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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).
Babcock,
Sperm Diffusion Models and In Situ Confirmation of Long-Distance Fertilization in the Free-Spawning Asteroid Acanthaster planci.
1994, Pubmed,
Echinobase
Babcock,
Sperm Diffusion Models and In Situ Confirmation of Long-Distance Fertilization in the Free-Spawning Asteroid Acanthaster planci.
1994,
Pubmed
,
Echinobase
Byrne,
Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios.
2009,
Pubmed
,
Echinobase
Byrne,
Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities.
2010,
Pubmed
,
Echinobase
Chan,
Effects of ocean-acidification-induced morphological changes on larval swimming and feeding.
2011,
Pubmed
,
Echinobase
Christen,
Metabolism of sea urchin sperm. Interrelationships between intracellular pH, ATPase activity, and mitochondrial respiration.
1983,
Pubmed
,
Echinobase
Christen,
Elevation of the intracellular pH activates respiration and motility of sperm of the sea urchin, Strongylocentrotus purpuratus.
1982,
Pubmed
,
Echinobase
Christen,
31P-NMR analysis of sea urchin sperm activation. Reversible formation of high energy phosphate compounds by changes in intracellular pH.
1983,
Pubmed
,
Echinobase
Doney,
Ocean acidification: the other CO2 problem.
2009,
Pubmed
,
Echinobase
Doney,
Climate change impacts on marine ecosystems.
2012,
Pubmed
Evans,
Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma.
2005,
Pubmed
,
Echinobase
Frankham,
Conservation biology: ecosystem recovery enhanced by genotypic diversity.
2005,
Pubmed
Hamamah,
Role of the ionic environment and internal pH on sperm activity.
1998,
Pubmed
,
Echinobase
Havenhand,
Near-future levels of ocean acidification reduce fertilization success in a sea urchin.
2008,
Pubmed
,
Echinobase
Kroeker,
Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms.
2010,
Pubmed
Lee,
Changes in internal pH associated with initiation of motility and acrosome reaction of sea urchin sperm.
1983,
Pubmed
,
Echinobase
Levitan,
The relationship between conspecific fertilization success and reproductive isolation among three congeneric sea urchins.
2002,
Pubmed
,
Echinobase
Levitan,
Selection on gamete recognition proteins depends on sex, density, and genotype frequency.
2006,
Pubmed
,
Echinobase
Levitan,
Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus.
2000,
Pubmed
,
Echinobase
Levitan,
Sperm limitation in the sea.
1995,
Pubmed
Levitan,
Gamete traits influence the variance in reproductive success, the intensity of sexual selection, and the outcome of sexual conflict among congeneric sea urchins.
2008,
Pubmed
,
Echinobase
Levitan,
Density-dependent sexual selection in external fertilizers: variances in male and female fertilization success along the continuum from sperm limitation to sexual conflict in the sea urchin Strongylocentrotus franciscanus.
2004,
Pubmed
,
Echinobase
Marshall,
Reliably estimating the effect of toxicants on fertilization success in marine broadcast spawners.
2006,
Pubmed
Martin,
Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification.
2011,
Pubmed
,
Echinobase
Nakagawa,
Effect size, confidence interval and statistical significance: a practical guide for biologists.
2007,
Pubmed
Palumbi,
All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins.
1999,
Pubmed
,
Echinobase
Pennington,
THE ECOLOGY OF FERTILIZATION OF ECHINOID EGGS: THE CONSEQUENCES OF SPERM DILUTION, ADULT AGGREGATION, AND SYNCHRONOUS SPAWNING.
1985,
Pubmed
,
Echinobase
Somero,
The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine 'winners' and 'losers'.
2010,
Pubmed
Styan,
Polyspermy, egg size, and the fertilization kinetics of free-spawning marine invertebrates.
1998,
Pubmed
Styan,
Barriers to cross-fertilization between populations of a widely dispersed polychaete species are unlikely to have arisen through gametic compatibility arms-races.
2008,
Pubmed
Sunday,
Quantifying rates of evolutionary adaptation in response to ocean acidification.
2011,
Pubmed
,
Echinobase
Tadros,
The maternal-to-zygotic transition: a play in two acts.
2009,
Pubmed
,
Echinobase
