Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna

Abstract

Daphnids (Daphnia magna) utilize cyclic parthenogenesis as a reproductive strategy. During periods of abundant resources, these organisms reproduce asexually. In response to environmental cues that signal the onset of environmental adversity, daphnids produce males and reproduce sexually. The environmental cues that stimulate the sexual reproductive phase are well known; however, the endocrine signals that transduce these environmental cues remain unknown. The present study was undertaken to test the hypothesis that the crustacean juvenoid hormone, methyl farnesoate, is a male sex determinant in this species. Continuous exposure to aqueous concentrations of methyl farnesoate greater than approximately 30 nM stimulated a concentration-dependent production of male-containing broods of organisms. Short-term exposures to methyl farnesoate during periods of egg and embryo maturation revealed that male sex determination occurred during a specific 12-hour period of ovarian egg development. Exposure of eggs to 400 nM methyl farnesoate during this sensitive developmental period resulted in the production of all-male broods of offspring, while exposure to concentrations as low as 52 nM produced mixed broods of males and females. This active concentration range of methyl farnesoate is consistent with levels measured in the hemolymph of some decapod crustaceans. These results demonstrate that methyl farnesoate is capable of programming daphnid embryos to develop into males and is likely the endocrine factor responsible for initiating the sexual reproductive phase in these organisms.

Localization of the Genetic Determinants of Meiosis Suppression in Daphnia pulex

“…Only a fraction of D. pulex are capable of male production, and although the genetic details remain to be worked out, the limited crosses that have been made between maleand nonmale-producing clones appear to be qualitatively consistent with a single-locus model in which individuals with male/female function are either MM or Mm and those incapable of male production are mm, with a dominant allele (or tight linkage group) M conferring the ability to produce males (Innes and Dunbrack 1993;Innes 1997;Tessier and Cáceres 2004). However, none of the significant markers that we identified in obligate asexuals were associated with the ability to produce males (revealed by application of male-inducing methyl farnesoate; Olmstead and Leblanc 2002). In addition, our broad geographic survey provides little support for the hypothesis that obligate asexuals tend to lose the ability to produce males (Innes et al 2000), as 59% (n ¼ 39) of the sexual clones and 52% (n ¼ 40) of the asexual clones in our survey produce males.…”

Endocrine regulation of the reproduction in crustaceans: Identification of potential targets for toxicants and environmental contaminants

“…Similarly, occurrence of male nauplii increased in T. battagliai exposed only to 86.5 µg L −1 of 20-HE, while less pronounced effects were recorded at lower or higher concentrations ranging 8.7-269 µg L −1 (Hutchinson et al 1999b). Also MF (5-30 µg L −1 ) stimulated male occur- rence in D. pulex offspring (Olmstead & Leblanc 2002) with the most sensitive period between 48-72 hours of neonates age. Similar effects have also been found for juvenile hormone antagonist methoprene that induced exclusive production of males in D. pulex exposed to 10 and 100 µg L −1 (Peterson et al 2001).…”

Ecological genomics in Daphnia: stress responses and environmental sex determination

“…Studies with MF demonstrate that D. magna and D. pulex produce male broods in a dose-dependent manner, with concentrations above 300 nM resulting in all male broods (Olmstead and LeBlanc, 2002;personal observation). Furthermore, the sensitive period for MF induction of male development is 1-2 days before egg laying during the vitellogenic period of oogenesis.…”

“…Fourth, evidence indicates important couplings between juvenile hormone (JH) pathways and ecdysone pathways in Daphnia (Mu and LeBlanc, 2004), which are likely to be useful for genetic and genomic analyses of these pathways across the Ecdysozoa. Olmstead and LeBlanc (2002) were first to demonstrate production of male broods of D. magna in response to the sesquiterpenoid hormone methyl farnesoate (MF), the unepoxidated form of insect JH III. Discovery of MF in crustaceans prompted extensive efforts to characterize the functions of this hormone, which largely appears to mirror the effects of JH in insects (Laufer and Biggers, 2001).…”