Stress signaling: coregulation of hemoglobin and male sex determination through a terpenoid signaling pathway in a crustacean

Abstract

Environmental signals can activate neuro-endocrine cascades that regulate various physiological processes. In the present study, we demonstrate that two responses to environmental stress signaling in the crustacean Daphnia magna -hemoglobin accumulation and male offspring production -are co-elevated by the crustacean terpenoid hormone methyl farnesoate and several synthetic analogs. Potency of the hormones with respect to the induction of both hemoglobin and male offspring was highly correlated, suggesting that both processes are regulated by the same terpenoid signaling pathway. Six clones of the D. pulex/pulicaria species complex that were previously characterized as unable to produce male offspring and five clones that were capable of producing males were evaluated for both hemoglobin induction and male offspring production in response to methyl farnesoate. Four of the five male-producing clones produced both hemoglobin and male offspring in response to the hormone. Five of the six non-male-producing clones produced neither hemoglobin nor males in response to the hormone. These results provide additional evidence that both physiological processes are regulated by the same signaling pathway. Furthermore, the results indicate that the non-male-producing clones are largely defective in some methyl farnesoate signaling component, downstream from methyl farnesoate synthesis but upstream from the genes regulated by the hormone. A likely candidate for the site of the defect is the methyl farnesoate receptor. As a consequence of this defect, non-male-producing clones have lost their responsiveness to environmental signals that are transduced by this endocrine pathway. This defect in signaling would be likely to enhance population growth in stable environments due to the elimination of males from the population, assuming that other processes critical to population growth are not also compromised by this defect.

Neural control of gene recruitment in metazoans

“…Transduction in the brain of the crustacean of the environmental signals into instructions (¼information) for switching to sexual reproduction involves activation of the cholinergic system in the brain (Eads et al, 2008) and causes a pulse of methyl farnesoate, which binds its specific receptor during a critical period of oocyte maturation (Rider et al 2005) (Fig. 1).…”

Ecological genomics in Daphnia: stress responses and environmental sex determination

“…The insecticides pyriproxyfen, fenoxycarb and methoprene cause male broods (Tatarazako et al, 2003), with orders of magnitude greater potency than MF for pyriproxyfen and fenoxycarb. Interestingly, all of these compounds also induce Hb production in Daphnia (Rider et al, 2005). Therefore, male production and Hb induction appear to be coupled at some level by JHA signaling (see below).…”

Pyriproxyfen, a juvenoid hormone analog, does not induce male production in parthenogenetic lineages of Eucypris virens (Crustacea: Ostracoda)

“…Recent experimental research revealed that juvenoid hormones regulate sex determination in different arthropod groups, including cladocerans (Olmstead & LeBlanc 2002Tatarazako et al 2003;Rider et al 2005;Kim et al 2006;Oda et al 2006) and aphids (Hales & Mittler 1987, 2005. For species where males were previously unknown, a whole range of new diagnostic characters could be obtained through application of a hormone treatment (Kim et al 2006).…”

“…Methylfarnesoate is a crustacean juvenoid hormone that acts through the same signalling pathway as haemoglobin induction (Rider et al 2005). The hormone induced male production in lineages that were considered as non-male producers (Rider et al 2005), and even in species for which males were not known (Kim et al 2006).…”

“…The hormone induced male production in lineages that were considered as non-male producers (Rider et al 2005), and even in species for which males were not known (Kim et al 2006). Several synthetic analogs of methylfarnesoate, namely pyriproxyfen, methoprene and fenoxycarb, were found to have similar sex determining effects (Olmstead & LeBlanc 2003;Rider et al 2005). In particular, pyriproxyfen proved to be very powerful.…”