Jongepier, E, Kemena, C, Lopez-Ezquerra, A, Belles, X, Bornberg-Bauer, E & Korb, J
Remodelling of the juvenile hormone pathway through caste-biased gene expression and positive selection along a gradient of termite eusociality
JEZ-B Molecular and Developmental Evolution, 2018

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The evolution of division of labour 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 non-eusocial 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 labour in termites, as it plays a key role in insect post-embryonic 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 comparable nymphs and adult females of the non-eusocial 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 signalling 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, remodelling 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.