Inter‐population ovarian fluid variation differentially modulates sperm motility in Atlantic cod <i>Gadus morhua</i>

Beirão, J.; Purchase, Craig F.; Wringe, Brendan F.; Fleming, Ian A.

doi:10.1111/jfb.12685

Cited by 27 publications

(33 citation statements)

References 63 publications

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“…To our knowledge, the only study to date that has explicitly investigated a possible role of PEMS in reproductive isolation has been with the congeneric fish, Salmo salar and S. trutta . Ovarian fluid composition is highly divergent in fish, exhibiting substantial differences among species (Lahnsteiner, Weismann, & Patzner, ) and even between members of different geographic populations within species (Beirão et al ., ). Studies comparing ovarian fluid‐induced modification to sperm exposed to ovarian fluid derived from the either the same or different populations or congeneric species provide strong support for the conclusion that ovarian fluid composition and interacting sperm traits are evolutionarily co‐diversifying (Yeates et al ., ; Beirão et al ., ; Devigili et al ., ).…”

Section: Evolutionary Implications Of Pemsmentioning

confidence: 97%

Post‐ejaculatory modifications to sperm (PEMS)

Pitnick¹,

Wolfner

Dorus³

2019

Biological Reviews

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Mammalian sperm must spend a minimum period of time within a female reproductive tract to achieve the capacity to fertilize oocytes. This phenomenon, termed sperm ‘capacitation’, was discovered nearly seven decades ago and opened a window into the complexities of sperm–female interaction. Capacitation is most commonly used to refer to a specific combination of processes that are believed to be widespread in mammals and includes modifications to the sperm plasma membrane, elevation of intracellular cyclic AMP levels, induction of protein tyrosine phosphorylation, increased intracellular Ca2+ levels, hyperactivation of motility, and, eventually, the acrosome reaction. Capacitation is only one example of post‐ejaculatory modifications to sperm (PEMS) that are widespread throughout the animal kingdom. Although PEMS are less well studied in non‐mammalian taxa, they likely represent the rule rather than the exception in species with internal fertilization. These PEMS are diverse in form and collectively represent the outcome of selection fashioning complex maturational trajectories of sperm that include multiple, sequential phenotypes that are specialized for stage‐specific functionality within the female. In many cases, PEMS are critical for sperm to migrate successfully through the female reproductive tract, survive a protracted period of storage, reach the site of fertilization and/or achieve the capacity to fertilize eggs. We predict that PEMS will exhibit widespread phenotypic plasticity mediated by sperm–female interactions. The successful execution of PEMS thus has important implications for variation in fitness and the operation of post‐copulatory sexual selection. Furthermore, it may provide a widespread mechanism of reproductive isolation and the maintenance of species boundaries. Despite their possible ubiquity and importance, the investigation of PEMS has been largely descriptive, lacking any phylogenetic consideration with regard to divergence, and there have been no theoretical or empirical investigations of their evolutionary significance. Here, we (i) clarify PEMS‐related nomenclature; (ii) address the evolutionary origin, maintenance and divergence in PEMS in the context of the protracted life history of sperm and the complex, selective environment of the female reproductive tract; (iii) describe taxonomically widespread types of PEMS: sperm activation, chemotaxis and the dissociation of sperm conjugates; (iv) review the occurence of PEMS throughout the animal kingdom; (v) consider alternative hypotheses for the adaptive value of PEMS; (vi) speculate on the evolutionary implications of PEMS for genomic architecture, sexual selection, and reproductive isolation; and (vii) suggest fruitful directions for future functional and evolutionary analyses of PEMS.

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Section: Evolutionary Implications Of Pemsmentioning

confidence: 97%

Post‐ejaculatory modifications to sperm (PEMS)

Pitnick¹,

Wolfner

Dorus³

2019

Biological Reviews

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“…Beside species‐specific differences, such variances in the composition of CF can be related to changes in a female's physiological status throughout the spawning season, as well as with changes in egg quality and maturity (Aegerter & Jalabert, ; Lahnsteiner, ; Lahnsteiner, Weismann, & Patzner, ). Beirão, Purchase, Wringe, and Fleming () also reported an inter‐population variation in the concentration of Ca ++ of CF that differentially modulates sperm motility in Atlantic cod Gadus morhua . The CFs of different sturgeon species in the present study were alkaline, as reported for cyprinids and salmonids (Hatef et al., ; Hirano, Morisawa, & Suzuki, ; Lahnsteiner, Urbanyi, Horvath, & Weismann, ; Niksirat, Sarvi, Mojazi Amiri, & Hatef, ; Niksirat, Sarvi, Mojazi Amiri, Karami, & Hatef, ).…”

