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Acclimatisation and Adaptive Capacity of Echinoderms in Response to Ocean Acidification and Warming

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Acclimatisation and Adaptive Capacity of Echinoderms in Response to Ocean Acidification and Warming Acclimatisation and adaptive capacity of echinoderms in response to ocean acidification and warming Kate Marie Sparks Thesis submitted for the degree of Doctor of Philosophy University of Otago Department of Marine Science New Zealand December 2017 Abstract Future ocean acidification and warming pose a substantial threat to the viability of some marine populations. In order to persist, marine species will need to acclimate or adapt to the forecasted changes. Recent research into adaptive capacity of marine species has identified mechanisms of non-genetic inheritance including trans-generational plasticity as important sources of resilience. Based on literature indicating that echinoderms are tolerant to moderate increases in temperature and seawater pCO2, this study hypothesises three outcomes of long-term exposure to combined ocean acidification and warming: 1. Echinoderms possess the genetic capacity to adapt over long time-scales to predicted levels of combined ocean acidification and warming. 2. Echinoderms possess the physiological capability to acclimatize to ocean acidification and warming over long time-scales without a significant cost to metabolic energy budget. 3. After long-term exposure to ocean acidification and warming, echinoderm parents would alter the phenotype (Anticipatory Parental Effect) of their offspring to increase fitness in the F1 generation in response to the environment to which the parents were exposed. Broadcast-spawning echinoderms from the phylum Echinodermata (Fellaster zelandiae; Arachnoides placenta; Acanthaster spp.; Patiriella regularis; Odontaster validus) are used to investigate these hypotheses. 2 Adaptive capacity was investigated using a quantitative genetic approach to examine the response in gastrula-stage offspring of multiple half-sib families raised in fully crossed treatment combinations of temperature (ambient, +2.0, +4.0 °C) and pCO2 (ambient; 2x; 3x ambient ppm). Interactions between genotype and environment were tested using a permutational multivariate ANOVA and restricted error maximum likelihood calculations of variance, and the variance components used to generate genetic correlations (g*E) and broad- sense heritability estimates (h2). Contributions of both genetic and environmental factors to the trait ‘normal development at gastrulation’ were examined for wild populations of all five echinoderm species. Complex interactions between sire (father) and dam (mother) identity and environmental factors were detected for most species, and the individual response to warming of between +2.5 - +3.0 °C and concurrent acidification equivalent to -0.4 pH units depended on phylogeny, genetic identity and environmental exposure history. For all species except O. validus, significant [sire x environment] interactions were found. The response of Acanthaster spp. as well as that of both clypeasteroids (A. placenta and F. zelandiae) to ocean acidification depends on both maternal and paternal lineage, and differences in resilience among genotypes will affect future population response. Maternal lineage (dam identity) was an important factor in every species. For O. validus, the only genetic sources of variation among genotypes came from dam identity and [dam x environment] interactions. The hypothesis that marine populations possess the capacity to adapt to future ocean warming and acidification is therefore supported. 3 Physiological acclimation was investigated in two sea star species: P. regularis and O. validus. Adults were acclimated to combinations of elevated temperature and low pH for 12 months, during which time physiological indices of gonad and pyloric cecum growth rate, righting time and tissue inorganic content were measured every three months. At the same time respiration, energy absorption efficiency, and nitrogenous excretion rates were measured to estimate Scope for Growth (SfG) in all treatments. Adult P. regularis from Dunedin were exposed to all combinations of three pH(T) levels (ambient 8.10, 7.90 and 7.70) and two temperature levels (ambient and +2.50 °C above ambient). SfG in adult P. regularis was reduced by ~48 % through long-term exposure to pH 7.70, but elevated temperature at pH 7.70 enabled some physiological compensation for low SfG i.e. an increase in SfG of ~45 % at pH 7.70/ elevated temperature. Reduced gonad size, pyloric indices and body organic content indicated that P. regularis can re-allocate energy away from gamete production at pH 7.70 in order to maintain homeostasis. Reduced parental investment in offspring due to energy reallocation may carry over into subsequent generations. Adult O. validus from Antarctica