Department of Biology, Boston University, Boston, Massachusetts, USA.
Department of Biology, Stanford University, Stanford, California, USA.
Brain Behav Evol. 2024;99(3):171-183. doi: 10.1159/000539546. Epub 2024 Jun 10.
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 Camponotus floridanus under conditions of social isolation for 2-53 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 C. floridanus 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.
生命早期的社会经验似乎是物种典型行为发展所必需的。尽管在成熟的关键时期进行隔离已经被证明会通过改变基因表达和无脊椎动物和脊椎动物的大脑发育来影响行为,但某些蚂蚁物种的工蚁似乎能够抵御社会剥夺和衰老或由于感觉输入丧失而发生的其他神经生物学挑战。目前尚不清楚如果早期成年工蚁的社会经验受到损害,神经解剖结构、神经化学和行为是否会表现出缺陷,以及如果会表现出缺陷,程度如何。
我们在社会隔离条件下饲养新羽化的成年佛罗里达 Camponotus 工蚁 2-53 天,量化了脑区体积,记录了单个大脑中的生物胺水平,并评估了运动和行为表现,以比较隔离工蚁的神经解剖结构、神经化学、育雏行为和觅食(捕食行为)与自然接触的工蚁。
我们发现,处理嗅觉输入的触角叶体积在平均隔离 40 天后显著减小,而蘑菇体(高级感官处理中心)的大小在羽化后增加,并且与对照组没有显著差异。神经调质 5-羟色胺、多巴胺和章鱼胺的滴度在隔离处理和对照组中保持稳定且没有显著差异。缺乏生命早期社会接触的工蚁的育雏、捕食和整体运动减少。
这些结果表明,C. floridanus 隔离工蚁的行为发育受到触角叶体积减小的特异性影响。因此,行为表现和运动能力似乎对嗅觉处理能力丧失而不是蘑菇体大小变化(蘑菇体在学习和记忆中起重要作用)或中央复合体(控制运动)丧失导致的社会接触丧失敏感。