The evolution of extreme fertility defied ancestral gonadotropin mediated brain-reproduction tradeoff

Abstract

16Gonadotropic hormones coordinate processes in diverse tissues regulating animal reproductive 17 physiology and behavior. Juvenile hormone (JH) is the ancient and most common gonadotropin in 18 insects, but not in advanced eusocial honey bees and ants. To probe the evolutionary basis of this change, 19we combined endocrine manipulations, transcriptomics, and behavioral analyses to study JH regulated 20 processes in a bumble bee showing an intermediate level of sociliality. We found that in the fat body, 21 more JH-regulated genes were upregulated and enriched for metabolic and biosynthetic pathways. This 22 34Addressing this question is crucial for understanding both the evolution of advanced eusociality and the 51 evolution of gonadotropic hormones in general. 52To study variability in socially-related JH functions, we focused on the best-studied bumble bee, 53Bombus terrestris. Bumble bees provide an excellent model system with which to address this issue 54 because they show a simpler form of social organization relative to honey bees and ants (Wilson 1971), 55 and JH is their major gonadotropic hormone (Röseler 1977;Röseler and Röseler 1978; Bloch, Borst, et al. 56 2000;Shpigler, et al. 2014). JH coordinates processes in various tissues that are 57 involved in B. terrestris reproduction including the fat body, ovaries, wax production, and exocrine gland 58 activity (Shpigler, et al. 2010;Shpigler, et al. 2014). JH apparently also regulates 59 processes in the central nervous system because JH manipulations affect behaviors such as dominance 60 and aggression Pandey, et al. 2019). The bumble bee B. terrestris thus provides an 61 excellent contrast to honey bees to address the question of the evolutionary change in JH function 62 associated with eusociality, but little is known on the molecular processes by which JH coordinates the 63 various cells and tissues in this species. 64Here we combine hormonal manipulations, behavioral observations, and RNA sequencing 65 (RNAseq) of the brain and fat body tissues of Bombus terrestris workers. We further take advantage of 66 two "natural experiments" in which we compared gene expression in bumble bees that naturally differ in 67 JH titers. First, we analyzed the brain transcriptomes of orphan workers in which the dominant individual 68 subjected to replacement therapy show that JH regulates the expression of many genes in both the brain 126 and the fat body of bumble bee workers. 127 8 128 129 Figure 2. The effect of JH on brain gene expression. Details as in Fig 1 (A) Heat map of 3060 DEGs 130 (FDR p < 0.05) in the brain. (B) Venn diagrams comparing DEGs between the CA-treatment (left) or the 131 Sham treatment (right) and the three other treatments. (C) Three-dimensional correlation analysis for the 132 fold change expression of 700 overlapping DEGs between the CA-and the three other groups. The R 2 was