Impacts of Acclimation in Warm-Low pH Conditions on the Physiology of the Sea Urchin Heliocidaris erythrogramma and Carryover Effects for Juvenile Offspring

Ocean warming (OW) and acidification (OA) affects nearly all aspects of marine organism physiology and it is important to consider both stressors when predicting responses to climate change. We investigated the effects of long-term exposure to OW and OA on the physiology of adults of the sea urchin, Heliocidaris erythrogramma, a species resident in the southeast Australia warming hotspot. The urchins were slowly introduced to stressor conditions in the laboratory over a 7-week adjustment period to three temperature (ambient, +2°C, +3°C) and two pH (ambient: pHT 8.0; −0.4 units: pHT 7.6) treatments. They were then maintained in a natural pattern of seasonal temperature and photoperiod change, and fixed pH, for 22 weeks. Survival was monitored through week 22 and metabolic rate was measured at 4 and 12 weeks of acclimation, feeding rate and ammonia excretion rate at 12 weeks and assimilation efficiency at 13 weeks. Acclimation to +3°C was deleterious regardless of pH. Mortality from week 6 indicated that recent marine heatwaves are likely to have been deleterious to this species. Acclimation to +2°C did not affect survival. Increased temperature decreased feeding and increased excretion rates, with no effect of acidification. While metabolic rate increased additively with temperature and low pH at week 4, there was no difference between treatments at week 12, indicating physiological acclimation in surviving urchins to stressful conditions. Regardless of treatment, H. erythrogramma had a net positive energy budget indicating that the responses were not due to energy limitation. To test for the effect of parental acclimation on offspring responses, the offspring of acclimated urchins were reared to the juvenile stage in OW and OA conditions. Parental acclimation to warming, but not acidification altered juvenile physiology with an increase in metabolic rate. Our results show that incorporation of gradual seasonal environmental change in long-term acclimation can influence outcomes, an important consideration in predicting the consequences of changing climate for marine species.

Evolution of abbreviated development in Heliocidaris erythrogramma dramatically re-wired the highly conserved sea urchin developmental gene regulatory network to decouple signaling center function from ultimate fate

Developmental gene regulatory networks (GRNs) describe the interactions among gene products that drive the differential transcriptional and cell regulatory states that pattern the embryo and specify distinct cell fates. GRNs are often deeply conserved, but whether this is the product of constraint inherent to the network structure or stabilizing selection remains unclear. We have constructed the first formal GRN for early development in Heliocidaris erythrogramma, a species with dramatically accelerated, direct development. This life history switch has important ecological consequences, arose rapidly, and has evolved independently many times in echinoderms, suggesting it is a product of selection. We find that H. erythrogramma exhibits dramatic differences in GRN topology compared with ancestral, indirect-developing sea urchins. In particular, the GRN sub-circuit that directs the early and autonomous commitment of skeletogenic cell precursors in indirect developers appears to be absent in H. erythrogramma, a particularly striking change in relation to both the prior conservation of this sub-circuit and the key role that these cells play ancestrally in early development as the embryonic signaling center. These results show that even highly conserved molecular mechanisms of early development can be substantially reconfigured in a relatively short evolutionary time span, suggesting that selection rather than constraint is responsible for the striking conservation of the GRN among other sea urchins.