Ovarian fluid enhances sperm velocity based on relatedness in lake trout, Salvelinus namaycush

Butts, Ian A.E.; Johnson, Katie; Wilson, Chris C.; Pitcher, Trevor E.

doi:10.1016/j.theriogenology.2012.06.031

Cited by 64 publications

(71 citation statements)

References 29 publications

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“…In contrast to our findings for male effects, we detected no overall effect of OF-donor identity on relative paternity success, and no evidence for male-by-female interactions arising from the differential effects of OF on sperm competitiveness (table 1). The latter finding was unanticipated, given prior evidence from O. tshawytscha and other salmonid fishes that variation in sperm velocity is contingent on the interactive effects of sperm-and OF-donor identities [21][22][23][24], a finding that is also supported in this paper. As we note in our methods, we were constrained to use a concentration of 10% OF compared with higher concentrations used previously.…”

Section: Resultssupporting

confidence: 81%

“…Previous work on O. tshawytscha and other salmonid fishes has revealed that ovarian fluid (OF), which forms an extracellular matrix surrounding externally spawned eggs, upregulates sperm motility [20] and differentially mediates the swimming velocities of sperm from conspecific males. Specifically, sperm tested in the presence of OF from certain females perform better (swim faster) than when tested with others, and such patterns can be non-transitive across different male-female pairings [21][22][23][24]. As relative differences in sperm swimming velocity have been shown to be associated with sperm competitiveness in salmonid fishes [25], OF has been implicated as a potential arbiter of cryptic female choice in these taxa [23].…”

Section: Introductionmentioning

confidence: 99%

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Delineating the roles of males and females in sperm competition

et al. 2013

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Disentangling the relative roles of males, females and their interactive effects on competitive fertilization success remains a challenge in sperm competition. In this study, we apply a novel experimental framework to an ideally suited externally fertilizing model system in order to delineate these roles. We focus on the chinook salmon, Oncorhynchus tshawytscha, a species in which ovarian fluid (OF) has been implicated as a potential arbiter of cryptic female choice for genetically compatible mates. We evaluated this predicted sexually selected function of OF using a series of factorial competitive fertilization trials. Our design involved a series of 10 factorial crosses, each involving two 'focal' rival males whose sperm competed against those from a single 'standardized' (non-focal) rival for a genetically uniform set of eggs in the presence of OF from two focal females. This design enabled us to attribute variation in competitive fertilization success among focal males, females (OF) and their interacting effects, while controlling for variation attributable to differences in the sperm competitive ability of rival males, and male-by-female genotypic interactions. Using this experimental framework, we found that variation in sperm competitiveness could be attributed exclusively to differences in the sperm competitive ability of focal males, a conclusion supported by subsequent analyses revealing that variation in sperm swimming velocity predicts paternity success. Together, these findings provide evidence that variation in paternity success can be attributed to intrinsic differences in the sperm competitive ability of rival males, and reveal that sperm swimming velocity is a key target of sexual selection.

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Section: Resultssupporting

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Delineating the roles of males and females in sperm competition

et al. 2013

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“…This is related to changes in viscosity (Turner and Montgomerie, 2002), pH (Wojtczak et al, 2007) and/or ionic composition of activation media (Rosengrave et al, 2009b). Ovarian fluid has even been found to differentially enhance sperm based on genetic relatedness of mates (Gasparini and Pilastro, 2011;Butts et al, 2012a) or spawning origin (i.e. wild versus farmed males; Beirão et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Ovarian fluid impacts flagellar beating and biomechanical metrics of sperm between alternative reproductive tactics

