Starvation stress during larval development reveals predictive adaptive response in adult worker honey bees (Apis mellifera)

Authors: WANG, YING - Arizona State University; KAFTANOGLU, OSMAN - Arizona State University; Brent, Colin; PAGE JR., ROBERT - Arizona State University; AMDAM, GRO - Arizona State University

Submitted to: Journal of Experimental Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/22/2015
Publication Date: 3/30/2016
Citation: Wang, Y., Kaftanoglu, O., Brent, C.S., Page Jr., R.E., Amdam, G.V. 2016. Starvation stress during larval development reveals predictive adaptive response in adult worker honey bees (Apis mellifera). Journal of Experimental Biology. 219:949-959.

Interpretive Summary: A hypothesis called 'Predictive Adaptive Response (PAR)' suggests that for some organisms set courses of development are triggered by early exposure to environmental stress and are meant to better prepare adults to cope with later stress. However, the response becomes disadvantageous when pre-adult and adult environments are dissimilar. In organisms living in highly social environment, which can buffer immature forms against environmental stressors during their development, it is unclear whether they have a PAR. Here, we test of whether starvation during early development can induce PAR in the honey bee, which is an advanced social insect capable of mitigating environmental stressors. Food deprivation during larval life caused adult bees to become more starvation resistant. Some of the adult modifications caused by juvenile starvation included changes to reproductive organs, metabolism, endocrine physiology and nutrient perception. Many of these changes are similar to those seen in humans that experience poor early nutrition. Our ability to demonstrate that PAR involves core physiology in honey bees, despite more than 60 million years of social evolution, suggests that PAR likely remains in other social organisms, including humans.

Technical Abstract: A variety of organisms exhibit developmental plasticity that results in differences in adult morphology, physiology or behavior. This variation in the phenotype, called “Predictive Adaptive Response (PAR),” gives a selective advantage in an adult's environment if the adult experiences environments similar to its developmental environment. However, the PAR can be disadvantageous when adult environments do not match the conditions of their development. Such mismatch may account for correlations between poor nutrition during early life and adult susceptibility to metabolic diseases, such as obesity and diabetes type II in humans. Still, it is unclear if humans have an intact PAR mechanism since social species have unique options for buffering environmental fluctuations. Here, we test of whether food deprivation during early development can induce PAR in honey bees, an advanced social insect with options for environmental buffering similar to those of humans. We found that food deprivation during larval life caused adults to become more starvation resistant. This increased starvation resilience in honey bees was associated with reduced ovary size, elevated glycogen stores and juvenile hormone (JH) titers, and decreased sugar perception. Similar physiological changes can help adult insects survive and reproduce in stressful environments. Our ability to demonstrate that PAR involves core physiology in honey bees, despite more than 60 million years of social evolution, suggests that the PAR likely remains in humans. Our study provides data resembling those of humans exposed to poor early nutrition. These similarities may suggest that conserved biological responses and pathways are involved in PAR.