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.

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.