The effect of intrinsic physiological traits on diapause survival and their underlying mechanisms in an annual bee speciesBombus impatiens

Abstract

In the face of insect declines, identifying phases of the life cycle when insects are particularly vulnerable to mortality is critical to conservation efforts. For numerous annual insect groups, diapause is both a key adaptation that allows survival of inhospitable conditions and a physiologically demanding life stage that can result in high rates of mortality. As bees continue to garner attention as a group experiencing high rates of decline, improving our understanding of how annual bees prepare for diapause and identifying factors that reduce survival is imperative. Here, we studied factors affecting diapause survival length and their underlying mechanisms using an economically and ecologically important annual bee species, Bombus impatiens. We examined how age and mass upon diapause onset correlate with diapause survival length, and the mechanistic role of nutrient acquisition and oxidative stress post pupal eclosion in mediating these effects. Our findings show that both age and mass were strong predictors of diapause survival length. Heavier queens or queens in the age range of ~6–17 days survived longer in diapause. Mass gain was attributed to increases in lipid, protein and glycerol amounts following pupal eclosion, and the ability to deal with oxidative stress was significantly compromised in older pre-diapause queens. Our results demonstrate that age-related shifts in bee physiology and timing of nutrient acquisition may both be critical factors driving diapause survival.

Flexibility in the Critical Period of Nutrient Sequestration in Bumble Bee Queens

“…Our NS3d queens, for example, refer to their being nectar starved for 3 days; these queens received pollen for the duration of the experiment but were starved of artificial nectar for 3 days, then were switched to the control nectar diet for the remainder of the experiment. Bombus impatiens queen nutrient stores completely plateau by around age 12 days ( Alford 1969a ; Röseler and Röseler 1986 ; Woodard et al 2019 ; Treanore and Amsalem 2020 ), which might signify preparation for or the onset of diapause ( Costa et al 2020 ). We chose the timepoints of 3, 6, 9, and 12 days of age because they span the approximately 12-day pre-diapause, nutrient storage period.…”

“…Adult queens are the only bumble bee life stage and caste that undergo diapause; workers and males live only during the season in which they eclose, whereas queens typically have a longer life cycle of around one year. In preparation for overwintering in a diapause state, queens sequester copious amount of lipids and glycogen, primarily in trophocytes of the fat body ( Alford 1969a ; Röseler and Röseler 1986 ; Fliszkiewicz and Wilkaniec 2007 ; Votavová et al 2015 ; Treanore and Amsalem 2020 ; but see Amsalem et al 2015 ). Protein levels remain consistent and do not increase in preparation for diapause ( Alford 1969b ; Woodard et al 2019 ; but see Treanore and Amsalem 2020 ).…”

“…In preparation for overwintering in a diapause state, queens sequester copious amount of lipids and glycogen, primarily in trophocytes of the fat body ( Alford 1969a ; Röseler and Röseler 1986 ; Fliszkiewicz and Wilkaniec 2007 ; Votavová et al 2015 ; Treanore and Amsalem 2020 ; but see Amsalem et al 2015 ). Protein levels remain consistent and do not increase in preparation for diapause ( Alford 1969b ; Woodard et al 2019 ; but see Treanore and Amsalem 2020 ). The fat body is a liver-like tissue in insects that is the primary location of energy storage and release and also plays important roles in detoxification and immune function ( Arrese and Soulages 2010 ; Hahn and Denlinger 2011 ).…”

“…Access to both pollen (the primary source of dietary fatty acids) and nectar (the primary source of sugars stored as glycogen) are critical for overwintering survival. Queen mass upon entering diapause has been positively associated with diapause survival in a number of studies ( Beekman et al 1998 , 2000 ; Bogo et al 2017 ; Treanore and Amsalem 2020 ), and a lack of either nectar-derived sugar or pollen in the diet during the pre-diapause period significantly reduces overwintering survival in laboratory-reared queens ( Woodard et al 2019 ). There are also sublethal consequences of pre-diapause food availability.…”

“…Typically this ranges from a radius of a few meters up to 10 km ( Chapman et al 2003 ; Darvill et al 2004 ; Knight et al 2005 ; Charman et al 2010 ; Rao and Strange 2012 ; Jha and Kremen 2013 ; Geib et al 2015 ). The majority of glycogen and lipids are sequestered during the first ∼3 days of adulthood, then levels plateau before or around day 6 ( Alford 1969a ; Woodard et al 2019 ; Treanore and Amsalem 2020 ). These timepoints correspond with the ages that queens are primarily still in their natal nests, and correspond with the timepoint around which pollen consumption by queens (of B. terrestris ) declines dramatically ( Přidal and Hofbauer 1996 ).…”