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Data from: Chromosome polymorphisms track trans‐Atlantic divergence and secondary contact in Atlantic salmon
Lehnert, Sarah J.; Bentzen, Paul; Kess, Tony; Lien, Sigbjorn; Horne, John B.; Clément, Marie; Bradbury, Ian R. — 2019-02-19 Pleistocene glaciations drove repeated range contractions and expansions shaping contemporary intraspecific diversity. Atlantic salmon (Salmo salar) in the western and eastern Atlantic diverged >600,000 YBP, with the two lineages isolated in different southern refugia during glacial maxima, driving trans-Atlantic genomic and karyotypic divergence. Here, we investigate genomic consequences of glacial isolation and trans-Atlantic secondary contact using 108,870 single nucleotide polymorphisms (SNPs) genotyped in 80 North American and European populations. Throughout North America, we identified extensive inter-individual variation and discrete linkage blocks within and between chromosomes with known trans-Atlantic differences in rearrangements: Ssa01/Ssa23 translocation and Ssa08/Ssa29 fusion. Spatial genetic analyses suggest independence of rearrangements, with Ssa01/Ssa23 showing high European introgression (>50%) in northern populations indicative of post-glacial trans-Atlantic secondary contact, contrasting low European ancestry genome-wide (3%). Ssa08/Ssa29 showed greater intra-population diversity suggesting a derived chromosome fusion polymorphism within North America. Evidence of potential selection on both genomic regions suggests that the adaptive role of rearrangements warrants further investigation in Atlantic salmon. Our study highlights how Pleistocene glaciations can influence large-scale intraspecific variation in genomic architecture of northern species.
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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: Temporal dynamics of the genetic clines of invasive European green crab (Carcinus maenas) in eastern North America
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Lehnert, Sarah J.; DiBacco, Claudio; Jeffery, Nicholas W.; Blakeslee, April M.H.; Isaksson, Jonatan; Roman, Joe; Wringe, Brendan F.; Stanley, Ryan R.E.; Matheson, Kyle; McKenzie, Cynthia H.; Hamilton, Lorraine C.; Bradbury, Ian R.; Stanley, Ryan R. E.; Blakeslee, April M. H. — 2018-06-05 Two genetically distinct lineages of European green crabs (Carcinus maenas) were independently introduced to eastern North America, the first in the early 19th century and the second in the late 20th century. These lineages first came into secondary contact in southeastern Nova Scotia, Canada (NS), where they hybridized, producing latitudinal genetic clines. Previous studies have documented a persistent southward shift in the clines of different marker types, consistent with existing dispersal and recruitment pathways. We evaluated current clinal structure by quantifying the distribution of lineages and fine-scale hybridization patterns across the eastern North American range (25 locations, ~39-49°N) using informative single nucleotide polymorphisms (SNPs; n=96). In addition, temporal changes in the genetic clines were evaluated using mitochondrial DNA and microsatellite loci (n=9-11) over a 15-year period (2000-2015). Clinal structure was consistent with prior work demonstrating the existence of both northern and southern lineages with a hybrid zone occurring between southern New Brunswick (NB) and southern NS. Extensive later generation hybrids were detected in this region and in southeastern Newfoundland. Temporal genetic analysis confirmed the southward progression of clines over time; however, the rate of this progression was slower than predicted by forecasting models, and current clines for all marker types deviated significantly from these predictions. Our results suggest that neutral and selective processes contribute to cline dynamics, and ultimately, highlight how selection, hybridization, and dispersal can collectively influence invasion success.
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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: Neutral genetic variation in adult Chinook salmon (Oncorhynchus tshawytscha) affects brain-to-body trade-off and brain laterality
Wiper, Mallory L.; Lehnert, Sarah J.; Heath, Daniel D.; Higgs, Dennis M. — 2017-11-06 Low levels of heterozygosity can have detrimental effects on life history and growth characteristics of organisms but more subtle effects such as those on trade-offs of expensive tissues and morphological laterality, especially of the brain, have not been explicitly tested. The objective of the current study was to investigate how estimated differences in heterozygosity may potentially affect brain-to-body trade-offs and to explore how these heterozygosity differences may affect differential brain growth, focusing on directional asymmetry in adult Chinook salmon (Oncorhynchus tshawytscha) using the laterality and absolute laterality indices. Level of inbreeding was estimated as mean microsatellite heterozygosity resulting in four ‘inbreeding level groups’ (Very High, High, Medium, Low). A higher inbreeding level corresponded with a decreased brain-to-body ratio, thus a decrease in investment in brain tissue, and also showed a decrease in the laterality index for the cerebellum, where the left hemisphere was larger than the right across all groups. These results begin to show the role that differences in heterozygosity may play in differential tissue investment and in morphological laterality, and may be useful in two ways. Firstly, the results may be valuable for restocking programmes that wish to emphasize brain or body growth when crossing adults to generate individuals for release, as we show that genetic variation does affect these trade-offs. Secondly, this study is one of the first examinations to test the hypothesized relationship between genetic variation and laterality, finding that in Chinook salmon there is potential for an effect of inbreeding on lateralized morphology, but not in the expected direction.
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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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(auteur : Lehnert, Sarah J.)

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