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PLoS One
2012 Jan 01;712:e53118. doi: 10.1371/journal.pone.0053118.
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Individual variability in reproductive success determines winners and losers under ocean acidification: a case study with sea urchins.
Schlegel P
,
Havenhand JN
,
Gillings MR
,
Williamson JE
.
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BACKGROUND: Climate change will lead to intense selection on many organisms, particularly during susceptible early life stages. To date, most studies on the likely biotic effects of climate change have focused on the mean responses of pooled groups of animals. Consequently, the extent to which inter-individual variation mediates different selection responses has not been tested. Investigating this variation is important, since some individuals may be preadapted to future climate scenarios.
METHODOLOGY/PRINCIPAL FINDINGS: We examined the effect of CO(2)-induced pH changes ("ocean acidification") in sperm swimming behaviour on the fertilization success of the Australasian sea urchin Heliocidaris erythrogramma, focusing on the responses of separate individuals and pairs. Acidification significantly decreased the proportion of motile sperm but had no effect on sperm swimming speed. Subsequent fertilization experiments showed strong inter-individual variation in responses to ocean acidification, ranging from a 44% decrease to a 14% increase in fertilization success. This was partly explained by the significant relationship between decreases in percent sperm motility and fertilization success at ΔpH = 0.3, but not at ΔpH = 0.5.
CONCLUSIONS AND SIGNIFICANCE: The effects of ocean acidification on reproductive success varied markedly between individuals. Our results suggest that some individuals will exhibit enhanced fertilization success in acidified oceans, supporting the concept of ''winners'' and ''losers'' of climate change at an individual level. If these differences are heritable it is likely that ocean acidification will lead to selection against susceptible phenotypes as well as to rapid fixation of alleles that allow reproduction under more acidic conditions. This selection may ameliorate the biotic effects of climate change if taxa have sufficient extant genetic variation upon which selection can act.
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23300876
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Figure 1. Schematic representation of the relationship between fertilization success and sperm concentration of Heliocidaris erythrogramma at different pH levels, assuming a negative pH impact on fertilization.Determining fertilization success at an intermediate sperm concentration (here, the sperm concentration that generates 50% of maximum observed fertilization success in controls) yields maximum sensitivity in the assay. All data in Fig. 1Figure 1 are theoretical. FSRmax Control = maximum fertilization success in Controls; FSR50 Control = 50% of maximum fertilization success in Controls; F
max Control = sperm concentration that generates maximum fertilization success in Controls; F
50 Control = sperm concentration that generates 50% of maximum fertilization success in Controls. FSR50 pH 7.8 = observed fertilization success in pH 7.8 treatment at the sperm concentration that generates 50% of maximum fertilization success in Controls; FSR50 pH 7.6 = observed fertilization success in pH 7.6 at the sperm concentration that generates 50% of maximum fertilization success in Controls. Actual fertilization curves vary for each individual pair.
Figure 2. Impacts of ocean acidification on sperm motility and sperm swimming speed in Heliocidaris erythrogramma.
Proportion of mean (±S.E.) motile sperm (A) and sperm speed (B) at different levels of ocean acidification (pH mediated by CO2 addition). Lower case letters indicate significantly different groups at p = 0.05 (Tukey’s test). (C) Mean logarithmic response ratios (±95% CI) of effects of ocean acidification on percent motility and sperm speed (n = 19).
Figure 3. Effects of ocean acidification on fertilization success (FSR) in H. erythrogramma.(A) Mean (±S.E.) observed (FSRobs) and modelled fertilization success (FSRmod) for pHs 7.6 and 7.8, and mean (±S.E.) FSR50 (50% of maximum FSR) for pH 8.1. (B) Bootstrapped mean logarithmic response ratios (±95% CI) of effects of ocean acidification on FSRobs and FSRmod. FSRmod shows change in fertilization success expected due to ocean acidification’s influence on sperm swimming behaviour (Fig. 2C). (n = 18 replicate trials). See text for details.
Figure 4. Scatterplots for observed (FSRobs) versus modelled (FSRmod) fertilization success for pH 7.8 (A) and 7.6 (B).Regression analyses revealed a significant relationship between observed (independent) and modelled fertilization (dependent) for pH 7.8 (P = 0.012, r2 = 0.336), but not for pH 7.6 (P = 0.413, r2 = 0.042).
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