Diet and nutritional status during early adult life have immediate and persistent effects on queen bumble bees

Abstract

Many insects sequester nutrients during developmentally programmed periods, which they metabolize during subsequent life history stages. During these periods, failure to store adequate nutrients can have persistent effects on fitness. Here, we examined a critical but under-studied nutrient storage period in queen bumble bees: the first days of adult life, which are followed by a diapause period typically coinciding with winter. We experimentally manipulated availability of pollen (the primary dietary source of lipids and protein) and the sugar concentration of artificial nectar (the primary source of carbohydrates) for laboratory-reared queens during this period and examined three nutritional phenomena: (i) diet impacts on nutritional status, (ii) the timescale upon which nutrient sequestration occurs and (iii) the fitness consequences of nutrient sequestration, specifically related to survival across the life cycle. We found evidence that pollen and nectar starvation negatively impact lipid storage, whereas nectar sugar concentration impacts stored carbohydrates. The majority of nutrients were stored during the first ~ 3 days of adult life. Nutrients derived from pollen during this period appear to be more critical for surviving earlier life stages, whereas nutrients sequestered from nectar become more important for surviving the diapause and post-diapause periods. Negative impacts of a poor diet during early life persisted in our experiment, even when pollen and a relatively high (50%) nectar sugar concentration were provided post-diapause. Based on these findings, we posit that the nutritional environment during the early adult life of queens has both immediate and persistent impacts on fitness. These findings underscore the importance of examining effects of stage-specific nutritional limitations on physiology and life history traits in this social insect group. Moreover, the findings may shed light on how declining food resources are contributing to the decline of wild bumble bee populations.

Transcriptome analysis reveals nutrition‐ and age‐related patterns of gene expression in the fat body of pre‐overwintering bumble bee queens

“…The highest concentration of sucrose (75%) in our experiment is similar to the concentration of stored honey in bumble bee nests, which has been reported as 70%–87% sugar (Crane, ; Knee & Medler, ). Furthermore, in a previous study of sugar diet impacts on queen nutritional state during the pre‐overwintering stage, a 0% sucrose diet caused queens to have significantly lower stored glycogen and lipid levels than queens fed 25% or 50% sucrose, whereas queens fed 75% sucrose had higher glycogen levels (Woodard et al, ). Thus, our diet treatment groups are both biologically realistic and have previously characterized impacts on queen nutrient levels in the period preceding diapause.…”

“…Our goal was to explore how nutritional stress and maturation impact fat body function and also broader organismal processes, during an important but under‐studied early‐life nutrient storage period in the life of an important insect pollinator. Queens store nutrients (primarily glycogen and triglycerides) during the pre‐diapause period (Alford, ; Fliszkiewicz & Wilkaniec, ; Röseler & Röseler, ; Woodard et al, ), then metabolize these nutrients during the overwintering stage of their life cycle (Alford, ; Amsalem et al, ). If queens have limited access to dietary sugar during this period, they are less likely to survive diapause (Woodard et al, ).…”

“…Queens store nutrients (primarily glycogen and triglycerides) during the pre‐diapause period (Alford, ; Fliszkiewicz & Wilkaniec, ; Röseler & Röseler, ; Woodard et al, ), then metabolize these nutrients during the overwintering stage of their life cycle (Alford, ; Amsalem et al, ). If queens have limited access to dietary sugar during this period, they are less likely to survive diapause (Woodard et al, ). Although we did not explore pollen diet composition in our study, this probably also has important effects on queens during this stage and would be an important focus of future studies.…”

“…For the last of these, many genes have expression patterns similar to genes in diapausing individuals of the relatively well‐studied dipteran Sarcophaga crassipalpis , suggesting that there is a “genetic toolkit” for diapause in insects (Amsalem et al, ). Prior to the overwintering diapause period, queens are not reproductive, and instead sequester copious amounts of glycogen (Alford, ; Röseler & Röseler, ; Woodard, Duennes, Watrous, & Jha, ; but see Votavová et al, ) and lipids (Alford, ; Fliszkiewicz & Wilkaniec, ; Woodard et al, ), which are derived largely from dietary nectar and pollen, respectively. Glycogen and lipids are both stored in the fat body (Alford, ; Votavová et al, ), a large organ that is the functional equivalent of the vertebrate liver and adipocytes and is the principal location of nutrient storage in insects (reviewed by Arrese & Soulages, ).…”

“…Glycogen and lipids are both stored in the fat body (Alford, ; Votavová et al, ), a large organ that is the functional equivalent of the vertebrate liver and adipocytes and is the principal location of nutrient storage in insects (reviewed by Arrese & Soulages, ). The ages at which the majority of nutrients are sequestered (age 0–3 days post‐eclosion for lipid stores and 0–5 days post‐eclosion for glycogen; Alford, ; Röseler & Röseler, ; Woodard et al, ) coincide with important early‐life maturational changes in queen physiology and behaviour. Upon eclosion, all bumble bee castes have a silvery appearance, an unhardened cuticle, and do not fly as melanization is still occurring (Tian & Hines, ).…”