Mate choice for nonadditive genetic benefits and the maintenance of genetic diversity in song sparrows

The lek paradox asserts that strong directional selection via female choice should deplete additive genetic variation in fitness and consequently any benefit to females expressing the preference. Recently, we have provided a novel resolution to the paradox by showing that nonadditive genetic effects such as overdominance can be inherited from parent to offspring, and populations with females that express a mating preference for outbred males maintain higher genetic variation than populations with females that mate randomly. Here, we test our dynamic model using empirical data previously published from a small island population of song sparrows (Melospiza melodia). The model assumes that fitness and male trait expression display overdominance effects. The results demonstrate that female choice for outbred males mediated by directional selection on song repertoire size provides a heritable benefit to offspring through reduced inbreeding depression. Within the population, we estimate the heritability of the inbreeding coefficient to be 0.18 +/- 0.08 (SD). Furthermore, we show that mate choice for outbred males increases fitness-related genetic variation in the population by 12% and thereby reduces inbreeding depression by 1% per generation in typical years and upwards of 15% in severe years. Thus, mate choice may help to stave off population extinction in this and other small populations

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

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

Organization of glomerular territories in the olfactory bulb of post-embryonic wild chinook salmon Oncorhynchus tshawytscha

The post-embryonic odor imprinting paradigm suggests Chinook salmon (Oncorhynchus tshawytscha) acquire memory to stream-specific amino acid olfactory odors prior to emergence as fry. Because effects of olfactory experience on development can be examined by mapping olfactory sensory neurons extending into distinct territories of glomerular neuropil in the olfactory bulb, glomerular patterning from early yolk-sac larva to fry was documented in wild salmonids, a temporal scale not yet thoroughly explored. Labeling olfactory sensory neurons with anti-keyhole limpet hemocyanin (anti-KLH) revealed seven spatially conserved glomerular territories visible at hatch and well established by the late yolk-sac larva developmental stage. Because of the responsiveness of microvillous olfactory sensory neurons to amino acids, corresponding glomeruli in the lateral bulbar region were mapped using anti-calretinin. The dorsolateral territory, distinct glomeruli of the lateral glomerular territory and the ventromedial glomeruli were immunoreactive to both KLH and calretinin. This study offers a morphological description of glomerular patterning in post-embryonic stages in wild Chinook salmon, a temporal window previously shown to be significant for olfactory imprinting. J. Morphol. 278:464–474, 2017. © 2017 Wiley Periodicals, Inc

Exposure to exogenous egg cortisol does not rescue juvenile Chinook salmon body size, condition, or survival from the effects of elevated water temperatures

Climate change is leading to altered temperature regimes which are impacting aquatic life, particularly for ectothermic fish. The impacts of environmental stress can be translated across generations through maternally derived glucocorticoids, leading to altered offspring phenotypes. Although these maternal stress effects are often considered negative, recent studies suggest this maternal stress signal may prepare offspring for a similarly stressful environment (environmental match). We applied the environmental match hypothesis to examine whether a prenatal stress signal can dampen the effects of elevated water temperatures on body size, condition, and survival during early development in Chinook salmon Oncorhynchus tshawytscha from Lake Ontario, Canada. We exposed fertilized eggs to prenatal exogenous egg cortisol (1,000 ng/ml cortisol or 0 ng/ml control) and then reared these dosed groups at temperatures indicative of current (+0°C) and future (+3°C) temperature conditions. Offspring reared in elevated temperatures were smaller and had a lower survival at the hatchling developmental stage. Overall, we found that our exogenous cortisol dose did not dampen effects of elevated rearing temperatures (environmental match) on body size or early survival. Instead, our eyed stage survival indicates that our prenatal cortisol dose may be detrimental, as cortisol-dosed offspring raised in elevated temperatures had lower survival than cortisol-dosed and control reared in current temperatures. Our results suggest that a maternal stress signal may not be able to ameliorate the effects of thermal stress during early development. However, we highlight the importance of interpreting the fitness impacts of maternal stress within an environmentally relevant context

Sperm competition, but not major histocompatibility divergence, drive differential fertilization success between alternative reproductive tactics in Chinook salmon

Post-copulatory sexual selection processes, including sperm competition and cryptic female choice (CFC), can operate based on major histocompatibility (MH) genes. We investigated sperm competition between male alternative reproductive tactics (jack (sneaker) and hooknose (guard)) of Chinook salmon (Oncorhynchus tshawytscha). Using a full factorial design, we examined in vitro competitive fertilization success of paired jack and hooknose males at three time points after sperm activation (0, 15 and 60 seconds) to test for male competition, CFC and time effects on male fertilization success. We also examined egg-mediated CFC at two MH genes by examining both the relationship between competitive fertilization success and MH divergence as well as inheritance patterns of MH alleles in resulting offspring. We found that jacks sired more offspring than hooknose males at 0 seconds post-activation; however, jack fertilization success declined over time post-activation, suggesting a trade-off between sperm speed and longevity. Enhanced fertilization success of jacks (presumably via higher sperm quality) may serve to increase sneaker tactic competitiveness relative to dominant hooknose males. We also found evidence of egg-mediated CFC (i.e., female x male interaction) influencing competitive fertilization success, however CFC was not acting on the MH genes as we found no relationship between fertilization success and MH II β1 or MH I α1 divergence and we found no deviations from Mendelian inheritance of MH alleles in the offspring. Our study provides insight into evolutionary mechanisms influencing variation in male mating success within alternative reproductive tactics, thus underscoring different strategies that males can adopt to attain success

Geographic variation in sperm traits reflects predation risk and natural rates of multiple paternity in the guppy

