Conservation and modification of genetic and physiological toolkits underpinning diapause in bumble bee queens

Abstract

Diapause is the key adaptation allowing insects to survive unfavourable conditions and inhabit an array of environments. Physiological changes during diapause are largely conserved across species and are hypothesized to be regulated by a conserved suite of genes (a 'toolkit'). Furthermore, it is hypothesized that in social insects, this toolkit was co-opted to mediate caste differentiation between long-lived, reproductive, diapause-capable queens and short-lived, sterile workers. Using Bombus terrestris queens, we examined the physiological and transcriptomic changes associated with diapause and CO2 treatment, which causes queens to bypass diapause. We performed comparative analyses with genes previously identified to be associated with diapause in the Dipteran Sarcophaga crassipalpis and with caste differentiation in bumble bees. As in Diptera, diapause in bumble bees is associated with physiological and transcriptional changes related to nutrient storage, stress resistance and core metabolic pathways. There is a significant overlap, both at the level of transcript and gene ontology, between the genetic mechanisms mediating diapause in B. terrestris and S. crassipalpis, reaffirming the existence of a conserved insect diapause genetic toolkit. However, a substantial proportion (10%) of the differentially regulated transcripts in diapausing queens have no clear orthologs in other species, and key players regulating diapause in Diptera (juvenile hormone and vitellogenin) appear to have distinct functions in bumble bees. We also found a substantial overlap between genes related to caste determination and diapause in bumble bees. Thus, our studies demonstrate an intriguing interplay between pathways underpinning adaptation to environmental extremes and the evolution of sociality in insects.

Gene Expression Dynamics in Major Endocrine Regulatory Pathways along the Transition from Solitary to Social Life in a Bumblebee, Bombus terrestris

“…Their low expression levels during diapause are characteristic for a reproductive arrest in hibernating insects (e.g., Goodman and Cusson, 2012). Our findings contrast with the data of Amsalem et al (2015b) who found no differences in Vg expression in fat bodies of mated, diapausing queens, and post diapause foundresses. Potentially, these differences stem from the time of sampling, i.e., before (Amsalem et al, 2015b) and after the emergence of workers (the present study).…”

“…Our findings contrast with the data of Amsalem et al (2015b) who found no differences in Vg expression in fat bodies of mated, diapausing queens, and post diapause foundresses. Potentially, these differences stem from the time of sampling, i.e., before (Amsalem et al, 2015b) and after the emergence of workers (the present study). Amsalem et al (2015b) suggested this discrepancy with most insects might be a sign of derived functions of vitellogenin in social insects.…”

“…Yet, since the alternative JH production sites are only poorly investigated so far, it is possible that the production of at least some JH in the ovaries may be more widespread than previously considered (De Loof et al, 2013). Even though a high JH synthesis is not automatically synonymous with elevated JH titers (Bloch et al, 2000), our results support the previously proposed conservation of the gonadotropic role of JH in bumblebees (Bloch et al, 2000; Shpigler et al, 2014, 2016; Amsalem et al, 2015b). …”

“…In bumblebees, the presence of queen diapause has been proposed to be a prerequisite for the evolution of sociality by co-option of the diapause-regulating gene network for new roles in caste differentiation (Hunt and Amdam, 2005; Hunt et al, 2007). Several studies have investigated the genetics underlying diapause in bumblebees (Kim et al, 2006, 2008; Colgan et al, 2011), including a very recent study communicating a genome-wide transcriptome comparison targeting the fat body of diapausing Bombus terrestris queens (Amsalem et al, 2015b). The latter study, concurrent with our own investigations, highlighted the functional association of the genes highly expressed in the queen's fat body with nutrient storage and stress resistance, as well as a different role of JH and Vg in diapausing bumblebee queens when compared to dipteran models.…”

Changes in histone acetylation as potential mediators of pupal diapause in the flesh fly, Sarcophaga bullata

“…The dormant period is characterized by developmental arrest, metabolic downregulation, and increased stress-resistance. These diapause-related changes are associated with wide-spread changes in gene expression patterns M A N U S C R I P T A C C E P T E D ACCEPTED MANUSCRIPT 4 (Denlinger, 2002) that have been characterized for a variety of insects and other arthropods including spider mites (Byron et al, 2013), crickets (Reynolds and Hand, 2009), moths (Wadsworth and Dopman, 2015), solitary bees (Yocum et al, 2015 ), bumble bees (Amsalem et al 2015), mosquitoes (e.g. Poelchau et al, 2013;Robich et al, 2007, Tormey et al, 2015, and several of the higher Diptera (Ragland et al, 2010, Ragland et al, 2011, Flannagan et al 1998, Kubrak et al 2014).…”