The endocrine control of reproduction in Nereidae: a new multi-hormonal model with implications for their functional role in a changing environment

Abstract

Nereidae are vital to the functioning of estuarine ecosystems and are major components in the diets of over-wintering birds and commercial fish. They use environmental cues to synchronize reproduction. Photoperiod is the proximate cue, initiating vitellogenesis in a temperature-compensated process. The prevailing paradigm in Nereidae is of a single 'juvenile' hormone controlling growth and reproduction. However, a new multi-hormone model is presented here that integrates the environmental and endocrine control of reproduction. This is supported by evidence from in vitro bioassays. The juvenile hormone is shown to be heat stable and cross reactive between species. In addition, a second neuro-hormone, identified here as a gonadotrophic hormone, is shown to be present in mature females and is found to promote oocyte growth. Furthermore, dopamine and melatonin appear to switch off the juvenile hormone while serotonin and oxytocin promote oocyte growth. Global warming is likely to uncouple the phase relationship between temperature and photoperiod, with significant consequences for Nereidae that use photoperiod to cue reproduction during the winter in northern latitudes. Genotypic adaptation of the photoperiodic response may be possible, but significant impacts on fecundity, spawning success and recruitment are likely in response to short-term extreme events. Endocrine-disrupting chemicals may also impact on putative steroid hormone pathways in Nereidae with similar consequences. These impacts may have significant implications for the functional role of Nereidae and highlight the importance of comparative endocrinology studies in these and other invertebrates.

Figure 1.

The average increase in diameter of P. dumerilii oocytes incubated in vitro with no ganglia (NB), juvenile P. dumerilii ganglia (JB), mature female P. dumerilii ganglia (FB) and mature male P. dumerilii ganglia (MB) and compared with an initial oocyte measurement. Bars denote standard error of the means. (a) Assay performed over 4 days. There were highly significant differences between treatments using a Kruskal–Wallis test, with Mann–Whitney U pair-wise comparisons (n = 500, χ² = 440.65, d.f. = 4, p < 0.001). (b) Assay performed over 5 days. Two-way ANOVA showed that both treatment and time had a significant effect on the data (p < 0.001). A significant interaction between the two was also observed (p < 0.001). Games–Howell post hoc analysis found significant differences between each of the treatment group except the juvenile ganglia with the initial reading (p > 0.74).

Figure 2.

The average increase in diameter of P. dumerilii and N. succinea oocytes incubated in vitro and compared with an initial oocyte measurement. Bars denote the standard error of the means. (a) Platynereis dumerilii oocytes incubated with no ganglia (NB), juvenile P. dumerilii ganglia (JB), mature female P. dumerilii ganglia (FB), boiled juvenile P. dumerilii ganglia (BJB) and juvenile Nereis virens ganglia (NVB). There was a highly significant difference between treatments using the Kruskal–Wallis test (n = 500, χ² = 1600.70, d.f. = 5, p < 0.001). (b) Nereis succinea oocytes incubated with no ganglia (NB), juvenile P. dumerilii ganglia (JB), mature female P. dumerilii ganglia (FB) and juvenile N. succinea ganglia (JNSB). There were significant differences between the treatments using the Kruskal–Wallis test (n = 250, χ² = 325.47, d.f. = 4, p < 0.001).

Figure 3.

The average increase in diameter of N. succinea oocytes incubated in vitro with no ganglia (NB), juvenile P. dumerilii ganglia (JB), mature female P. dumerilii ganglia (FB), juvenile ganglia incubated for 3 days in vivo with dopamine (10 µg ml⁻¹) (JBD), melatonin (10 µg ml⁻¹) (JBM), serotonin (10 µg ml⁻¹) (JBS) and oxytocin (10 µg ml⁻¹) (JBO). Bars denote the standard error of the means. There was a highly significant difference between treatments using the Kruskal–Wallace test (n = 250, χ² = 544.46, d.f. = 7, p < 0.001).

Figure 4.

A multi-hormonal model showing the interaction between environmental and endocrine factors controlling the reproductive cycle of Nereis. JH, juvenile hormone; GH, gonadotrophic hormone.