Guppies (Poecilia reticulata) are models for understanding the interplay between natural and sexual selection. In particular, predation has been implicated as a major force affecting female sexual preferences, male mating tactics and the level of sperm competition. When predation is high, females typically reduce their preferences for showy males and engage more in antipredator behaviours, whereas males exploit these changes by switching from sexual displays to forced matings. These patterns are thought to account for the relatively high levels of multiple paternity in high-predation populations compared to low-predation populations. Here, we assess the possible evolutionary consequences of these patterns by asking whether variation in sperm traits reflect differences in predation intensity among four pairs of Trinidadian populations: four that experience relatively low levels of predation from a gape-limited predator and four that experience relatively high levels of predation from a variety of piscivores. We found that males in high-predation populations had faster swimming sperm with longer midpieces compared to males in low-predation populations. However, we found no differences among males in high- and low-predation populations with respect to sperm number, sperm head length, flagellum length and total sperm length

Mimicking Transgenerational Signals of Future Stress: Thermal Tolerance of Juvenile Chinook Salmon Is More Sensitive to Elevated Rearing Temperature Than Exogenously Increased Egg Cortisol

Elevated temperatures resulting from climate change are expected to disproportionately affect ectotherms given their biological function has a direct link to environmental temperature. Thus, as climate change leads to rapid increases in water temperatures in rivers, aquatic ectotherms, such as fish may be highly impacted. Organisms can respond to these stressors through flexible and rapid phenotypic change induced via developmental and/or transgenerational plasticity. In oviparous species, gravid females may translate environmental stress across generations via increased exposure of eggs to maternally derived glucocorticoids (i.e., maternal stress), which has been shown to result in diverse phenotypic effects in offspring. Recent studies suggest these phenotypic changes from maternal glucocorticoids may elicit predictive adaptive responses, where offspring exposed to maternal stress may be better prepared for the stressful environment they will encounter (i.e., environmental match hypothesis). We applied the environmental match hypothesis to examine whether a prenatal exogenous increase in egg cortisol may prepare Chinook salmon offspring (Oncorhynchus tshawytscha) to cope with thermal challenges after being reared in chronically elevated temperatures. Specifically, we exposed eggs to aqueous bath of cortisol-dosed (1,000 ng/mL) or control (0 ng/ml) solutions, and then raised both treatments at current (+0°C—contemporary ambient river temperature) or elevated (+3°C—projected future river temperature) thermal regimes. We quantified thermal performance in fish 7–9 month post fertilization using two methods: via critical thermal maximum (CTMax), and energetic responses (in plasma cortisol, glucose, and lactate) to environmentally relevant, but challenging thermal spikes over 3 days. Overall, we found that exposure to elevated rearing temperatures had a large impact on thermal tolerance, where elevated-temperature reared offspring had significantly higher CTMax. In comparison, egg cortisol treatment had little to no clear effects on CTMax and blood energetic response. Our study demonstrates the importance of elevated water temperatures as an inducer of offspring phenotypes (via early developmental cues), and highlights the significance of examining offspring performance in environments with ecologically relevant stressors

Multigenerational outbreeding effects in Chinook salmon (Oncorhynchus tshawytscha)

Outbreeding, mating between genetically divergent individuals, may result in negative fitness consequences for offspring via outbreeding depression. Outbreeding effects are of notable concern in salmonid research as outbreeding can have major implications for salmon aquaculture and conservation management. We therefore quantified outbreeding effects in two generations (F1 hybrids and F2 backcrossed hybrids) of Chinook salmon (Oncorhynchus tshawytscha) derived from captively-reared purebred lines that had been selectively bred for differential performance based on disease resistance and growth rate. Parental lines were crossed in 2009 to create purebred and reciprocal hybrid crosses (n = 53 families), and in 2010 parental and hybrid crosses were crossed to create purebred and backcrossed hybrid crosses (n = 66 families). Although we found significant genetic divergence between the parental lines (FST = 0.130), reciprocal F1 hybrids showed no evidence of outbreeding depression (hybrid breakdown) or favorable heterosis for weight, length, condition or survival. The F2 backcrossed hybrids showed no outbreeding depression for a suite of fitness related traits measured from egg to sexually mature adult life stages. Our study contributes to the current knowledge of outbreeding effects in salmonids and supports the need for more research to better comprehend the mechanisms driving outbreeding depression. © 2014 Springer International Publishing Switzerland

Sperm allocation in relation to female size in a semelparous salmonid

To maximize reproductive success, males have to adaptively tailor their sperm expenditure in relation to the quality of potential mates because they require time to replenish their sperm supply for subsequent mating opportunities. Therefore, in mating contexts where males must choose among females in a short period of time, as is the case with semelparous species (which die after one intensely competitive short duration breeding season), selection on sperm allocation can be expected to be a powerful selective agent that shapes the male reproductive success. We quantitatively investigated sperm allocation patterns in chum salmon in relation to perceived female quality by developing a novel method for determining the amount of sperm allocated per ejaculate during spawning bouts. We examined the relationship between sperm expenditure and the body size of paired females (a proxy of egg number and egg quality) in the absence of male–male competition in an experimental channel. The estimated amount of sperm released per spawning event was positively correlated with the size of paired females. However, the number of spawning events a female participated in, which reduces the number of eggs she spawns in each subsequent bout, did not affect this relationship. These results provide support for predictions arising from the sperm allocation hypothesis, male salmon do economize their sperm expenditure in accordance with paired female body size as predicted for their first spawning event, but males overestimate or are unable to assess the quality of females beyond size and provide more sperm than they should in theory when paired with a female that spawned previously. Overall, the observed sperm allocation pattern in chum salmon appears to be adapted to maximize reproductive success assuming female size is an honest indicator of quality, although temporal changes in a female\u27s quality during a reproductive season should be considered when examining sperm allocation strategies