Transgenerational plasticity and acclimation of tropical sea urchins to ocean warming and acidification

Anthropogenic CO2 emissions are causing the oceans to simultaneously warm and become increasingly acidic, with rates of change that are putting evolutionary pressure on many marine organisms. As a result, both short-term responses and the ability of organisms to acclimate to rapid environmental change through phenotypic plasticity are expected to play a considerable role in persistence of many species under future ocean change. Evidence is accumulating that non-genetic inheritance and transgenerational plasticity (TGP) may be important mechanisms which may facilitate acclimation to ocean warming and acidification. This thesis tests the overarching hypothesis that TGP and parental acclimation to predicted ocean warming and acidification conditions promote greater resilience in offspring using two tropical sea urchins, Tripneustes gratilla and Echinometra sp. A, as model organisms. Echinoderms are an ecologically important group which have been useful models for understanding responses of developmental stages to climate change stressors. However, the majority of existing studies have examined responses within a single generation, with little allowance for acclimation. To date, only a handful of studies have examined the effects of climate stressors on offspring whose parents had also experienced similar environmental conditions. Here, transgenerational responses of T. gratilla were examined in offspring derived from parents raised in ocean warming (+2C/29C) and acidification (-0.3 pH/ pHT 7.77) treatments from juveniles to mature adults, a period encompassing the entirety of gonadogenesis. This study found that although larvae generally performed best when raised in the same treatments as their parents, parental acclimation had a predominantly negative effect on larval size. When raised in control conditions, 2 day old pluteus larvae derived from parents acclimated to warming and/or acidification were consistently smaller, with reductions in postoral arm lengths of up to 21%, compared to larvae derived from parents raised in control conditions. These results indicate that acclimation to predicted warming and acidification conditions may result in fitness trade-offs during early development, which may have consequences for later developmental stages and survival in the form of negative carryover effects. A longer-term study followed development of Echinometra sp. A progeny (throughout development to near competency) derived from parents maintained for two years in either present-day (ambient) conditions (mean = 26C/pHT 8.10) or warming (+2C/mean = 28C) and acidification (-0.3 pH/ pHT 7.80) conditions predicted for the year 2100. Egg size as well as larval survival, morphology, and respiration were quantified, and molecular analyses were performed to gain a better understanding of mechanisms underlying acclimation. Egg size was not affected by parental treatment, but larvae derived from parents acclimated to conditions predicted for the year 2100 were larger and developed faster than larvae derived from parents maintained in ambient, present-day conditions. However, offspring of urchins acclimated to predicted 2100 conditions had higher mortality than offspring of urchins cultured in present-day conditions, with up to 38% higher mortality by the time they were reaching competency at 15 days post-fertilisation. When raised in 2100 conditions, respiration rates of larvae derived from 2100 acclimated parents increased 109% while respiration rates of offspring derived from present-day parents decline 36.8%, suggesting that mortality may have been due to higher energetic consumption. Molecular analysis found that gene expression patterns in gastrula stages were strongly influenced by the environment experienced by parents. Gastrula derived from parents acclimated to predicted 2100 conditions upregulated genes involved in biomineralisation, suggesting greater allocation of energy toward calcification, which may have influenced the higher growth rates seen in these larvae. Later stage pluteus larvae showed far fewer differences in gene expression among treatments, and in contrast to gastrula stages, differences were primarily driven by the environment experienced by larvae. These results may indicate that early developmental stages were primed for similar environments to those experienced by parents while later developmental stages may be more capable of responding to their own environmental conditions. The research presented in this thesis partially supports the hypothesis that TGP and parental acclimation to ocean warming and acidification results in offspring that are more optimally suited to future ocean conditions. Reallocation of energy and resources may result in fitness gains in one developmental trait or stage while compromising another. Fitness trade-offs may be an important outcome and the results of these studies highlight the complex nature of transgenerational plasticity and acclimation to future ocean conditions.

