Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Ecol Evol
2017 Mar 01;76:1737-1750. doi: 10.1002/ece3.2776.
Show Gene links
Show Anatomy links
Sensitivity of sea urchin fertilization to pH varies across a natural pH mosaic.
Kapsenberg L
,
Okamoto DK
,
Dutton JM
,
Hofmann GE
.
???displayArticle.abstract???
In the coastal ocean, temporal fluctuations in pH vary dramatically across biogeographic ranges. How such spatial differences in pH variability regimes might shape ocean acidification resistance in marine species remains unknown. We assessed the pH sensitivity of the sea urchin Strongylocentrotus purpuratus in the context of ocean pH variability. Using unique male-female pairs, originating from three sites with similar mean pH but different variability and frequency of low pH (pHT ≤ 7.8) exposures, fertilization was tested across a range of pH (pHT 7.61-8.03) and sperm concentrations. High fertilization success was maintained at low pH via a slight right shift in the fertilization function across sperm concentration. This pH effect differed by site. Urchins from the site with the narrowest pH variability regime exhibited the greatest pH sensitivity. At this site, mechanistic fertilization dynamics models support a decrease in sperm-egg interaction rate with decreasing pH. The site differences in pH sensitivity build upon recent evidence of local pH adaptation in S. purpuratus and highlight the need to incorporate environmental variability in the study of global change biology.
Figure 1. Conceptual diagram describing the climate variability hypothesis. In the context of ocean acidification, the environmental parameter is pH. As low pH exposures increase in frequency and the pH variability envelope widens (Site 2), the pH range within which organismal physiology must operate also widens. Through local environmental conditioning or natural selection, this may cause spatial differences in a species’ tolerance window across its biogeographic range (dashed lines)
Figure 2. Map of study sites in the California Current Large Marine Ecosystem (a) and normal fertilization (NF) functions of Strongylocentrotus purpuratus from those sites by pH treatment (b). Sites span >10° latitude from Oregon (FC) to California (BMR, SB) and exhibit similar mean pH values but unique pH variability regimes as described by percent of pH observations ≤7.80 and coefficient of variation (CV) of pH sensor observations (FC and BMR, April‐October, 2011–2013; SB, 2012–2015). For the NF functions (b), the gray band with dotted line represents the “global” normal fertilization curve (pooled site and pH treatment) at the 95% confidence interval, while points and thin lines represent mean site–pH treatment combinations. Extreme outliers under the fertilization curve originate largely from two pairs from BMR
Figure 3. Proportion total fertilization over a range of sperm concentrations for Strongylocentrotus purpuratus from FC, BMR, and SB by pH treatment (colors are the same as in Figure 2b). The dotted line represents the global mean estimate. Solid, thick lines represent the site–pH treatment level estimates with the 95% confidence interval as the colored band. Thin, solid lines represent unique pair estimates (i.e., random effects) for each site–pH treatment. The horizontal line denotes 50% total fertilization. Only three pH treatments were tested per site
Figure 4. Proportion abnormal fertilization over a range of sperm concentrations for Strongylocentrotus purpuratus from FC, BMR, and SB by pH treatment (colors are the same as in Figure 2b). The dotted line represents the global mean estimate. Solid, thick lines represent the site–pH treatment level estimates with the 95% confidence interval as the colored band. Thin, solid lines represent unique pair estimates (i.e., random effects) for each site–pH treatment. The horizontal line denotes 25% abnormal fertilization. Only three pH treatments were tested per site
Figure 5. Estimated sperm concentrations required to reach 50% normal fertilization (SNF
50), optimal normal fertilization (SO
pt
NF), and 25% abnormal fertilization (SA
bnF25) under different pH treatments (y‐axis), for Strongylocentrotus purpuratus from FC, BMR, and SB. Points within a population‐metric combination that do not share a common letter within a metric are significantly different (α = 0.017, following a Bonferroni correction for three comparisons under a parametric bootstrap). Those with no letters indicate no significant differences among treatments (within site, per metric). Percentages are the estimated peak levels of normal fertilization. Error bars are 95% confidence intervals estimated via parametric bootstrap. Colors are the same as in Figure 2b
Figure 6. Parameter estimates for the instantaneous per capita sperm–egg interaction rate (per no., per second, a‐c) and polyspermy block rate (per second, d‐f) by pH treatment, for Strongylocentrotus purpuratus from FC (a, d), BMR (b, e), and SB (c, f), using the mechanistic model of Okamoto (2016). Large symbols represent among‐pair means with 95% posterior credibility intervals (error bars) and horizontal dashes are the pair‐specific mean estimates. Asterisk denotes mean estimates with >95% posterior probability of a decline compared to the ambient (pHT = 8.03) treatment. Colors are the same as in Figure 2b
Boyd,
Biological responses to environmental heterogeneity under future ocean conditions.
