Cryptic female choice enhances fertilization success and embryo survival in chinook salmon

In this study, we investigated two potentially important intersexual postcopulatory gametic interactions in a population of chinook salmon ( Oncorhynchus tshawytscha ): (i) the effect of female ovarian fluid (OF) on the behaviour of spermatozoa during fertilization and (ii) the effects of multilocus heterozygosity (MLH) (as an index of male quality) and female–male genetic relatedness on sperm behaviour and male fertilization success when there is sperm competition in the presence of that OF. To do this, we conducted a series of in vitro competitive fertilization experiments and found that, when ejaculates from two males are competing for access to a single female's unfertilized eggs, fertilization success was significantly biased towards the male whose sperm swam fastest in the female's OF. Embryo survival—a measure of fitness—was also positively correlated with both sperm swimming speed in OF and male MLH, providing novel evidence that cryptic female choice is adaptive for the female, enhancing the early survival of her offspring and potentially influencing her fitness.

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Male–female relatedness at specific SNP-linkage groups influences cryptic female choice in Chinook salmon ( Oncorhynchus tshawytscha )

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.0853 ◽

2017 ◽

Vol 284 (1859) ◽

pp. 20170853 ◽

Cited By ~ 5

Author(s):

Cornelia Geßner ◽

Sheri L. Johnson ◽

Paul Fisher ◽

Shannon Clarke ◽

Kim Rutherford ◽

...

Keyword(s):

Female Choice ◽

Chinook Salmon ◽

Oncorhynchus Tshawytscha ◽

Fertilization Success ◽

Cryptic Female Choice ◽

Linkage Groups ◽

Sperm Velocity ◽

Ovarian Fluid ◽

The Impact

In a range of taxa, the relatedness between mates influences both pre- and post-mating processes of sexual selection. However, relatively little is known about the genetic loci facilitating such a bias, with the exception of the major histocompatibility complex. Here, we performed tightly controlled replicated in vitro fertilization trials to explore the impact of relatedness on two possible mechanisms of cryptic female choice (CFC) in Chinook salmon ( Oncorhynchus tshawytscha ). We tested (i) whether relatedness of mates, assessed using 682 single nucleotide polymorphisms (SNPs) on 29 SNP-linkage groups (LGs), biases a male's sperm velocity in ovarian fluid (a parameter previously shown to predict male fertilization success), and (ii) whether relatedness of mates governs fertilization success via other mechanisms, probably via sperm–egg interactions. We found that relatedness on three LGs explained the variation in sperm velocity, and relatedness on two LGs explained fertilization success, which might indicate the presence of genes important in sperm–ovarian fluid and sperm–egg interactions in these genomic regions. Mapping of the SNPs on these LGs to the rainbow trout genome revealed two genes that affect fertility in humans and represent candidate genes for further studies. Our results thereby provide a novel contribution to the understanding of the mechanism of CFC.

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

Heredity ◽

10.1038/hdy.2016.116 ◽

2017 ◽

Vol 118 (5) ◽

pp. 442-452 ◽

Cited By ~ 16

Author(s):

C Gessner ◽

S Nakagawa ◽

M Zavodna ◽

N J Gemmell

Keyword(s):

Sexual Selection ◽

Major Histocompatibility Complex ◽

Female Choice ◽

Chinook Salmon ◽

Oncorhynchus Tshawytscha ◽

Cryptic Female Choice ◽

Genetic Compatibility ◽

Histocompatibility Complex ◽

Selection For

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Post-Copulatory Sexual Selection

Evolutionary Biology ◽

10.1093/obo/9780199941728-0131 ◽

2021 ◽

Author(s):

Patricia L.R. Brennan ◽

Dara N. Orbach

Keyword(s):

