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Data from: Red and white Chinook salmon: genetic divergence and mate choice
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Lehnert, Sarah J.; Pitcher, Trevor E.; Devlin, Robert H.; Heath, Daniel D. — 2016-01-25 Chinook salmon (Oncorhynchus tshawytscha) exhibit extreme differences in coloration of skin, eggs and flesh due to genetic polymorphisms affecting carotenoid deposition, where colour can range from white to bright red. A sympatric population of red and white Chinook salmon occurs in the Quesnel River, British Columbia, where frequencies of each phenotype are relatively equal. In our study, we examined evolutionary mechanisms responsible for the maintenance of the morphs, where we first tested whether morphs were reproductively isolated using microsatellite genotyping, and second, using breeding trials in seminatural spawning channels, we tested whether colour assortative mate choice could be operating to maintain the polymorphism in nature. Next, given extreme difference in carotenoid assimilation and the importance of carotenoids to immune function, we examined mate choice and selection between colour morphs at immune genes (major histocompatibility complex genes: MHC I-A1 and MHC II-B1). In our study, red and white individuals were found to interbreed, and under seminatural conditions, some degree of colour assortative mate choice (71% of matings) was observed. We found significant genetic differences at both MHC genes between morphs, but no evidence of MHC II-B1-based mate choice. White individuals were more heterozygous at MHC II-B1 compared with red individuals, and morphs showed significant allele frequency differences at MHC I-A1. Although colour assortative mate choice is likely not a primary mechanism maintaining the polymorphisms in the population, our results suggest that selection is operating differentially at immune genes in red and white Chinook salmon, possibly due to differences in carotenoid utilization.
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Data from: Redder isn’t always better: cost of carotenoids in Chinook salmon eggs
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Lehnert, Sarah J.; Devlin, Robert H.; Pitcher, Trevor E.; Semeniuk, Christina A.D.; Heath, Daniel D. — 2016-11-30 Carotenoids provide animals with many fitness benefits through increased mating success, immune function, gamete quality, and antioxidant capacity. Despite these benefits, carotenoids are not utilized equally by all animals, implying trade-offs associated with the pigments; although, few studies have quantified fitness costs of carotenoid pigmentation. Salmon are known for their conspicuous red coloration; however, amongst Chinook salmon (Oncorhynchus tshawytscha), a natural genetic color polymorphism exists (red and white morphs) which results in carotenoid-based color differences in eggs and other tissues. Although the fitness benefit of egg carotenoid content on egg incubation survival has been demonstrated, carotenoid pigmentation also results in highly visible eggs vulnerable to predation. Therefore, although white Chinook salmon eggs experience costs in terms of viability, a potential benefit in terms of reduced predation could help explain the maintenance of the polymorphism. Here, using red and white eggs from wild Chinook salmon, we show that increased carotenoid content of salmon eggs leads to greater predation risk. We found that 2 populations of wild-type rainbow trout (O. mykiss; an ecologically relevant predator) showed a significant bias for red eggs over white eggs under choice experiments, where red eggs were consumed first twice as often and significantly faster than white eggs. Our study suggests that trade-offs between red and white Chinook salmon during the egg stage provide an evolutionary mechanism promoting the maintenance of the unique Chinook salmon color polymorphism in nature, while also, for the first time, demonstrating a direct fitness cost of carotenoids in salmon.
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Data from: Significant differences in maternal carotenoid provisioning and effects on offspring fitness in Chinook salmon colour morphs
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Lehnert, Sarah J.; Garver, Kyle A.; Richard, Jon; Devlin, Robert H.; Lajoie, Celine; Pitcher, Trevor E.; Heath, Daniel D. — 2018-10-02 In oviparous species, maternal carotenoid provisioning can deliver diverse fitness benefits to offspring via increased survival, growth, and immune function. Despite demonstrated advantages of carotenoids, large intra‐ and interspecific variation in carotenoid utilization exists, suggesting trade‐offs associated with carotenoids. In Chinook salmon (Oncorhynchus tshawytscha), extreme variation in carotenoid utilization delineates two colour morphs (red and white) that differ genetically in their ability to deposit carotenoids into tissues. Here, we take advantage of this natural variation to examine how large differences in maternal carotenoid provisioning influence offspring fitness. Using a full‐factorial breeding design crossing morphs and common‐garden rearing, we measured differences in a suite of fitness‐related traits, including survival, growth, viral susceptibility, and host response, in offspring of red (carotenoid‐rich eggs) and white (carotenoid‐poor eggs) females. Eggs of red females had significantly higher carotenoid content than those of white females (6X more); however, this did not translate into measurable differences in offspring fitness. Given that white Chinook salmon may have evolved to counteract their maternal carotenoid deficiency, we also examined the relationship between egg carotenoid content and offspring fitness within each morph separately. Egg carotenoids only had a positive effect within the red morph on survival to eyed‐egg (earliest measured trait), but not within the white morph. While previous work shows that white females benefit from reduced egg predation, our study also supports a hypothesis that white Chinook salmon have evolved additional mechanisms to improve egg survival despite low carotenoids, providing novel insight into evolutionary mechanisms that maintain this stable polymorphism.
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Data from: Effects of ovarian fluid and genetic differences on sperm performance and fertilization success of alternative reproductive tactics in Chinook salmon
Lehnert, Sarah J.; Butts, Ian A.E.; Flannery, Erin W.; Peters, Kia M.; Heath, Daniel D.; Pitcher, Trevor E.; Butts, I. A. E. — 2017-04-04 In many species, sperm velocity affects variation in the outcome of male competitive fertilization success. In fishes, ovarian fluid (OF) released with the eggs can increase male sperm velocity and potentially facilitate cryptic female choice for males of specific phenotypes and/or genotypes. Therefore, to investigate the role of OF on fertilization success, we measured sperm velocity and conducted in vitro competitive fertilizations with paired Chinook salmon (Oncorhynchus tshawytscha) males representing two alternative reproductive tactics, jacks (small sneaker males) and hooknoses (large guarding males), in the presence of river water alone and OF mixed with river water. To determine the role of genetic differences on fertilization success, we genotyped fish at neutral (microsatellites) and functional [major histocompatibility complex (MHC) II ß1] markers. We found that when sperm were competed in river water, jacks sired significantly more offspring than hooknoses, however, in OF there was no difference in paternity between the tactics. Sperm velocity was significantly correlated with paternity success in river water but not in ovarian fluid. Paternity success in OF, but not in river water alone, was correlated with genetic relatedness between male and female, where males that were less related to the female attained greater paternity. We found no relationship between MHC II ß1 divergence between mates and paternity success in water or OF. Our results indicate that OF can influence the outcome of sperm competition in Chinook salmon, where OF provides both male tactics with fertilization opportunities, which may in part explain what maintains both tactics in nature.
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Data from: Sperm competition, but not major histocompatibility divergence, drives differential fertilization success between alternative reproductive tactics in Chinook salmon
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Lehnert, Sarah J.; Helou, Leila; Pitcher, Trevor E.; Heath, John W.; Heath, Daniel D. — 2017-10-17 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 s) 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 s 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 × 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.

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(Author: Pitcher, Trevor E.)

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