2016, Pubmed
Boyd,
Biological responses to environmental heterogeneity under future ocean conditions.
2016,
Pubmed
Byrne,
Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities.
2010,
Pubmed
,
Echinobase
Campbell,
Ocean acidification changes the male fitness landscape.
2016,
Pubmed
,
Echinobase
Chan,
Persistent spatial structuring of coastal ocean acidification in the California Current System.
2017,
Pubmed
Crimaldi,
The role of structured stirring and mixing on gamete dispersal and aggregation in broadcast spawning.
2012,
Pubmed
Dawson,
Beyond predictions: biodiversity conservation in a changing climate.
2011,
Pubmed
Evans,
Transcriptomic responses to seawater acidification among sea urchin populations inhabiting a natural pH mosaic.
2017,
Pubmed
,
Echinobase
Farley,
The role of jelly coats in sperm-egg encounters, fertilization success, and selection on egg size in broadcast spawners.
2001,
Pubmed
,
Echinobase
Feely,
Evidence for upwelling of corrosive "acidified" water onto the continental shelf.
2008,
Pubmed
Fitzer,
Ocean acidification reduces the crystallographic control in juvenile mussel shells.
2014,
Pubmed
Flowers,
The recruitment sweepstakes has many winners: genetic evidence from the sea urchin Strongylocentrotus purpuratus.
2002,
Pubmed
,
Echinobase
Franke,
Sexual conflict and polyspermy under sperm-limited conditions: in situ evidence from field simulations with the free-spawning marine echinoid Evechinus chloroticus.
2002,
Pubmed
,
Echinobase
Frieder,
Present-day nearshore pH differentially depresses fertilization in congeneric sea urchins.
2014,
Pubmed
,
Echinobase
Gruber,
Rapid progression of ocean acidification in the California Current System.
2012,
Pubmed
Hammond,
Thermal tolerance of Strongylocentrotus purpuratus early life history stages: mortality, stress-induced gene expression and biogeographic patterns.
2010,
Pubmed
,
Echinobase
Havenhand,
Near-future levels of ocean acidification reduce fertilization success in a sea urchin.
2008,
Pubmed
,
Echinobase
Hofmann,
High-frequency dynamics of ocean pH: a multi-ecosystem comparison.
2011,
Pubmed
Johnson,
Extension of Nakagawa & Schielzeth's R2GLMM to random slopes models.
2014,
Pubmed
Kapsenberg,
Sensitivity of sea urchin fertilization to pH varies across a natural pH mosaic.
2021,
Pubmed
,
Echinobase
Kapsenberg,
Erratum: Near-shore Antarctic pH variability has implications for the design of ocean acidification experiments.
2015,
Pubmed
Kelly,
Natural variation and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus.
2013,
Pubmed
,
Echinobase
Kroeker,
Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability.
2016,
Pubmed
Kwiatkowski,
Nighttime dissolution in a temperate coastal ocean ecosystem increases under acidification.
2016,
Pubmed
Levitan,
Sex-specific spawning behavior and its consequences in an external fertilizer.
