Convergent Evolution Associated with the Loss of Developmental Diapause May Promote Extended Lifespan in Bees

Abstract

Diapause has long been proposed to play a significant role in the evolution of eusociality in Hymenoptera. Recent studies have shown that shifts in the diapause stage precede social evolution in wasps and bees; however, the genomic basis remains unknown. Given the overlap in molecular pathways that regulate diapause and lifespan, we hypothesized that the evolutionary loss of developmental diapause may lead to extended lifespan among adults, which is a prerequisite for the evolution of eusociality. To test whether the loss of prepupal diapause is followed by genomic changes associated with lifespan extension, we compared 27 bee genomes with or without prepupal diapause. Our results point to several potential mechanisms for lifespan extension in species lacking prepupal diapause, including the loss of the growth hormone PTTH and its receptor TORSO, along with convergent selection in genes known to regulate lifespan in animals. Specifically, we observed purifying selection of prolongevity genes and relaxed selection of antilongevity genes within the IIS/TOR pathway in species that have lost prepupal diapause. Changes in selection pressures on this pathway may lead to the evolution of new phenotypes, such as lifespan extension and altered responses to nutritional signals that are crucial for social evolution.

Keywords: aging; comparative genomics; dormancy; eusociality; selection.

Fig. 1.

The 27 species included in the molecular evolution analysis and their associated life history traits. The prepupal diapause stage is depicted in dark blue, while the loss of developmental diapause is represented in lighter blue. Solitary bees are indicated by a stronger yellow color, and social species are denoted by a lighter yellow. Purple represents the presence of the PTTH and its receptor TORSO, while the absence of color indicates orthologs could not be found. The species marked with “?” had conflicting results regarding the presence of PTTH, depending on whether the search was conducted using the genome or the annotated protein-coding genes set as a reference.

Fig. 2.

The Venn diagram depicts orthogroups categorized under relaxed a) or intensified b) selection, which intersect with genes under positive selection (aBSREL), accelerated evolution (Rho+), and/or decelerated evolution (Rho−). Different colors denote orthogroups potentially experiencing positive (yellow), purifying (blue), relaxed (purple), or intensified (green) selection, while dashed lines indicate orthogroups with the strongest evidence for positive (yellow) and purifying (blue) selection. Refer to the Materials and Methods section for comprehensive classification details.

Fig. 3.

Simplified scheme illustrating 2 pathways regulating the production and release of ecdysone by the prothoracic gland (PG). The pathway utilizing the tyrosine-protein kinase receptor TORSO as a receptor for the prothoracicotropic hormone PTTH is absent in species that do not undergo prepupal diapause. epidermal growth factor receptor substrate 15 (EGFR15), a substrate of the alternative pathway that uses EGFR as a receptor, is subject to positive selection, along with the son of sevenless (SOS) gene, highlighting the significance of this pathway in species without prepupal diapause.

Fig. 4.

Simplified scheme of the IIS and TOR pathways containing genes under selection in the current study. When the insulin pathway is activated (high nutrition), Akt phosphorylates FoxO, preventing its entrance to the nucleus of the cell, and activates Tor, leading to growth. When there is a reduction in the IIS/TOR pathway activation (low nutrition), FoxO enters in the nucleus of the cells, regulating thousands of genes, leading to lifespan extension. Continuous arrows represent activation of the pathway in an environment with high nutrition, for example, while dashed arrows represent the alternative pathway in environments with low nutrition. Genes within green, blue, or purple boxes represent those under intensified, purifying, and relaxed selection in the current study, respectively. The box in the bottom right classifies the genes as pro- or antilongevity based on their known effects on Drosophila lifespan (Tacutu et al. 2018). Figure made based on Kapahi and Zid (2004), Dutriaux et al. (2013), Texada et al. (2020), and Denlinger (2022a, .