Live‐fast‐die‐young: Carryover effects of heatwave‐exposed adult urchins on the development of the next generation

• Published in: Global change biology Vol. 28; no. 19; pp. 5781 - 5792
• Main Authors: Minuti, Jay J., Byrne, Maria, Campbell, Hamish, Hemraj, Deevesh A., Russell, Bayden D.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01-10-2022; John Wiley and Sons Inc
• Subjects: Acclimatization; Adults; Animals; carryover effects; climate change; Conditioning; Echinoidea; Exposure; Extreme weather; Heat waves; Heatwaves; Heliocidaris erythrogramma; Hot Temperature; Humans; Juveniles; Larval stage; marine heatwave; Marine invertebrates; Metamorphosis; Minors; Ocean temperature; Offspring; Physiology; Progeny; sea urchin; Sea Urchins; Seasons; Summer; Survival; Temperature; Temperature gradients; Temperature tolerance; thermal physiology; Thermal stress; marine heatwave; Heliocidaris erythrogramma; sea urchin; carryover effects; thermal physiology; climate change
• ISSN: 1354-1013; 1365-2486; 1365-2486
• DOI: 10.1111/gcb.16339

With rising ocean temperatures, extreme weather events such as marine heatwaves (MHWs) are increasing in frequency and duration, pushing marine life beyond their physiological limits. The potential to respond to extreme conditions through physiological acclimatization, and pass on resistance to the next generation, fundamentally depends on the capacity of an organism to cope within their thermal tolerance limits. To elucidate whether heat conditioning of parents could benefit offspring development, we exposed adult sea urchins (Heliocidaris erythrogramma) to ambient summer (23°C), moderate (25°C) or strong (26°C) MHW conditions for 10 days. Offspring were then reared at constant temperature along a thermal gradient (22–28°C) and development was tracked to the 14‐day juvenile stage. Progeny from the MHW‐conditioned adults developed through to metamorphosis faster than those of ambient conditioned parents, with most individuals from the moderate and strong heatwaves developing to the larval stage across all temperatures. In contrast, the majority of offspring from the control summer temperature died before metamorphosis at temperatures above 25°C (moderate MHW). Juveniles produced from the strong MHW‐conditioned adults were also larger across all temperatures, with the largest juveniles in the 26°C treatment. In contrast, the smallest juveniles were from control (current‐day summer) parents (and reared at 22 and 25°C). Surprisingly, initial survival was higher in the progeny of MHW exposed parents, even at temperatures hotter than predicted MHWs (28°C). Importantly, however, there was substantial mortality of juveniles from the strong MHW parents by day 14. Therefore, while carryover effects of parental conditioning to MHWs resulted in faster growing, larger progeny, this benefit will only persist beyond the more sensitive juvenile stage and enhance survival if conditions return promptly to normal seasonal temperatures within current thermal tolerance limits.
Marine heatwaves (MHWs) can have devastating effects on marine ecosystems by driving widespread mortality of organisms, but individuals which survive the thermal stress may be able to pass heat tolerance to their offspring. We show that MHW‐conditioned sea urchins produce faster‐growing, larger and more heat tolerant offspring. If heatwaves continued too long, however, there was high mortality even in progeny from heatwave‐exposed parents. Therefore, the beneficial carryover effects of parental conditioning to MHWs will only persist beyond the more sensitive juvenile stage, and enhance survival, if MHWs are not extended and temperatures promptly return to normal.