Sexual Selection ◽

Sperm Competition ◽

Female Choice ◽

Reproductive Tract ◽

Seminal Fluid ◽

Fertilization Success ◽

Female Reproductive Tract ◽

Cryptic Female Choice ◽

Trade Offs ◽

Morphological Criteria

The field of post-copulatory sexual selection investigates how female and male adaptations have evolved to influence the fertilization of eggs while optimizing fitness during and after copulation, when females mate with multiple males. When females are polyandrous (one female mates with multiple males), they may optimize their mating rate and control the outcome of mating interactions to acquire direct and indirect benefits. Polyandry may also favor the evolution of male traits that offer an advantage in post-copulatory male-male sperm competition. Sperm competition occurs when the sperm, seminal fluid, and/or genitalia of one male directly impacts the outcome of fertilization success of a rival male. When a female mates with multiple males, she may use information from a number of traits to choose who will sire her offspring. This cryptic female choice (CFC) to bias paternity can be based on behavioral, physiological, and morphological criteria (e.g., copulatory courtship, volume and/or composition of seminal fluid, shape of grasping appendages). Because male fitness interests are rarely perfectly aligned with female fitness interests, sexual conflict over mating and fertilization commonly occur during copulatory and post-copulatory interactions. Post-copulatory interactions inherently involve close associations between female and male reproductive characteristics, which in many species potentially include sperm storage and sperm movement inside the female reproductive tract, and highlight the intricate coevolution between the sexes. This coevolution is also common in genital morphology. The great diversity of genitalia among species is attributed to sexual selection. The evolution of genital attributes that allow females to maintain reproductive autonomy over paternity via cryptic female choice or that prevent male manipulation and sexual control via sexually antagonistic coevolution have been well documented. Additionally, cases where genitalia evolve through intrasexual competition are well known. Another important area of study in post-copulatory sexual selection is the examination of trade-offs between investments in pre-copulatory and post-copulatory traits, since organisms have limited energetic resources to allocate to reproduction, and securing both mating and fertilization is essential for reproductive success.

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Delineating the roles of males and females in sperm competition

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.2047 ◽

2013 ◽

Vol 280 (1772) ◽

pp. 20132047 ◽

Cited By ~ 37

Author(s):

Jonathan P. Evans ◽

Patrice Rosengrave ◽

Clelia Gasparini ◽

Neil J. Gemmell

Keyword(s):

Sperm Competition ◽

Chinook Salmon ◽

Competitive Ability ◽

Oncorhynchus Tshawytscha ◽

Fertilization Success ◽

Interactive Effects ◽

Swimming Velocity ◽

Ovarian Fluid ◽

Males And Females ◽

Paternity Success

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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Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha)

Journal of Endocrinology ◽

10.1677/joe.0.1200135 ◽

1989 ◽

Vol 120 (1) ◽

pp. 135-142 ◽

Cited By ~ 231

Author(s):

A. G. Maule ◽

R. A. Tripp ◽

S. L. Kaattari ◽

C. B. Schreck

Keyword(s):

Disease Resistance ◽

Immune Function ◽

Chinook Salmon ◽

Plasma Cortisol ◽

Oncorhynchus Tshawytscha ◽

Acute Stress ◽

Vibrio Anguillarum ◽

Time To Death ◽

Mean Time

ABSTRACT We examined the effects of acute stress on the immune system and disease resistance of juvenile chinook salmon (Oncorhynchus tshawytscha) in laboratory and clinical trials. Immune function, as measured by the ability of lymphocytes from the anterior kidney to generate specific antibody-producing cells (APC) in vitro, was depressed 4 h after stress, when plasma cortisol levels were highest. At the same time, resistance to the fish pathogen, Vibrio anguillarum, was also depressed. Compared with controls, plasma cortisol and APC of stressed fish were unchanged after 24 h, and disease resistance was enhanced as evidenced by higher survival rate and longer mean time to death of mortalities. After 7 days, even though numbers of APC were depressed, plasma cortisol concentration and disease resistance did not differ from controls. This pattern was generally the same, independent of the type of stress applied: i.e. being held out of water in a dipnet for 30 s, manipulation during hatchery operations for 4 h, or transportation for 9 h. These and earlier findings suggest that similar endocrine-immune interactions operate in the mammalian and salmonid systems during acute stress. Journal of Endocrinology (1989) 120, 135–142

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Sperm traits in Chinook salmon depend upon activation medium: implications for studies of sperm competition in fishes

Canadian Journal of Zoology ◽

10.1139/z09-081 ◽

2009 ◽

Vol 87 (10) ◽

pp. 920-927 ◽

Cited By ~ 23

Author(s):

P. Rosengrave ◽

R. Montgomerie ◽

V. J. Metcalf ◽

K. McBride ◽

N. J. Gemmell

Keyword(s):

Sperm Competition ◽

Fresh Water ◽

Swimming Speed ◽

Chinook Salmon ◽

Oncorhynchus Tshawytscha ◽

Salt Water ◽

Computer Assisted ◽

Ovarian Fluid ◽

Sperm Swimming Speed ◽

Sperm Traits

Sperm traits of externally fertilizing fish species are typically measured in fresh (or salt) water, even though the spawning environment of their ova contains ovarian fluid. In this study, we measured sperm traits of Chinook salmon ( Oncorhynchus tshawytscha (Walbaum in Artedi, 1792)) in both fresh water and dilute ovarian fluid at 10 and 20 s postactivation, using a computer-assisted sperm analysis system. Spermatozoa swam faster, and had both higher percent motility and a straighter path trajectory for a longer period of forward motility when activated in ovarian fluid compared with activation in fresh water. Comparing sperm activity of 10 males in water versus ovarian fluid, we found a weak but significant correlation for sperm swimming speed at 10 s postactivation (r = 0.34, p = 0.01), but not for any other sperm traits measured. Most important, across males, mean sperm swimming speed in water accounted for <10% of the observed variation in mean sperm swimming speed in ovarian fluid. Thus, we argue that sperm traits measured in fresh water are not particularly relevant to those same traits during normal spawning in this species. We suggest that sperm performance measured in fresh water should be used with caution when comparing the potential for individual males to fertilize ova, especially in studies of sperm competition in externally fertilizing species.

