Goolsby Billie C, Smith E Jordan, Muratore Isabella B, Coto Zach N, Muscedere Mario L, Traniello James F A
Department of Biology, Boston University, Boston, MA, 02215, USA.
Department of Biology, Stanford University, Stanford, CA, 94305, USA.
bioRxiv. 2023 Dec 17:2023.06.29.546928. doi: 10.1101/2023.06.29.546928.
Social experience early in life appears to be necessary for the development of species-typical behavior. Although isolation during critical periods of maturation has been shown to impact behavior by altering gene expression and brain development in invertebrates and vertebrates, workers of some ant species appear resilient to social deprivation and other neurobiological challenges that occur during senescence or due to loss of sensory input. It is unclear if and to what degree neuroanatomy, neurochemistry, and behavior will show deficiencies if social experience in the early adult life of worker ants is compromised. We reared newly-eclosed adult workers of under conditions of social isolation for 2 to 53 days, quantified brain compartment volumes, recorded biogenic amine levels in individual brains, and evaluated movement and behavioral performance to compare the neuroanatomy, neurochemistry, brood-care behavior, and foraging (predatory behavior) of isolated workers with that of workers experiencing natural social contact after adult eclosion. We found that the volume of the antennal lobe, which processes olfactory inputs, was significantly reduced in workers isolated for an average of 40 days, whereas the size of the mushroom bodies, centers of higher-order sensory processing, increased after eclosion and was not significantly different from controls. Titers of the neuromodulators serotonin, dopamine, and octopamine remained stable and were not significantly different in isolation treatments and controls. Brood care, predation, and overall movement were reduced in workers lacking social contact early in life. These results suggest that the behavioral development of isolated workers of is specifically impacted by a reduction in the size of the antennal lobe. Task performance and locomotor ability therefore appear to be sensitive to a loss of social contact through a reduction of olfactory processing ability rather than change in the size of the mushroom bodies, which serve important functions in learning and memory, or the central complex, which controls movement.
生命早期的社会经历似乎是物种典型行为发展所必需的。虽然在无脊椎动物和脊椎动物的关键成熟时期进行隔离已被证明会通过改变基因表达和大脑发育来影响行为，但一些蚂蚁种类的工蚁似乎对衰老期间或由于感觉输入丧失而出现的社会剥夺和其他神经生物学挑战具有抵抗力。目前尚不清楚，如果工蚁成年早期的社会经历受到损害，神经解剖学、神经化学和行为是否会出现缺陷以及缺陷程度如何。我们在社会隔离条件下饲养了新羽化的成年工蚁2至53天，量化了脑区体积，记录了个体大脑中的生物胺水平，并评估了运动和行为表现，以比较隔离工蚁与成年羽化后经历自然社会接触的工蚁的神经解剖学、神经化学、育幼行为和觅食（捕食行为）。我们发现，处理嗅觉输入的触角叶体积在平均隔离40天的工蚁中显著减小，而作为高阶感觉处理中心的蘑菇体大小在羽化后增加，且与对照组无显著差异。神经调节物质血清素、多巴胺和章鱼胺的滴度保持稳定，在隔离处理组和对照组中无显著差异。缺乏早期社会接触的工蚁的育幼、捕食和总体运动能力下降。这些结果表明，隔离的工蚁的行为发育受到触角叶大小减小的特定影响。因此，任务表现和运动能力似乎对因嗅觉处理能力下降而导致的社会接触丧失敏感，而非对在学习和记忆中起重要作用的蘑菇体大小变化或控制运动的中央复合体大小变化敏感。
