Metamorphosis is induced by food absence rather than a critical weight in the solitary bee, Osmia lignaria

Authors: HELM, BRYAN - North Dakota State University; Rinehart, Joseph - Joe; Yocum, George; GREENLEE, KENDRA - North Dakota State University; BOWSHER, JULIA - North Dakota State University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/23/2017
Publication Date: 10/10/2017
Publication URL: http://handle.nal.usda.gov/10113/5852199
Citation: Helm, B.R., Rinehart, J.P., Yocum, G.D., Greenlee, K.J., Bowsher, J.H. 2017. Metamorphosis is induced by food absence rather than a critical weight in the solitary bee, Osmia lignaria. Proceedings of the National Academy of Sciences. 114(41): 10924–10929. https://doi.org/10.1073/pnas.1703008114.

Interpretive Summary: Body size influences nearly every aspect of organismal performance. The timing of development (directly related to final body size) has a direct impact on pollinators because larger body size increases foraging range and reproductive investment in bees. Thus, the mechanisms regulating the onset of development have occupied insect physiologists for almost a century. Much of this research centers on the concept of a ‘critical weight,’ the weight that triggers the hormonal cascade for development. Despite decades of research, the physiological factor or factors inducing developmental commitment at the critical weight remains a mystery for most insects. Here, we show that starvation is the cue for development in blue orchard bee, Osmai lignaria and that a critical weight, as traditionally defined, does not exist in this species. When we starved O. lignaria larvae at a wide range of body sizes, larvae immediately (<24hrs) initiated development. We found that manipulation of food provision quantity resulted in more than a 10-fold body mass difference between the smallest and largest adult O. lignaria, a range that spanned the body sizes of bees collected in the field. Application of the drug precocene that blocks the action of a key developmental regulating hormone, juvenile hormone, suggest that starvation initiates development through a decrease in juvenile hormone. This is the same mechanism employed by insects whose development is triggered by the critical weight mechanism. These results indicate that complete consumption of the larval provision and the subsequent lack of food is the mechanism that initiates development under natural conditions for O. lignaria. Mothers provision a discrete amount of larval food in many species of insects, including all species of bees and wasps, and therefore our results have implications for many species under similar life-history constraints as O. lignaria.

Technical Abstract: Body size influences nearly every aspect of organismal performance. Adult body size in holometabolous insects is determined by the size of the insect at metamorphosis. Thus, the mechanisms regulating the onset of metamorphosis have occupied insect physiologists for almost a century. Much of this research centers on the concept of a ‘critical weight’ the weight that triggers the hormonal cascade for metamorphosis. Despite decades of research, the physiological factor or factors inducing metamorphic commitment at the critical weight remains a mystery for most insects. Here, we show that starvation is the cue for metamorphosis in Osmai lignaria and that a critical weight, as traditionally defined, does not exist in this species. When we starved O. lignaria larvae at a wide range of body sizes, larvae immediately (<24hrs) initiated pupation. We found that manipulation of food provision quantity resulted in more than a 10-fold body mass difference between the smallest and largest adult O. lignaria, a range that spanned the body sizes of bees fed un-manipulated provisions. Application of the juvenile hormone antagonist precocene suggests that starvation initiates metamorphosis through a decrease in juvenile hormone, a mechanism similar to the critical weight in other insects. These results indicate that complete consumption of the larval provision and the subsequent lack of food is the mechanism that initiates metamorphosis under natural conditions. The timing of metamorphosis has fitness implications because larger body size increases foraging range and reproductive investment in solitary bees. Mothers provision a discrete amount of larval food in many species of insects, including all species of bees and wasps, and therefore our results have implications for many species under similar life-history constraints as O. lignaria.