Different as night and day: Behavioural and life history responses to varied photoperiods in Daphnia magna

Abstract

Nearly all animal species have utilized photoperiod to cue seasonal behaviours and life history traits. We investigated photoperiod responses in keystone species, Daphnia magna, to identify molecular processes underlying ecologically important behaviours and traits using functional transcriptomic analyses. Daphnia magna were photoperiod-entrained immediately posthatch to a standard control photoperiod of 16 light/ 8 dark hours (16L:8D) relative to shorter (4L:20D, 8L:16D, 12L:12L) and longer (20L:4D) day length photoperiods. Short-day photoperiods induced significantly increased light-avoidance behaviours relative to controls. Correspondingly, significant differential transcript expression for genes involved in glutamate signalling was observed, a critical signalling pathway in arthropod light-avoidance behaviour. Additionally, period circadian protein and proteins coding F-box/LRR-repeat domains were differentially expressed which are recognized to establish circadian rhythms in arthropods. Indicators of metabolic rate increased in short-day photoperiods which corresponded with broadscale changes in transcriptional expression across system-level energy metabolism pathways. The most striking observations included significantly decreased neonate production at the shortest day length photoperiod (4L:20D) and significantly increased male production across short-day and equinox photoperiods (4L:20D, 8L:16D and 12L:12D). Transcriptional expression consistent with putative mechanisms of male production was observed including photoperiod-dependent expression of transformer-2 sex-determining protein and small nuclear ribonucleoprotein particles (snRNPs) which control splice variant expression for genes like transformer. Finally, increased transcriptional expression of glutamate has also been shown to induce male production in Daphnia pulex via photoperiod-sensitive mechanisms. Overall, photoperiod entrainment affected molecular pathways that underpin critical behavioural and life history traits in D. magna providing fundamental insights into biological responses to this primary environmental cue.

Keywords: Daphnia behaviour; Daphnia life history; male production; photoperiod; phototaxis.

Figure 1

Cumulative reproductive output expressed as (a) average total neonates by experiment and pooled average total neonates from both experiments and (b) per cent male neonates across the five experimental photoperiods. Error bars represent standard deviations, and asterisks denote a statistically significant difference (p = .05) relative to the control (16L:8D photoperiod)

Figure 2

Effect of photoperiod on metabolic rate in Daphnia magna (from experimental trial 1, n = 8–11), as estimated by metabolism of fluorescently labelled sugar molecules and quantified as pixel intensity from whole‐animal images. Error bars represent standard deviations, and asterisks denote a statistically significant differences (p = .05) relative to the control photoperiod (16L:8D)

Figure 3

Phototaxis investigation summarizing Daphnia magna behavioural data in the phototaxis chamber for 7‐day‐olds (panels a and b) and 21‐day‐olds (panels c and d). The duration of time spent in light versus dark zones is summarized in panels (a) and (c), while swimming velocity is summarized in panels (b) and (d). These results represent the combined data for the two experimental trials (n = 6). Black bars indicate the dark zone, while white bars indicate the light zone. Error bars represent standard deviations. The “S” and “NS” designations denote significant and nonsignificant differences (p = .05), respectively, in time spent in light versus dark zones within each photoperiod

Figure 4

Transcript expression for gene targets having significant differential expression in response to photoperiod relative to the 16L:8D control that were involved in neuroactive ligand–receptor interactions (NLRI). Association with NLRI is based on KEGG orthology (KO) annotations. Fold changes represent means of all replicates, and error bars represent one standard deviation. Results provided for each individual experimental block