Metabolic and transcriptomic characterization of summer and winter dormancy in the solitary bee, Osmia lignaria

Authors: MELICHER, DACOTAH - US Department Of Agriculture (USDA); Torson, Alex; Yocum, George; BOSCH, JODI - Centre De Recerca Ecologia; KEMP, WILLIAM - Retired ARS Employee; BOWSHER, JULIA - North Dakota State University; Rinehart, Joe

Submitted to: Insect Biochemistry and Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/13/2024
Publication Date: N/A
Citation: N/A

Interpretive Summary: The blue orchard bee, Osmia lignaria, is an economically important orchard pollinator in the United States. Many insect species in temperate environments enter a state of dormancy to endure harsh environmental conditions. Most insects go dormant during winter, but O. lignaria goes dormant twice during its lifecycle: once as a larva to avoid hot temperatures during summer and once as adults to overwinter. Insects employ two main types of dormancies – one that is a programmed part of the lifecycle and one that occurs directly in response to stress. These two different types of dormancies are managed differently in commercially reared insect species. However, we do not know whether O. lignaria’s larval dormancy is a programmed part of the lifecycle or if it simply occurs in response to stressful environmental conditions. Therefore, we measured metabolic rates and gene expression to compare adult and larval dormancy. We found that both dormancies are characterized by temperature-independent decreases in metabolic rate, consistent with a programmed dormancy, but they exhibit very different physiology. Developing a better understanding of this prepupal dormancy will be critical for the continued development of optimal rearing protocols O. lignaria to manage its pollination services.

Technical Abstract: The solitary bee Osmia lignaria is a native pollinator in North American and of growing economic importance. This species is unusual in that they enter an obligate dormancy at two developmental stages to survive very different environmental conditions. Larvae develop during the spring and early summer. Upon cocoon spinning, fully developed larvae (prepupae) become dormant until late summer when they resume development and complete metamorphosis. Shortly after adult eclosion, they enter a second dormancy period and overwinter as diapausing adults. The life cycle of O. lignaria provides a unique opportunity to compare the physiological and molecular mechanisms underlying two ecologically contrasting dormancies within the same species. To compare these two dormancies, we measured metabolic rates and gene expression across development as bees initiate, maintain, and terminate both prepupal (summer) and adult (overwintering) dormancies. We observed a moderate temperature-independent decrease in gas exchange during both the prepupal dormancy after cocoon spinning (45 %) and during adult diapause after eclosion (60 %). To facilitate our investigations of the transcriptomic signatures of these dormancies, we sequenced and assembled a high-quality reference genome from a single haploid male bee with a contiguous n50 of 5.5Mbp. The transcriptomes of dormant prepupae and diapausing adults clustered into distinct groups most closely associated with life stage rather than dormancy status. Membrane transport, membrane-bound cellular components, oxidoreductase activity, glutathione metabolism, and transcription factor activity increased during adult diapause, relative to prepupal dormancy. Further, the transcriptomes of adults in diapause clustered into two groups, supporting multiple phases of diapause during winter. Late adult diapause is associated with gene expression profiles supporting increased insulin/IGF signaling and juvenile hormone and ecdysone signaling.