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Sea urchin reproductive performance in a changing ocean: poor males improve while good males worsen in response to ocean acidification.

ABSTRACT: Ocean acidification (OA) is predicted to be a major driver of ocean biodiversity change. At projected rates of change, sensitive marine taxa may not have time to adapt. Their persistence may depend on pre-existing inter-individual variability. We investigated individual male reproductive performance under present-day and OA conditions using two representative broadcast spawners, the sea urchins Lytechinus pictus and Heliocidaris erythrogramma. Under the non-competitive individual ejaculate scenario, we examined sperm functional parameters (e.g. swimming speed, motility) and their relationship with fertilization success under current and near-future OA conditions. Significant inter-individual differences in almost every parameter measured were identified. Importantly, we observed strong inverse relationships between individual fertilization success rate under current conditions and change in fertilization success under OA. Individuals with a high fertilization success under current conditions had reduced fertilization under OA, while individuals with a low fertilization success under current conditions improved. Change in fertilization success ranged from -67% to +114% across individuals. Our results demonstrate that while average population fertilization rates remain similar under OA and present-day conditions, the contribution by different males to the population significantly shifts, with implications for how selection will operate in a future ocean.

SUBMITTER: Smith KE

PROVIDER: S-EPMC6661356 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Sea urchin reproductive performance in a changing ocean: poor males improve while good males worsen in response to ocean acidification.

Smith Kathryn E KE Byrne Maria M Deaker Dione D Hird Cameron M CM Nielson Clara C Wilson-McNeal Alice A Lewis Ceri C

Proceedings. Biological sciences 20190724 1907

Ocean acidification (OA) is predicted to be a major driver of ocean biodiversity change. At projected rates of change, sensitive marine taxa may not have time to adapt. Their persistence may depend on pre-existing inter-individual variability. We investigated individual male reproductive performance under present-day and OA conditions using two representative broadcast spawners, the sea urchins Lytechinus pictus and Heliocidaris erythrogramma. Under the non-competitive individual ejaculate scena ...[more]

PMID: 31337311

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Project description:In this research we present a transcriptomics analysis of the physiological response of a marine calcifier, Strongylocentrotus purpuratus, to ocean acidification, a decline in ocean pH that results from the absorption of anthropogenic carbon dioxide (CO2). Larvae were raised from fertilization to prism stage in seawater with elevated CO2 conditions based upon IPCC emissions scenario B1 (540ppm CO2) and A1FI (1020ppm CO2). Adult S. purpuratus were collected using SCUBA from Goleta Pier (Goleta,CA, USA) and maintained in flowing seawater tables at 15-16°C. Spawning was induced by coelomic injection of 0.5M KCl following standard methods (Strathmann 1987). Eggs were collected from 3 females and separately fertilized by sperm from a single male (i.e. all larvae were full or half-siblings). Each of the three replicate cultures were divided in three (nine cultures total) and held in 10L flow-through containers filled with seawater aerated through a side arm with commercially manufactured air containing three different pCO2: 380ppm CO2 (present day atmospheric CO2 level, pH 8.01 ± 0.01), 540ppm CO2, an optimistic atmospheric CO2 concentration predicted by the Intergovernmental Panel on Climate Change for 2100 (B1 scenario, pH 7.96 ± 0.01) and 1020ppm CO2 (A1FI scenario, pH 7.88 ± 0.01). Larvae were cultured at 15°C until prism stage (40h post-fertilization). At the 40 hour time point, a sample of 60,000 larvae was removed from each of the 9 cultures in the 380, 540 and 1020 ppm treatments and stored in 1 mL Trizol at -80 ºC for later RNA analysis. The larval cDNA sample from each replicate 540ppm CO2 culture was competitively hybridized against the 380ppm CO2 control culture from the same replicate female. Similarly, the larval cDNA sample from each replicate 1020ppm CO2 culture was competitively hybridized against the 380ppm CO2 control culture from the same replicate female. Using dye swaps of technical replicates, treatment effects could be estimated independently of dye effects.

