Remodeling of the juvenile hormone pathway through caste‐biased gene expression and positive selection along a gradient of termite eusociality

Abstract

The evolution of division of labor between sterile and fertile individuals represents one of the major transitions in biological complexity. A fascinating gradient in eusociality evolved among the ancient hemimetabolous insects, ranging from noneusocial cockroaches through the primitively social lower termites-where workers retain the ability to reproduce-to the higher termites, characterized by lifetime commitment to worker sterility. Juvenile hormone (JH) is a prime candidate for the regulation of reproductive division of labor in termites, as it plays a key role in insect postembryonic development and reproduction. We compared the expression of JH pathway genes between workers and queens in two lower termites (Zootermopsis nevadensis and Cryptotermes secundus) and a higher termite (Macrotermes natalensis) to that of analogous nymphs and adult females of the noneusocial cockroach Blattella germanica. JH biosynthesis and metabolism genes ranged from reproductive female-biased expression in the cockroach to predominantly worker-biased expression in the lower termites. Remarkably, the expression profile of JH pathway genes sets the higher termite apart from the two lower termites, as well as the cockroach, indicating that JH signaling has undergone major changes in this eusocial termite. These changes go beyond mere shifts in gene expression between the different castes, as we find evidence for positive selection in several termite JH pathway genes. Thus, remodeling of the JH pathway may have played a major role in termite social evolution, representing a striking case of convergent molecular evolution between the termites and the distantly related social hymenoptera.

Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects

“…The latter finding is interesting since, in the nematode worm Caenorhabditis elegans and in D. melanogaster, E3 ubiquitin ligases have been found to regulate lifespan [67,68]. By contrast, the top +50 genes with the strongest positive loadings (characterizing workers) comprised two TEs, three genes potentially linked to chemical communication and a JH epoxidase that is likely to be worker-specific [69]. The top −50 genes with the strongest negative loadings on the age/caste-related PC2 (characterizing kings, old reproductives and young workers) included two antimicrobial peptide genes (AMPs) involved in immunity, one transferrin potentially representing an antioxidant (see [70]) and one gene probably linked to chemical communication.…”

The first cockroach genome and its significance for understanding development and the evolution of insect eusociality

“…Similarly, Jongepier et al. () identified a remodeling of the JH pathway within termites compared to the noneusocial B. germanica , possibly allowing the evolution of castes. Even stronger changes in the JH pathway occurred within the higher termite, Macrotermes natalensis , which, in contrast to lower termites, live in highly complex, large colonies with irreversible worker castes.…”

How Can Termites Achieve Their Unparalleled Postembryonic Developmental Plasticity? A Test for the Role of Intermolt-Specific High Juvenile Hormone Titers

“…We quantified the expression of Kr-h1 (Krüppel-homolog 1, CsecKr-h1), which is an early response gene upregulated under high JH titers in insects (e.g., Bellés et al, 2005;Bellés and Santos, 2014;Jindra et al, 2015). Additionally, we tested genes supposed to be involved in JH biosynthesis: two JH epoxidases (P450-15A1; CsecJH epoxidase1 and CsecJH epoxidase2) and the supposed two JH receptor genes, CsecMet (Methoprene-tolerant) and CsecTai (Taiman) (for more details on genes and methods, see below) (Harrison et al, 2018;Jongepier et al, 2018). If methoprene treatment functions efficiently, these four JH biosynthesis genes should not be affected by methoprene treatment.…”

“…and CsecJH epoxidase2; these two genes have been identified as an ortholog and a paralog of the D. melanogaster JH epoxidase that synthesize JH (Harrison et al, 2018;Jongepier et al, 2018). As we do not know which of both genes has the same function in C. secundus, we tested both genes.…”