Effects of Ocean Acidification on Developmental Thermal Windows of Echinoderms

Under future ocean warming, thermal tolerance of developmental stages may be a key driver of changes in the geographical distributions and abundance of marine invertebrates. Additional stressors such as ocean acidification may influence thermal windows and are therefore important considerations under realistic future climate change scenarios. The effects of reduced seawater pH on the thermal windows of fertilisation, embryology and larval morphology were examined using five echinoderm species; two polar (Sterechinus neumayeri and Odontaster validus), two temperate (Fellaster zelandiae and Patiriella regularis) and one tropical (Arachnoides placenta). Using a thermal heat block, heated and cooled at each end to create a temperature gradient, responses were examined across 12 temperatures ranging from -1.1 –5.7 C (S. neumayeri), -0.5 –10.7 C (O. validus), 5.8 –27 C (F. zelandiae), 6 –27.1 C (P. regularis) and 13.9 –34.8 C (A. placenta) under present day and near future (2100+) ocean acidification conditions to test the hypothesis that a synergistic interaction between temperature and reduced seawater pH would result in a narrowing of thermal windows. Thermal windows for fertilisation were broad and were not influenced by seawater pH. Optimal thermal windows for fertilisation were -1.1 –4.3 C for S. neumayeri, -0.5 –10.1 C for O. validus, 17.7 –25.4 C for F. zelandiae, 15.8 –23.4 C for P. regularis and 18.9 –32.2 C for A. placenta. Embryological development was less thermotolerant, with thermal windows ranging from -1.1 –1.35 C for S. neumayeri, -0.5 –5.6 C for O. validus, 10 –19.7 C for F. zelandiae, 10.1 –21.3 C for P. regularis and 20 –31 C for A. placenta. Although near future pH significantly reduced normal development for S. neumayeri, O. validus, P. regularis, and A. placenta, it did not affect the thermal windows for embryonic development. Thermal windows for larval development ranged from -1.1 –3.8 C for S. neumayeri, -0.5 –7.6 C for O. validus, 10 –25 C for F. zelandiae, 11.9 –23.2 C for P. regularis and 20 –32.2 C for A. placenta. Thermal windows were not influenced by seawater pH, however, larvae of S. neumayeri, F. zelandiae, P. regularis and A. placenta reared in reduced pH treatments were significantly smaller than those reared in ambient pH treatments. Postoral arm symmetry of echinoids was not affected by reduced pH, indicating that size reductions were due to developmental delay as opposed to abnormal development. Bipinnaria larvae of O. validus reared in reduced seawater pH had longer body lengths on average than larvae in ambient pH treatments. Contrary to the overarching hypothesis, effects of reduced seawater pH on thermal windows were additive, with no evidence of a synergism between temperature and pH causing thermal windows to narrow, nor was there an antagonistic effect in which temperature buffered deleterious effects of reduced pH. Results of this study suggest that in terms of fertilisation and development, temperature may be the most important factor influencing species’ latitudinal distributions in future ocean conditions, and that there is little evidence of a synergistic effect of ocean acidification on this thermal response. If this is the case, warming may reduce northern ranges of S. neumayeri and A. placenta, which are both found at the upper limits of their thermal tolerance. Ocean warming may facilitate pole-ward range expansions of F. zelandiae and P. regularis if temperature currently limits their southern distributions. The current range of O. validus does not appear to be controlled by temperature, therefore, ocean warming is unlikely to directly effect latitudinal distribution. In all cases, ocean acidification is not likely to play a synergistic role in future species distributions

Effects of Ocean Acidification on Developmental Thermal Windows of Echinoderms

Under future ocean warming, thermal tolerance of developmental stages may be a key driver of changes in the geographical distributions and abundance of marine invertebrates. Additional stressors such as ocean acidification may influence thermal windows and are therefore important considerations under realistic future climate change scenarios. The effects of reduced seawater pH on the thermal windows of fertilisation, embryology and larval morphology were examined using five echinoderm species; two polar (Sterechinus neumayeri and Odontaster validus), two temperate (Fellaster zelandiae and Patiriella regularis) and one tropical (Arachnoides placenta). Using a thermal heat block, heated and cooled at each end to create a temperature gradient, responses were examined across 12 temperatures ranging from -1.1 –5.7 C (S. neumayeri), -0.5 –10.7 C (O. validus), 5.8 –27 C (F. zelandiae), 6 –27.1 C (P. regularis) and 13.9 –34.8 C (A. placenta) under present day and near future (2100+) ocean acidification conditions to test the hypothesis that a synergistic interaction between temperature and reduced seawater pH would result in a narrowing of thermal windows. Thermal windows for fertilisation were broad and were not influenced by seawater pH. Optimal thermal windows for fertilisation were -1.1 –4.3 C for S. neumayeri, -0.5 –10.1 C for O. validus, 17.7 –25.4 C for F. zelandiae, 15.8 –23.4 C for P. regularis and 18.9 –32.2 C for A. placenta. Embryological development was less thermotolerant, with thermal windows ranging from -1.1 –1.35 C for S. neumayeri, -0.5 –5.6 C for O. validus, 10 –19.7 C for F. zelandiae, 10.1 –21.3 C for P. regularis and 20 –31 C for A. placenta. Although near future pH significantly reduced normal development for S. neumayeri, O. validus, P. regularis, and A. placenta, it did not affect the thermal windows for embryonic development. Thermal windows for larval development ranged from -1.1 –3.8 C for S. neumayeri, -0.5 –7.6 C for O. validus, 10 –25 C for F. zelandiae, 11.9 –23.2 C for P. regularis and 20 –32.2 C for A. placenta. Thermal windows were not influenced by seawater pH, however, larvae of S. neumayeri, F. zelandiae, P. regularis and A. placenta reared in reduced pH treatments were significantly smaller than those reared in ambient pH treatments. Postoral arm symmetry of echinoids was not affected by reduced pH, indicating that size reductions were due to developmental delay as opposed to abnormal development. Bipinnaria larvae of O. validus reared in reduced seawater pH had longer body lengths on average than larvae in ambient pH treatments. Contrary to the overarching hypothesis, effects of reduced seawater pH on thermal windows were additive, with no evidence of a synergism between temperature and pH causing thermal windows to narrow, nor was there an antagonistic effect in which temperature buffered deleterious effects of reduced pH. Results of this study suggest that in terms of fertilisation and development, temperature may be the most important factor influencing species’ latitudinal distributions in future ocean conditions, and that there is little evidence of a synergistic effect of ocean acidification on this thermal response. If this is the case, warming may reduce northern ranges of S. neumayeri and A. placenta, which are both found at the upper limits of their thermal tolerance. Ocean warming may facilitate pole-ward range expansions of F. zelandiae and P. regularis if temperature currently limits their southern distributions. The current range of O. validus does not appear to be controlled by temperature, therefore, ocean warming is unlikely to directly effect latitudinal distribution. In all cases, ocean acidification is not likely to play a synergistic role in future species distributions

