Males on demand: the environmental–neuro‐endocrine control of male sex determination in daphnids

Abstract

Branchiopod crustaceans (e.g., Daphnia sp.) and some other taxa utilize both asexual and sexual reproduction to maximize population sustainability. The decision to switch from asexual to sexual reproduction is triggered by environmental cues that foretell a potentially detrimental change in environmental conditions. This review describes the cascade of events beginning with environmental cues and ending with changes in gene expression that dictate male sex determination in daphnids, the initial event in the switch to sexual reproduction. Several environmental cues have been identified which, either in isolation or in combination, stimulate male sex determination. These cues are typically associated with change of season, exhaustion of resources or loss of habitat. Maternal daphnids receive and respond to these cues, we propose, through the secretion of neuropeptides, which suppress (hyperglycemic hormone‐like neuropeptides, allatostatin) or stimulate (allatotropin) the male sex differentiation program. In response, maternal daphnids produce the male sex‐determining hormone, methyl farnesoate. Methyl farnesoate binds to a protein MET that dimerizes with the protein SRC forming an active transcription factor. This complex then regulates the expression of genes, primarily doublesex (dsx), involved in programming the single‐celled embryo to develop into a male. In the absence of methyl farnesoate programming, the embryo develops into a female. Epigenetic modifications of the genome as a possible mode of methyl farnesoate action and the utility of this model to decipher the role of epigenetics in sex differentiation in other species are discussed.

De Novo Transcriptome Assembly and Sex-Biased Gene Expression in the Cyclical ParthenogeneticDaphnia galeata

“…Male sex-determination in daphnids is initiated by environmental cues leading to synthesis of MF, an analog of JH III produced in the mandibular gland. MF signals are perceived by a methyl-farnesonate receptor (MfR) (LeBlanc and Medlock 2015; Toyota, Miyakawa, Yamaguchi, et al 2015) leading to a downstream cascade that ultimately produces the male phenotype. We thus searched the D. galeata transcriptome for genes from the JH pathway that have been shown to contribute to MF synthesis and signaling.…”

“…The signaling cascade leading to MF production in response to environmental cues remains to be elucidated. A recent study showed that the NMDA receptor seems to be involved in signaling upstream of MF and may be a sensor of environmental stimuli (LeBlanc and Medlock 2015; Toyota, Miyakawa, Yamaguchi, et al 2015). In addition, exogenous treatment with MF and other JH III analogs induces male production in a dose-dependent manner (Olmstead and LeBlanc 2002; Tatarazako et al 2003; Ginjupalli and Baldwin 2013).…”

Agonist-mediated assembly of the crustacean methyl farnesoate receptor

“…Environmental cues, such as photoperiod, temperature, population density and food availability alter reproductive patterns in some crustacean species58911. The hormone, methyl farnesoate, is recognized as mediating many of these actions18.…”

“…For example, some branchiopod crustaceans exclusively produce female offspring via parthenogenesis under certain environmental conditions. However, in response to environmental cues, that denote pending environmental adversity, maternal organisms produce methyl farnesoate which programs oocytes to develop into males5. Further, some environmental chemicals, known as insect growth regulating insecticides (IGRs), can stimulate male sex determination in some crustacean species67.…”

When males outlive females: Sex‐specific effects of temperature on lifespan in a cyclic parthenogen

“…A single genotype can express a multitude of phenotypes depending on the environment it experiences (see e.g., Colbourne et al., ; Tollrian, ), and also sex is environmentally determined. Although males and females are genetically identical (Hebert & Ward, ; LeBlanc & Medlock, ), they differ in morphology and physiology (MacArthur & Baillie, ,b; Mitchell, ). Also, the sexes seem to show different life history strategies to maximize fitness.…”