High juvenile hormone titre and abdominal activation of JH signalling may induce reproduction of termite neotenics

Abstract

Termite castes are a key example of polyphenism, in which reproductive division of labour is clearly seen in colonies. The reproductive castes in termites include primary and neotenic reproductives; primary reproductives found a new colony whereas neotenics succeed them in the reproductive role when the primary reproductives die or become senescent. Neotenics usually differentiate from nymphs or workers by developing functional gonads while retaining juvenile characteristics; however, the developmental mechanism during neotenic differentiation remains poorly understood. Juvenile hormone (JH) mediates a number of aspects of developmental regulation in caste differentiation in termites. In the present study we quantified JH titres in neotenic reproductives of Reticulitermes speratus, and compared these with other developmental stages. In addition, expression changes in JH signalling gene homologues (Methoprene-tolerant [Met], Krüppel-homolog1, Broad-Complex) in the head, thorax and abdomen were investigated during neotenic differentiation. Finally, we examined the function of Met in reproduction of neotenics by RNA interference (RNAi). Our results showed that the JH titres of neotenics were significantly higher than those of nymphs and workers. JH signalling genes were highly expressed in neotenic abdomens, compared with those in workers and nymphs. Met RNAi resulted in the inhibition of vitellogenin gene expression in newly moulted neotenics. These results suggest that the fertility of neotenics might be controlled by a large increase of JH titres and body-part-specific activation of JH signalling pathways.

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

“…This may explain why the lower termite C. secundus shows reproductive female‐biased expression of the JH receptor and transcription factor Met, although it remains unclear why none of the JH signaling genes were differentially expressed in the other lower termite, Z. nevadensis . The upregulation of Met in reproductive C. secundus females is consistent with the fact that this factor transduces the vitellogenic signal of JH, for example, in neotenic reproductives of Reticulitermes speratus , a lower termite (Elliott, & Stay, ; Saiki, Gotoh, Toga, Miura, & Maekawa, ). The lack of a similar signal in Kr‐h1 is however surprising as Kr‐h1 is an early response gene of JH activity.…”

Expressions of juvenile hormone biosynthetic genes during presoldier differentiation in the incipient colony of Zootermopsis nevadensis (Isoptera: Archotermopsidae)

“…Experimental details were reported previously (Maekawa et al 2010;Saiki et al 2015;Watanabe et al 2011). Briefly, the 3rd instar larvae for JH extraction were sampled from a mature colony.…”

Genes Underlying Reproductive Division of Labor in Termites, with Comparisons to Social Hymenoptera

“…In termites, as in many insects (cockroaches: Comas et al, 1999Comas et al, , 2001Süeren-Castillo et al, 2012;others: Nijhout, 1994), generally high vitellogenin titers correlate with high JH titers Maekawa et al, 2010;reviewed in: Korb, 2015) (exception: the archotermopsid Hodotermopsis sjostedti ;Cornette et al, 2008). The causal link between both was recently confirmed with RNAi experiments (Saiki et al, 2015). Down-regulation of met (Methopren-tolerant), the major receptor of JH, resulted in inhibition of Vg expression in R. speratus neotenics.…”

“…According to results for the rhinotermitid Reticulitermes aculabialis, oogenesis in workers is arrested after the oocycte growth stage so that vitellogenic oocytes are absent (Su et al, 2014). Vitellogenic oocytes only occur after a reproductive molt, associated with increased Vg expression in female reproductives in many species (Saiki et al, 2015;reviewed in Korb, 2015). Strikingly, a doubling of DNA content through endoploidy in the fat body (i.e., the main tissue for vitellogenesis) was found in queens, but not other castes, in R. speratus (Nozaki and Matsuura, 2016).…”