Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish

Abstract

Life cycle delays are beneficial for opportunistic species encountering suboptimal environments. Many animals display a programmed arrest of development (diapause) at some stage(s) of their development, and the diapause state may or may not be associated with some degree of metabolic depression. In this review, we will evaluate current advancements in our understanding of the mechanisms responsible for the remarkable phenotype, as well as environmental cues that signal entry and termination of the state. The developmental stage at which diapause occurs dictates and constrains the mechanisms governing diapause. Considerable progress has been made in clarifying proximal mechanisms of metabolic arrest and the signaling pathways like insulin/Foxo that control gene expression patterns. Overlapping themes are also seen in mechanisms that control cell cycle arrest. Evidence is emerging for epigenetic contributions to diapause regulation via small RNAs in nematodes, crustaceans, insects, and fish. Knockdown of circadian clock genes in selected insect species supports the importance of clock genes in the photoperiodic response that cues diapause. A large suite of chaperone-like proteins, expressed during diapause, protects biological structures during long periods of energy-limited stasis. More information is needed to paint a complete picture of how environmental cues are coupled to the signal transduction that initiates the complex diapause phenotype, as well as molecular explanations for how the state is terminated. Excellent examples of molecular memory in post-dauer animals have been documented in Caenorhabditis elegans It is clear that a single suite of mechanisms does not regulate diapause across all species and developmental stages.

The African turquoise killifish: A research organism to study vertebrate aging and diapause

“…As a consequence, it helps the species survive extreme forms of stress (e.g., drought) and it also “times” the birth of offspring to a more favorable environment (e.g., rainy season). In nature, diapause phenomena are widespread throughout the animal kingdom, from simple organisms such as brine shrimps and silkworms, to mammals such as the roe deer, bats, and mice (Bleier, 1975; Emerson, Bradshaw & Holzapfel, 2009; Hand, Denlinger, Podrabsky & Roy, 2016; Lambert et al., 2001; Lopes, Desmarais & Murphy, 2004; Meenakumari & Krishna, 2005; Ptak et al., 2012; Sato et al., 2014; Schiesari & O'Connor, 2013; Sim & Denlinger, 2013). Our current knowledge of diapause has benefited greatly from the studies in invertebrates.…”

“…Diapause can occur at different developmental stages in diverse species (Hand et al., 2016; Lopes et al., 2004; Mead, 1993; Ptak et al., 2012). In killifishes, diapause can occur during early, intermediate, and late developmental stages (diapause I, II, and III, respectively; Wourms, 1972).…”

Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus

“…Cellular metabolism, growth and proliferation are severely downregulated in most organisms that arrest development (Hand et al, 2016). The mechanisms responsible for developmental arrest are not completely understood in any species, but a wealth of evidence points to the central importance of IGF signaling in regulating entrance into metabolic dormancy.…”

Association between gut microbiota and diapause preparation in the cabbage beetle: a new perspective for studying insect diapause

“…Many animals, such as nematodes, crustaceans, fish and insects, have evolved diapause (a programmed arrest of development during specific life stages) to adapt to seasonal changes and survive unfavorable environmental conditions12. Diapause-destined individuals generally store large fat reserves for diapause maintenance and post-diapause development134.…”