Endocrine regulation of predator-induced phenotypic plasticity

Abstract

Elucidating the developmental and genetic control of phenotypic plasticity remains a central agenda in evolutionary ecology. Here, we investigate the physiological regulation of phenotypic plasticity induced by another organism, specifically predator-induced phenotypic plasticity in the model ecological and evolutionary organism Daphnia pulex. Our research centres on using molecular tools to test among alternative mechanisms of developmental control tied to hormone titres, receptors and their timing in the life cycle. First, we synthesize detail about predator-induced defenses and the physiological regulation of arthropod somatic growth and morphology, leading to a clear prediction that morphological defences are regulated by juvenile hormone and life-history plasticity by ecdysone and juvenile hormone. We then show how a small network of genes can differentiate phenotype expression between the two primary developmental control pathways in arthropods: juvenoid and ecdysteroid hormone signalling. Then, by applying an experimental gradient of predation risk, we show dose-dependent gene expression linking predator-induced plasticity to the juvenoid hormone pathway. Our data support three conclusions: (1) the juvenoid signalling pathway regulates predator-induced phenotypic plasticity; (2) the hormone titre (ligand), rather than receptor, regulates predator-induced developmental plasticity; (3) evolution has favoured the harnessing of a major, highly conserved endocrine pathway in arthropod development to regulate the response to cues about changing environments (risk) from another organism (predator).

Fig. 1

Exposure to chemical cues from midge (Chaoborus flavicans) larvae results in a defended phenotype in Daphnia pulex. a Second-instar daphnid exhibiting a defended morphology. b An undefended second-instar daphnid

Fig. 2

Relative expression of the five genes in the proposed mini gene network. Significant predator kairomone dose-dependent upregulation of Dappu-EcRb, Dappu-HR3 and Dappu-HB2 expression are consistent with an increase in juvenoid hormone titres. Inset: a five-gene network, dominated by nuclear receptors central to arthropod development, that can discriminate between activity in the ecdysteroid and juvenoid endocrine pathways. Solid lines indicate upregulation (more expression) and dashed lines indicate downregulation (less expression). Thicker vs. thinner lines indicate relative (qualitative) magnitudes of gene expression