Interactive effects of ocean warming and acidification on sperm motility and fertilization in the mussel Mytilus galloprovincialis

Eads, Angela R.; Kennington, W. Jason; Evans, Jonathan P.

doi:10.3354/meps11944

Cited by 31 publications

(29 citation statements)

References 66 publications

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“…In the mussel, Mytilus galloprovincialis , decreasing seawater pH from 8.0 to 7.6 induced a 25% reduction of percentage of motile spermatozoa and their sperm swimming speed ( Vihtakari et al, 2013 ). In the same species, Eads et al (2016) found that the effect of pH on spermatozoa movement was only noticeable after 2 h of exposure. In the sea urchin, Heliocidaris erythrogramma , seawater acidification Δ pH of 0.3 and 0.5 units resulted in 7 and 9% reduction of percentage of motile spermatozoa, respectively, without affecting sperm swimming speed ( Schlegel et al, 2012 ).…”

Section: Discussionmentioning

confidence: 90%

“…As in sea urchins, acidic external pH (pHe) inhibits sperm movement in the Japanese pearl oyster ( Pinctada fucata martensii ; Ohta et al, 2007 ), black lip pearl oyster ( Pinctada margaritifera ; Demoy-Schneider et al, 2012 , 2014 ), king scallop ( Pecten maximus ; Faure et al, 1994 ), and Pacific oyster ( Crassostrea gigas ; Dong et al, 2002 ; Alavi et al, 2014 ). A complex interaction between environmental pH and temperature modified sperm movement characteristics in the mussel, Mytilus galloprovincialis ( Eads et al, 2016 ). Recently, it was shown that the concentration of some gonadal ions (i.e.…”

Section: Introductionmentioning

confidence: 99%

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pH controls spermatozoa motility in the Pacific oyster (Crassostrea gigas)

et al. 2018

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Investigating the roles of chemical factors stimulating and inhibiting sperm motility is required to understand the mechanisms of spermatozoa movement. In this study, we described the composition of the seminal fluid (osmotic pressure, pH, and ions) and investigated the roles of these factors and salinity in initiating spermatozoa movement in the Pacific oyster.The acidic pH of the gonad (5.82 ± 0.22) maintained sperm in the quiescent stage and initiation of flagellar movement was triggered by a sudden increase of spermatozoa external pH (pHe) when released in seawater (SW). At pH 6.4, percentage of motile spermatozoa was three times higher when they were activated in SW containing 30 mM NH4Cl, which alkalinizes internal pH (pHi) of spermatozoa, compared to NH4Cl-free SW, revealing the role of pHi in triggering sperm movement. Percentage of motile spermatozoa activated in Na + -free artificial seawater (ASW) was highly reduced compared to ASW, suggesting that change of pHi triggering sperm motility was mediated by a Na + /H + exchanger. Motility and swimming speed were highest in salinities between 33.8 and 42.7‰ (within a range of 0 to 50 ‰), and pH values above 7.5 (within a range of 4.5 to 9.5).

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Section: Discussionmentioning

confidence: 90%

Section: Introductionmentioning

confidence: 99%

pH controls spermatozoa motility in the Pacific oyster (Crassostrea gigas)

et al. 2018

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“…We consider the former possibility as a more likely explanation for the differential response of sperm across pH treatments, given the important role that ECs play in affecting the fertilization ability of sperm (Kekäläinen & Evans, 2016;Lymbery et al, 2017) and the likely sensitivity of sperm-egg chemical signalling to seawater pH changes (Foo, Deaker, et al, 2018). Additionally, previous work on M. galloprovincialis revealed lower fertilization rates after sperm and eggs had been separately pre-exposed to low pH environments (Eads et al, 2016), although the individual effects of pH on fertilization ability of eggs and sperm were not isolated in that study. Our current results, when combined with previous studies, indicate that effects of OA on reproductive success are likely to be complex and multifaceted and could act in different directions at different stages of sperm-egg interactions.…”

Section: Discussionmentioning

confidence: 96%

“…Relatively few studies have examined early reproductive stages of external fertilizers under OA, and among those that have, most have focused on in vitro fertilization assays, or on sperm swimming behavior (due to the well-documented importance of intracellular pH for sperm function; Nishigaki et al, 2014). Results from these investigations have so far been mixed; some studies have reported negative effects of OA on sperm motility (e.g., Campbell, Levitan, Hosken, & Lewis, 2016;Morita et al, 2010;Nakamura & Morita, 2012;Schlegel, Havenhand, Gillings, & Williamson, 2012;Vihtakari et al, 2013) while others have revealed negligible or even positive effects (Caldwell et al, 2011;Eads, Kennington, & Evans, 2016;Graham et al, 2016;Havenhand & Schlegel, 2009). Furthermore, there are inconsistent associations between OA-induced changes in sperm motility and in vitro fertilization rates (reviewed in Byrne, 2011;Ross, Parker, O'Connor, & Bailey, 2011), and thus, the fitness consequences of the effects of OA on gametes remain elusive.…”