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A mechanism for cryptic female choice in chinook salmon

Behavioral Ecology ◽

10.1093/beheco/arn089 ◽

2008 ◽

Vol 19 (6) ◽

pp. 1179-1185 ◽

Cited By ~ 83

Author(s):

Patrice Rosengrave ◽

Neil J. Gemmell ◽

Victoria Metcalf ◽

Katherine McBride ◽

Robert Montgomerie

Keyword(s):

Female Choice ◽

Chinook Salmon ◽

Cryptic Female Choice

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A non-functional copy of the salmonid sex determining gene (sdY) is responsible for the “apparent” XY females in Chinook salmon, Oncorhynchus tshawytscha

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkab451 ◽

2022 ◽

Author(s):

Sylvain Bertho ◽

Amaury Herpin ◽

Elodie Jouanno ◽

Ayaka Yano ◽

Julien Bobe ◽

...

Keyword(s):

Missense Mutation ◽

Chinook Salmon ◽

Oncorhynchus Tshawytscha ◽

Nuclear Translocation ◽

Naturally Occurring ◽

Determination System ◽

Synergistic Induction ◽

Sex Determination System

Abstract Many salmonids have a male heterogametic (XX/XY) sex determination system, and they are supposed to have a conserved master sex determining gene (sdY), that interacts at the protein level with Foxl2 leading to the blockage of the synergistic induction of Foxl2 and Nr5a1 of the cyp19a1a promoter. However, this hypothesis of a conserved master sex determining role of sdY in salmonids is challenged by a few exceptions, one of them being the presence of naturally occurring “apparent” XY Chinook salmon, Oncorhynchus tshawytscha, females. Here we show that some XY Chinook salmon females have a sdY gene (sdY-N183), with one missense mutation leading to a substitution of a conserved isoleucine to an asparagine (I183N). In contrast, Chinook salmon males have both a non-mutated sdY-I183 gene and the missense mutation sdY-N183 gene. The 3D model of SdY-I183N predicts that the I183N hydrophobic to hydrophilic amino acid change leads to a modification of the SdY β-sandwich structure. Using in vitro cell transfection assays we found that SdY-I183N, like the wildtype SdY, is preferentially localized in the cytoplasm. However, compared to wildtype SdY, SdY-I183N is more prone to degradation, its nuclear translocation by Foxl2 is reduced and SdY-I183N is unable to significantly repress the synergistic Foxl2/Nr5a1 induction of the cyp19a1a promoter. Altogether our results suggest that the sdY-N183 gene of XY Chinook females is non-functional and that SdY-I183N is no longer able to promote testicular differentiation by impairing the synthesis of estrogens in the early differentiating gonads of wild Chinook salmon XY females.

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Differential sperm storage by female zebra finches Taeniopygia guttata

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.1032 ◽

2017 ◽

Vol 284 (1860) ◽

pp. 20171032 ◽

Cited By ~ 8

Author(s):

Nicola Hemmings ◽

Tim Birkhead

Keyword(s):

Female Choice ◽

Reproductive Tract ◽

Fertilization Success ◽

Sperm Storage ◽

Taeniopygia Guttata ◽

Female Reproductive Tract ◽

Cryptic Female Choice ◽

Zebra Finches ◽

Novel Technique ◽

Sperm Storage Tubules

When females mate promiscuously, female sperm storage provides scope to bias the fertilization success towards particular males via the non-random acceptance and utilization of sperm. The difficulties observing post-copulatory processes within the female reproductive tract mean that the mechanisms underlying cryptic female choice remain poorly understood. Here, we use zebra finches Taeniopygia guttata , selected for divergent sperm lengths, combined with a novel technique for isolating and extracting sperm from avian sperm storage tubules (SSTs), to test the hypothesis that sperm from separate ejaculates are stored differentially by female birds. We show that sperm from different inseminations enter different SSTs in the female reproductive tract, resulting in almost complete segregation of the sperm of competing males. We propose that non-random acceptance of sperm into SSTs, reflected in this case by sperm phenotype, provides a mechanism by which long sperm enjoy enhanced fertilization success in zebra finches.

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