were exposed to combinations of a +3.0 °C temperature and -0.4 pH unit decrease for 9 months. There were no reductions in overall SfG of animals subjected to combined warm and acidified seawater. Exposure to elevated temperature in the absence of acidification significantly increased SfG by ~41 % relative to the control treatment. Maintenance of metabolic energy budget was sustained by an increase in food intake to compensate for increased respiration and excretion at elevated temperature and low pH. Animals had the same reproductive capacity in every treatment, indicating that stored 4 energy reserves are sufficient to maintain base metabolism as well as somatic growth and reproductive output. The hypothesis that adult echinoderms exposed to near-future climate- change conditions will be able to acclimate was supported for both species, however P. regularis may still be at risk of physiological distress over multiple generations as it maintains SfG by taking energetic investment away from gametes. Odontaster validus may be one of the most thermally-tolerant polar species and therefore may be one of the ‘winners’ of future climate change. Trans-generational plasticity was investigated in F1 offspring of the P. regularis and O. validus parents used in the long-term acclimation study. F1 offspring were generated using a quantitative genetic breeding design and raised to the gastrula stage in all combinations of elevated temperature and pCO2, either in the same environment as their parents or a different environment. Parent acclimation increased the fitness of F1 gastrulae in response to elevated temperature in O. validus. Broad-sense heritability (h2) was 0.34, indicating that trait plasticity is partly attributable to genetic variation. There was little variation among offspring phenotype attributable to sire identity, but dam identity accounted for 5.79 % of variation among genotypes in the wild population and 23.27 % of variation among genotypes in the F1 population. Maternal identity accounted for 23.27 % of variation among genotypes in the F1 population. Strong maternal effects (m2) were observed at the gastrula stage (m2 = 0.51), indicating that maternal environmental history is a strong determinant factor in non-genetic inheritance. Maternal effects increased trans-generational fitness in response to elevated temperature, and, to a lesser extent, pCO2. These results suggests that O. validus has a pre- adaptive capacity to respond to ocean warming and acidification that may facilitate population persistence over the next century. 5 In P. regularis, parent adaptation to ocean acidification was maladaptive for F1 gastrulae, and this was only partially compensated for by F1 exposure to elevated temperature. Parent exposure to pH 7.70 for 12 months reduced offspring % normal development by ~ 13 % regardless of the offspring temperature or pH environment. Offspring exposure to pH 7.70 reduced % normal development by ~25 %. Among F1 offspring of parents at the end of the exposure period, 17.62 % of variation in % normal development between families was explained by dam identity, and strong maternal effects (m2 = 0.41) were detected. Broad- sense heritability was h2 = 0.06 at ambient pH and h2 = 0.16 at pH 7.70. Maladaptive TGP in response to low pH and strong maternal effects indicate intense natural selection for this population in the near future. The hypothesis that echinoderm parents can alter the fitness of their offspring in response to their own thermal or CO2 environment is supported for O. validus but not P. regularis. This is the first study to combine long-term parent acclimatization to ocean acidification and warming with estimates of broad-sense heritability and trans-generational plasticity in the next generation, and can go some way towards answering questions about the effect of parent environment on non-genetic inheritance and evolutionary fitness. The result of this study have wider implications for predictive models of how Southern Ocean echinoderm species adapt to ocean acidification and warming, and supports the need to exercise caution when using models which predict the responses of temperate marine species from examining their related polar counterparts, or models which use parent environmental stability as a predictor of trans-generational responses to climate change. 6 Acknowledgments I would like to thank my supervisors, Assoc. Prof. Miles Lamare, Prof. Abby Smith and Prof. Steve Wing of the University of Otago, for your unending support, kindness and care throughout this process. Miles, you’ve been a sounding board, lab partner and endless supply of enthusiasm for science and discovery. Abby, you are one of my role models for female scientists, thank you for taking care of me and reminding me to eat, sleep and exercise. Steve, thank you for helping me along in the world of Antarctic science and your generous
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