Project description:Using standard morphometric methods and gene expression profiling with a DNA microarray, we explored the impacts of high CO2 conditions on development of the sea urchin, Lytechinus pictus, a pelagic larvae that forms a calcium carbonate endoskeleton. Larvae were raised from fertilization to pluteus stage in seawater with elevated CO2 conditions based upon IPCC emissions scenarios B1 (540ppm CO2) and A1FI (970ppm CO2). Larval L. pictus were cultured in seawater treated with three different concentrations of CO2. We aerated water in culture chambers with air that had been mixed to different CO2 concentrations chosen from IPCC predictions of future atmospheric CO2 levels (28). The B1 scenario, one of the most optimistic, predicts a stabilization of atmospheric CO2 levels at ~540 ppm by 2100, and the A1F1 scenario, which, reflecting a more âbusiness as usualâ scenario, predicts atmospheric CO2 levels of ~970 ppm by 2100. Compressed air (~380 ppm CO2) was used as a control condition. The culture chambers were 20 L buckets medified to allow aeration bubbles of the experimental gas to mix with and gently stir the culture water without contacting the larvae. Replacement seawater (0.35 Î¼m filtered) was added at a constant rate of 0.5 L hr-1. Water pH of each chamber was monitored daily using a Radiometer Analytical PHM240 pH meter. Adult L. pictus were maintained in flowing seawater at ambient temperature (~15-18 ÂºC) and fed kelp until use. Spawning was induced by coelomic injection of 0.5 M KCl, and eggs were collected in 0.35 Î¼m-filtered seawater. Eggs from 5 females were combined in approximately equal concentrations. Sperm from a single male was collected in the same way, diluted with filtered seawater and added to the egg mixture; thus, all the larvae are half-siblings. Immediately following fertilization, embryos were split into 12 culture chambers providing four replicates of the three CO2 treatments. At the 48 hour time point, a sample of 40,000 larvae was removed from each of the 8 cultures in the 380 and 970 ppm treatments and stored in1 mL Trizol at -80 ÂºC for later RNA analysis. The larval cDNA samples from each treatment were competitively hybridized on each microarray following a balanced incomplete block design (BIBD) with respect to the assignment of treatments to arrays. In this way, differential expression between all pairs of treatments is estimated with equal precision. Although dye swaps of technical replicates were not used, treatment and dye effects are orthogonal to one another, i.e. treatment effects can be estimated independently of dye effects.

Project description:BACKGROUND: Predicting effects of rapid climate change on populations depends on measuring the effects of climate stressors on performance, and potential for adaptation. Adaptation to stressful climatic conditions requires heritable genetic variance for stress tolerance present in populations. METHODOLOGY/PRINCIPAL FINDINGS: We quantified genetic variation in tolerance of early development of the ecologically important sea urchin Centrostephanus rodgersii to near-future (2100) ocean conditions projected for the southeast Australian global change hot spot. Multiple dam-sire crosses were used to quantify the interactive effects of warming (+2-4 °C) and acidification (-0.3-0.5 pH units) across twenty-seven family lines. Acidification, but not temperature, decreased the percentage of cleavage stage embryos. In contrast, temperature, but not acidification decreased the percentage of gastrulation. Cleavage success in response to both stressors was strongly affected by sire identity. Sire and dam identity significantly affected gastrulation and both interacted with temperature to determine developmental success. Positive genetic correlations for gastrulation indicated that genotypes that did well at lower pH also did well in higher temperatures. CONCLUSIONS/SIGNIFICANCE: Significant genotype (sire) by environment interactions for both stressors at gastrulation indicated the presence of heritable variation in thermal tolerance and the ability of embryos to respond to changing environments. The significant influence of dam may be due to maternal provisioning (maternal genotype or environment) and/or offspring genotype. It appears that early development in this ecologically important sea urchin is not constrained in adapting to the multiple stressors of ocean warming and acidification. The presence of tolerant genotypes indicates the potential to adapt to concurrent warming and acidification, contributing to the resilience of C. rodgersii in a changing ocean.

Project description:Ocean warming (OW) and acidification (OA) are intensively investigated as they pose major threats to marine organism. However, little effort is dedicated to another collateral climate change stressor, the increased frequency, and intensity of storm events, here referred to as intensified hydrodynamics. A 2-month experiment was performed to identify how OW and OA (temperature: 21°C; pHT: 7.7, 7.4; control: 17°C-pHT7.9) affect the resistance to hydrodynamics in the sea urchin Paracentrotus lividus using an integrative approach that includes physiology, biomechanics, and behavior. Biomechanics was studied under both no-flow condition at the tube foot (TF) scale and flow condition at the individual scale. For the former, TF disk adhesive properties (attachment strength, tenacity) and TF stem mechanical properties (breaking force, extensibility, tensile strength, stiffness, toughness) were evaluated. For the latter, resistance to flow was addressed as the flow velocity at which individuals detached. Under near- and far-future OW and OA, individuals fully balanced their acid-base status, but skeletal growth was halved. TF adhesive properties were not affected by treatments. Compared to the control, mechanical properties were in general improved under pHT7.7 while in the extreme treatment (21°C-pHT7.4) breaking force was diminished. Three behavioral strategies were implemented by sea urchins and acted together to cope with flow: improving TF attachment, streamlining, and escaping. Behavioral responses varied according to treatment and flow velocity. For instance, individuals at 21°C-pHT7.4 increased the density of attached TF at slow flows or controlled TF detachment at fast flows to compensate for weakened TF mechanical properties. They also showed an absence of streamlining favoring an escaping behavior as they ventured in a riskier faster movement at slow flows. At faster flows, the effects of OW and OA were detrimental causing earlier dislodgment. These plastic behaviors reflect a potential scope for acclimation in the field, where this species already experiences diel temperature and pH fluctuations.

Dataset Information

Sea urchin reproductive performance in a changing ocean: poor males improve while good males worsen in response to ocean acidification.

Publications

Sea urchin reproductive performance in a changing ocean: poor males improve while good males worsen in response to ocean acidification.

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