Section: Discussionmentioning

confidence: 92%

Comparative coelomic fluid composition of sterlet sturgeon Acipenser ruthenus Linnaeus, 1758, Siberian sturgeon Acipenser baerii Brandt, 1869, and Russian sturgeon Acipenser gueldenstaedtii Brandt & Ratzeburg, 1833

2016

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Summary The objectives of this study were to compare the physicochemical properties of coelomic fluid (CF) in three sturgeon species, sterlet sturgeon Acipenser ruthenus (age 5–8 years), Siberian sturgeon Acipenser baerii (age 15–20 years), and Russian sturgeon Acipenser gueldenstaedtii (age 13–18 years). For the study, CF was collected by plastic pipette from the eggs of mature female sterlet sturgeon (N = 10), Siberian sturgeon (N = 7) and Russian sturgeon (N = 4); osmolality, pH, ionic composition (Na+, K+, Ca2+, Mg2+, Cl−), glucose, cholesterol and total protein of the CF were then analyzed. Mean concentration of K+ (4.4–6.11 mmol/L), Cl− (89.8–98.0 mmol/L), Ca2+ (0.87–0.96 mmol/L), Mg2+ (0.57–0.67 mmol/L), cholesterol (0.13–0.16 mmol/L), total protein (2.41–3.57 g/L), pH (7.92–7.98), and osmolality (190–213 mOsm/kg) of CF were not significantly different among these three species. However, the mean concentration of Na+ was significantly lower in sterlet sturgeon (104.6 ± 7.7 mmol/L; p < .05) than in the Siberian (126.4 ± 6.2) and Russian (123.0 ± 5.9) sturgeon. For these three species, Na+, K+, Cl−, and Mg2+ were the dominating ions; several significant correlations were observed among these ions and other physiochemical properties of CF. This is the first report on the ionic and biochemical composition of the CF of sterlet, Siberian and Russian sturgeon, which can be used as a reference point for further development of artificial media for the short‐term storage of unfertilized sturgeon eggs as well as for the standardization of the fertilization protocol for these species in controlled reproduction.

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“…testing more than two populations, from a range of geographical origins). However, our results are in line with previous studies that evaluated the presence of similar reproductive barriers acting among (Yeates et al ., ; Cramer et al ., ) and within species (Beirao et al ., ). Nevertheless, our findings indicate some complexity in the observed patterns at the within‐species level, where the direction of the effect depended on the specific combination of populations examined.…”

Section: Discussionmentioning

confidence: 97%

Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post‐copulatory isolation between two guppy populations

Devigili

Fitzpatrick

Gasparini

et al. 2017

J of Evolutionary Biology

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Identifying mechanisms of reproductive isolation is key to understanding speciation. Among the putative mechanisms underlying reproductive isolation, sperm-female interactions (post-mating-prezygotic barriers) are arguably the hardest to identify, not least because these are likely to operate at the cellular or molecular level. Yet sperm-female interactions offer great potential to prevent the transfer of genetic information between different populations at the initial stages of speciation. Here, we provide a preliminary test for the presence of a putative post-mating-prezygotic barrier operating between three populations of Trinidadian guppies (Poecilia reticulata), an internally fertilizing fish that inhabits streams with different levels of connectivity across Trinidad. We experimentally evaluate the effect of female ovarian fluid on sperm velocity (a predictor of competitive fertilization success) according to whether males and females were from the same (native) or different (foreign) populations. Our results reveal the potential for ovarian fluid to act as a post-mating-prezygotic barrier between two populations from different drainages, but also that the strength of this barrier is different among populations. This result may explain the previous finding that, in some populations, sperm from native males have precedence over foreign sperm, which could eventually lead to reproductive isolation between these populations.

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Inter‐population ovarian fluid variation differentially modulates sperm motility in Atlantic cod Gadus morhua

Cited by 27 publications

References 63 publications

Post‐ejaculatory modifications to sperm (PEMS)

Post‐ejaculatory modifications to sperm (PEMS)

Comparative coelomic fluid composition of sterlet sturgeon Acipenser ruthenus Linnaeus, 1758, Siberian sturgeon Acipenser baerii Brandt, 1869, and Russian sturgeon Acipenser gueldenstaedtii Brandt & Ratzeburg, 1833

Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post‐copulatory isolation between two guppy populations

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