2005,
Pubmed
,
Echinobase
Levitan,
Kinetics of Fertilization in the Sea Urchin Strongylocentrotus franciscanus: Interaction of Gamete Dilution, Age, and Contact Time.
1991,
Pubmed
,
Echinobase
Levitan,
Selection on gamete recognition proteins depends on sex, density, and genotype frequency.
2006,
Pubmed
,
Echinobase
Levitan,
Contemporary evolution of sea urchin gamete-recognition proteins: experimental evidence of density-dependent gamete performance predicts shifts in allele frequencies over time.
2012,
Pubmed
,
Echinobase
Levitan,
The risk of polyspermy in three congeneric sea urchins and its implications for gametic incompatibility and reproductive isolation.
2007,
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
Levitan,
Simultaneous positive and negative frequency-dependent selection on sperm bindin, a gamete recognition protein in the sea urchin Strongylocentrotus purpuratus.
2010,
Pubmed
,
Echinobase
Millar,
The kinetics of monospermic and polyspermic fertilization in free-spawning marine invertebrates.
2003,
Pubmed
Moulin,
Effects of seawater acidification on early development of the intertidal sea urchin Paracentrotus lividus (Lamarck 1816).
2011,
Pubmed
,
Echinobase
Munday,
Transgenerational acclimation of fishes to climate change and ocean acidification.
2014,
Pubmed
Okamoto,
Competition among Eggs Shifts to Cooperation along a Sperm Supply Gradient in an External Fertilizer.
2016,
Pubmed
,
Echinobase
Palumbi,
MITOCHONDRIAL DNA DIVERSITY IN THE SEA URCHINS STRONGYLOCENTROTUS PURPURATUS AND S. DROEBACHIENSIS.
1990,
Pubmed
,
Echinobase
Parker,
Persistence of Positive Carryover Effects in the Oyster, Saccostrea glomerata, following Transgenerational Exposure to Ocean Acidification.
2015,
Pubmed
Pearse,
Ecological role of purple sea urchins.
2006,
Pubmed
,
Echinobase
Pedersen,
Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates.
2014,
Pubmed
Pespeni,
Signs of adaptation to local pH conditions across an environmental mosaic in the California Current Ecosystem.
2013,
Pubmed
,
Echinobase
Pespeni,
Evolutionary change during experimental ocean acidification.
2013,
Pubmed
,
Echinobase
Pespeni,
Restriction Site Tiling Analysis: accurate discovery and quantitative genotyping of genome-wide polymorphisms using nucleotide arrays.
2010,
Pubmed
,
Echinobase
Putnam,
Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions.
2015,
Pubmed
Sanford,
Local adaptation in marine invertebrates.
2011,
Pubmed
Schlegel,
Individual variability in reproductive success determines winners and losers under ocean acidification: a case study with sea urchins.
2012,
Pubmed
,
Echinobase
Sewell,
Ocean acidification and fertilization in the antarctic sea urchin Sterechinus neumayeri: the importance of polyspermy.
2014,
Pubmed
,
Echinobase
Stapper,
Assortative mating drives linkage disequilibrium between sperm and egg recognition protein loci in the sea urchin Strongylocentrotus purpuratus.
2015,
Pubmed
,
Echinobase
Styan,
Polyspermy, egg size, and the fertilization kinetics of free-spawning marine invertebrates.
1998,
Pubmed
Suckling,
Adult acclimation to combined temperature and pH stressors significantly enhances reproductive outcomes compared to short-term exposures.
2015,
Pubmed
,
Echinobase
Sunday,
Global analysis of thermal tolerance and latitude in ectotherms.
2011,
Pubmed
Thor,
Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod.
2015,
Pubmed
Thornton,
Climate variability and vulnerability to climate change: a review.
2014,
Pubmed
Trimmer,
Activation of sea urchin gametes.
1986,
Pubmed
,
Echinobase