Section: Introductionmentioning

confidence: 99%

Ocean acidification during prefertilization chemical communication affects sperm success

Lymbery

Kennington

Cornwall

et al. 2019

Ecology and Evolution

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Ocean acidification (OA) poses a major threat to marine organisms, particularly during reproduction when externally shed gametes are vulnerable to changes in seawater pH. Accordingly, several studies on OA have focused on how changes in seawater pH influence sperm behavior and/or rates of in vitro fertilization. By contrast, few studies have examined how pH influences prefertilization gamete interactions, which are crucial during natural spawning events in most externally fertilizing taxa. One mechanism of gamete interaction that forms an important component of fertilization in most taxa is communication between sperm and egg‐derived chemicals. These chemical signals, along with the physiological responses in sperm they elicit, are likely to be highly sensitive to changes in seawater chemistry. In this study, we experimentally tested this possibility using the blue mussel, Mytilus galloprovincialis, a species in which females have been shown to use egg‐derived chemicals to promote the success of sperm from genetically compatible males. We conducted trials in which sperm were allowed to swim in gradients of egg‐derived chemicals under different seawater CO2 (and therefore pH) treatments. We found that sperm had elevated fertilization rates after swimming in the presence of egg‐derived chemicals in low pH (pH 7.6) compared with ambient (pH 8.0) seawater. This observed effect could have important implications for the reproductive fitness of external fertilizers, where gamete compatibility plays a critical role in modulating reproduction in many species. For example, elevated sperm fertilization rates might disrupt the eggs' capacity to avoid fertilizations by genetically incompatible sperm. Our findings highlight the need to understand how OA affects the multiple stages of sperm‐egg interactions and to develop approaches that disentangle the implications of OA for female, male, and population fitness.

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“…spermatogenesis, sperm motility, viability, and fertility). According to [41], the optimal strategy for sperm in Mytilus might be to swim slowly and in tight circles in the absence of egg chemoattractant cues, but swim faster and straighter in their presence. It would be interesting to assess if typical 'slower' sperm with the M-type mitochondria rely more on OXPHOS, until chemoattractant cues are detected and possibly cause a switch to a faster glycolytic ATP production.…”

Section: (B) Intraspecific Analysesmentioning

confidence: 99%

Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly uniparental inheritance of mitochondria

et al. 2019

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Mitochondria produce energy through oxidative phosphorylation (OXPHOS), which depends on the expression of both nuclear and mitochondrial DNA (mtDNA). In metazoans, a striking exception from strictly maternal inheritance of mitochondria is doubly uniparental inheritance (DUI). This unique system involves the maintenance of two highly divergent mtDNAs (F-and M-type, 8-40% of nucleotide divergence) associated with gametes, and occasionally coexisting in somatic tissues. To address whether metabolic differences underlie this condition, we characterized the OXPHOS activity of oocytes, spermatozoa, and gills of different species through respirometry. DUI species express different gender-linked mitochondrial phenotypes in gametes and partly in somatic tissues. The M-phenotype is specific to sperm and entails (i) low coupled/uncoupled respiration rates, (ii) a limitation by the phosphorylation system, and (iii) a null excess capacity of the final oxidases, supporting a strong control over the upstream complexes. To our knowledge, this is the first example of a phenotype resulting from direct selection on sperm mitochondria. This metabolic remodelling suggests an adaptive value of mtDNA variations and we propose that bearing sex-linked mitochondria could assure the energetic requirements of different gametes, potentially linking male-energetic adaptation, mitotype preservation and inheritance, as well as resistance to both heteroplasmy and ageing.

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Interactive effects of ocean warming and acidification on sperm motility and fertilization in the mussel Mytilus galloprovincialis

Cited by 31 publications

References 66 publications

pH controls spermatozoa motility in the Pacific oyster (Crassostrea gigas)

pH controls spermatozoa motility in the Pacific oyster (Crassostrea gigas)

Ocean acidification during prefertilization chemical communication affects sperm success

Metabolic remodelling associated with mtDNA: insights into the adaptive value of doubly uniparental inheritance of mitochondria

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