Butts

Prokopchuk

Kašpar

et al. 2017

Journal of Experimental Biology

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Alternative reproductive tactics (ARTs) are prevalent in nature, where smaller parasitic males typically have better sperm quality than larger territorial guard males. At present, it is unclear what is causing this phenomenon. Our objective was to gain insights into sperm form and function by examining flagellar beating patterns (beat frequency, wave amplitude, bend length, bend angle, wave velocity) and biomechanical sperm metrics (velocity, hydrodynamic power output, propulsive efficiency) of wild spawning Chinook salmon ARTs. Ovarian fluid and milt were collected to form a series of eight experimental blocks, each composed of ovarian fluid from a unique female and sperm from a unique pair of parasitic jack and guard hooknose males. Sperm from each ART were activated in river water and ovarian fluid. Flagellar parameters were evaluated from recordings using high-speed video microscopy and biomechanical metrics were quantified. We show that ART has an impact on flagellar beating, where jacks had a higher bend length and bend angle than hooknoses. Activation media also impacted the pattern of flagellar parameters, such that beat frequency, wave velocity and bend angle declined, while wave amplitude of flagella increased when ovarian fluid was incorporated into activation media. Furthermore, we found that sperm from jacks swam faster than those from hooknoses and required less hydrodynamic power output to propel themselves in river water and ovarian fluid. Jack sperm were also more efficient at swimming than hooknose sperm, and propulsive efficiency increased when cells were activated in ovarian fluid. The results demonstrate that sperm biomechanics may be driving divergence in competitive reproductive success between ARTs.

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“…Fertilization experiments in Arctic charr (Liljedal et al, 2008) revealed a higher fertilization success for males genetically less similar to the female, while in the Peron's tree frog (Sherman et al, 2008) fertilization success was biased towards males genetically more similar to the female. In contrast, in Lake Trout, sperm velocity was lower for males unrelated to the female than for related (full-sib) males (Butts et al, 2012). Possibly, selection might have promoted alleles enabling an avoidance of genetically incompatible matings (Tregenza and Wedell, 2000).…”

Section: Introductionmentioning

confidence: 88%

Sexual selection for genetic compatibility: the role of the major histocompatibility complex on cryptic female choice in Chinook salmon (Oncorhynchus tshawytscha)

et al. 2017

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Cryptic female choice (CFC), a form of sexual selection during or post mating, describes processes of differential sperm utilization by females to bias fertilization outcomes towards certain males. In Chinook salmon (Oncorhynchus tshawytscha) the ovarian fluid surrounding the ova of a given female differently enhances the sperm velocity of males. Sperm velocity is a key ejaculate trait that determines fertilization success in externally fertilizing fishes, thus the differential effect on sperm velocity might bias male fertilization outcomes and represent a mechanism of CFC. Once sperm reach the oocyte, CFC could potentially be further facilitated by sperm-egg interactions, which are well understood in externally fertilizing marine invertebrates. Here, we explored the potential genetic basis of both possible mechanisms of CFC by examining whether the genotypic combinations of mates (amino-acid divergence, number of shared alleles) at the major histocompatibility complex (MHC) class I and II explain the variation in sperm velocity and/or male fertilization success that is not explained by sperm velocity, which might indicate MHC-based sperm-egg interactions. We recorded sperm velocity in ovarian fluid, employed paired-male fertilization trials and evaluated the fertilization success of each male using microsatellite-based paternity assignment. We showed that relative sperm velocity was positively correlated with fertilization success, confirming that the differential effect on sperm velocity may be a mechanism of CFC in Chinook salmon. The variation in sperm velocity was independent of MHC class I and II. However, the MHC class II divergence of mates explained fertilization success, indicating that this locus might influence sperm-egg interactions.

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Ovarian fluid enhances sperm velocity based on relatedness in lake trout, Salvelinus namaycush

Cited by 64 publications

References 29 publications

Delineating the roles of males and females in sperm competition

Delineating the roles of males and females in sperm competition

Ovarian fluid impacts flagellar beating and biomechanical metrics of sperm between alternative reproductive tactics

Sexual selection for genetic compatibility: the role of the major histocompatibility complex on cryptic female choice in Chinook salmon (Oncorhynchus tshawytscha)

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