Transgenerational plasticity and acclimation of tropical sea urchins to ocean warming and acidification

Anthropogenic CO2 emissions are causing the oceans to simultaneously warm and become increasingly acidic, with rates of change that are putting evolutionary pressure on many marine organisms. As a result, both short-term responses and the ability of organisms to acclimate to rapid environmental change through phenotypic plasticity are expected to play a considerable role in persistence of many species under future ocean change. Evidence is accumulating that non-genetic inheritance and transgenerational plasticity (TGP) may be important mechanisms which may facilitate acclimation to ocean warming and acidification. This thesis tests the overarching hypothesis that TGP and parental acclimation to predicted ocean warming and acidification conditions promote greater resilience in offspring using two tropical sea urchins, Tripneustes gratilla and Echinometra sp. A, as model organisms. Echinoderms are an ecologically important group which have been useful models for understanding responses of developmental stages to climate change stressors. However, the majority of existing studies have examined responses within a single generation, with little allowance for acclimation. To date, only a handful of studies have examined the effects of climate stressors on offspring whose parents had also experienced similar environmental conditions. Here, transgenerational responses of T. gratilla were examined in offspring derived from parents raised in ocean warming (+2C/29C) and acidification (-0.3 pH/ pHT 7.77) treatments from juveniles to mature adults, a period encompassing the entirety of gonadogenesis. This study found that although larvae generally performed best when raised in the same treatments as their parents, parental acclimation had a predominantly negative effect on larval size. When raised in control conditions, 2 day old pluteus larvae derived from parents acclimated to warming and/or acidification were consistently smaller, with reductions in postoral arm lengths of up to 21%, compared to larvae derived from parents raised in control conditions. These results indicate that acclimation to predicted warming and acidification conditions may result in fitness trade-offs during early development, which may have consequences for later developmental stages and survival in the form of negative carryover effects. A longer-term study followed development of Echinometra sp. A progeny (throughout development to near competency) derived from parents maintained for two years in either present-day (ambient) conditions (mean = 26C/pHT 8.10) or warming (+2C/mean = 28C) and acidification (-0.3 pH/ pHT 7.80) conditions predicted for the year 2100. Egg size as well as larval survival, morphology, and respiration were quantified, and molecular analyses were performed to gain a better understanding of mechanisms underlying acclimation. Egg size was not affected by parental treatment, but larvae derived from parents acclimated to conditions predicted for the year 2100 were larger and developed faster than larvae derived from parents maintained in ambient, present-day conditions. However, offspring of urchins acclimated to predicted 2100 conditions had higher mortality than offspring of urchins cultured in present-day conditions, with up to 38% higher mortality by the time they were reaching competency at 15 days post-fertilisation. When raised in 2100 conditions, respiration rates of larvae derived from 2100 acclimated parents increased 109% while respiration rates of offspring derived from present-day parents decline 36.8%, suggesting that mortality may have been due to higher energetic consumption. Molecular analysis found that gene expression patterns in gastrula stages were strongly influenced by the environment experienced by parents. Gastrula derived from parents acclimated to predicted 2100 conditions upregulated genes involved in biomineralisation, suggesting greater allocation of energy toward calcification, which may have influenced the higher growth rates seen in these larvae. Later stage pluteus larvae showed far fewer differences in gene expression among treatments, and in contrast to gastrula stages, differences were primarily driven by the environment experienced by larvae. These results may indicate that early developmental stages were primed for similar environments to those experienced by parents while later developmental stages may be more capable of responding to their own environmental conditions. The research presented in this thesis partially supports the hypothesis that TGP and parental acclimation to ocean warming and acidification results in offspring that are more optimally suited to future ocean conditions. Reallocation of energy and resources may result in fitness gains in one developmental trait or stage while compromising another. Fitness trade-offs may be an important outcome and the results of these studies highlight the complex nature of transgenerational plasticity and acclimation to future ocean conditions.