behavior can be mimicked by chronically exposing single-housed males to an Or47b ligand. At the molecular level, group housing elevates Ca levels in Or47b ORNs, likely leading to CaMKI-mediated activation of the histone-acetyl transferase CBP. This signaling event in turn enhances the efficacy of juvenile hormone, an age-related regulator of reproductive maturation in flies. Furthermore, the male-specific Fruitless isoform (Fru) is required for the sensory plasticity, suggesting that Fru functions as a downstream genomic coincidence detector in Or47b ORNs-integrating reproductive maturity, signaled by juvenile hormone, and population density, signaled by CBP. In all, we identify a neural substrate and activity-dependent mechanism by which social context can directly influence pheromone sensitivity, thereby modulating social behavior according to animals' life-history stage.
动物通过整合来自外部环境和内部状态的信号来调节社会行为，这对其进化适应至关重要。在这里，我们发现种群密度以年龄依赖的方式调节黑腹果蝇雄蝇的求偶行为。在竞争性交配实验中，与单独饲养的雄蝇相比，在社交环境中饲养的雄蝇在求偶时具有明显的优势。群体饲养促进了成熟（7 天）但不促进未成熟（2 天）雄蝇的求偶行为；这种行为可塑性需要 Or47b 信息素受体。通过单感器记录，我们发现群体饲养仅增加了成熟雄蝇中 Or47b 嗅觉受体神经元（ORNs）的反应。群体饲养对嗅觉反应和行为的影响可以通过慢性暴露于 Or47b 配体来模拟单养雄蝇。在分子水平上，群体饲养提高了 Or47b ORNs 中的 Ca 水平，这可能导致 CaMKI 介导的组蛋白乙酰转移酶 CBP 的激活。这种信号事件反过来又增强了保幼激素的效力，保幼激素是调节果蝇生殖成熟的与年龄相关的调节剂。此外，雄性特异性 Fruitless 同工型（Fru）是感觉可塑性所必需的，这表明 Fru 作为下游基因组巧合探测器在 Or47b ORNs 中发挥作用，整合生殖成熟度（由保幼激素信号）和种群密度（由 CBP 信号）。总之，我们确定了一个神经基质和活性依赖的机制，通过该机制，社会环境可以直接影响信息素敏感性，从而根据动物的生活史阶段调节社会行为。
