Environmental and Genetic (vgll3) Effects on the Prevalence of Male Maturation Phenotypes in Domesticated Atlantic Salmon

Pre-harvest male maturation is problematic for Atlantic salmon (Salmo salar) farmers and is regulated by the environment and genetics (e.g., vgll3). Five families of all-male salmon parr (produced using YY males crossed with XX females) with different vgll3 genotypes were split between three environmental regimes in January 2018. The “advanced maturation” regime used elevated temperature (16 °C) and continuous light from January 2018 with post-smolt maturation assessed in March 2018. The “extended freshwater” regime used ambient freshwater (1–16 °C) and simulated natural photoperiod (SNP) with post-smolt maturation assessed in November 2018. The “sea transfer” regime used ambient temperatures (1–14 °C) and SNP in freshwater until May 2018 when they were transferred to 9 °C seawater with natural photoperiod for 2.5 years (final mean weight of circa. 14 kg) and assessed for post-smolt maturation, 1 sea-winter (1 SW) maturation, and 2 sea-winter (2 SW) maturation in the autumn (November/December) of 2018, 2019, and 2020, respectively. Post-smolt maturation was highest in the advanced maturation and extended freshwater regimes (39–99% depending on family) and lowest in the sea transfer regime (0–95% depending on family). In the sea transfer regime, maturity incidence increased over time (0–95% post-smolt maturation, 1–100% 1 SW, and 50–90% 2 SW maturation, depending on family). In all regimes, those homozygous for the pre-designated vgll3 “early” maturing allele had the highest incidences of maturation whilst those homozygous for the “late” allele had the lowest. A low percentage of 2 SW phenotypic and genetic females were found (0–5% depending on family), one of which was successfully crossed with an XY male resulting in progeny with an approx. 50/50 sex ratio. These results show (i) post-smolt maturation varies dramatically depending on environment although genetic regulation by vgll3 was as expected, and (ii) crossing YY sperm with XX eggs can result in XX progeny which can themselves produce viable progeny with an equal sex ratio when crossed with an XY male.publishedVersio

Effects of laboratory salmon louse infection on osmoregulation, growth and survival in Atlantic salmon

Anadromous Atlantic salmon (Salmo salar) rely on long ocean migrations to build energy stores for maturation and spawning. In seawater, wild Atlantic salmon are threatened by high salmon lice (Lepeophtheirus salmonis) infestation levels resulting from intensive salmonid sea-cage aquaculture. Salmon lice infection can cause a stress response and an osmotic imbalance in the host. The lice infection intensity threshold values for these responses, however, remain to be identified in Atlantic salmon. In order to define this under laboratory conditions, individually tagged F1 wild origin Atlantic post-smolts (40 g) were infected with salmon lice copepodids or left as uninfected controls. Twenty-eight days post infection, infected post-smolts had a mean of 0.38 (range of 0.07–0.9) mobile lice g−1 fish weight. During this period, specific growth rates (SGRs) were lower in infected than control fish (0.4 vs 1.0% day−1). Higher plasma Na+, Cl− and osmolality in infected fish also indicate osmoregulatory impairment. SGR correlated negatively with plasma Na+, Cl−, osmolality and cortisol in the infected, but not in the control group. Infection intensity (lice g−1 fish) correlated positively with mortality rate and plasma Na+, Cl−, osmolality and cortisol and correlated negatively with SGR and condition factor. Calculated lice intensity threshold values for changes in plasma ions were 0.18 lice g−1 for plasma Cl−, and 0.22 lice g−1 for plasma Na+. Moribund infected fish occurred at infection intensities above 0.2 lice g−1, and these fish had extreme plasma Cl−, Na+, osmolality and cortisol levels. There was a positive correlation between plasma cortisol and plasma Na+, Cl− and osmolality in infected fish. This study provides vital information that can be used to define thresholds in the monitoring and conservation of wild Atlantic salmon populations affected by aquaculture-driven salmon lice infestations.publishedVersio

Vertebral deformities in interspecific diploid and triploid salmonid hybrids

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Triploidy effects growth, life history strategies, and bone health in Arctic char (Salvelinus alpinus), but does not impact cataract incidence

Skeletal deformities and ocular cataracts have limited the farm performance of sterile triploid salmonids, but have not been assessed in Arctic char (Salvelinus alpinus). We repeatedly radiographed mixed-sex diploid and triploid char (n = 110/ploidy) of Hammerfest (Norway) origin reared on a natural photoperiod and temperature in freshwater over a 3-year period and assessed cataracts at termination. At the population level, triploids were significantly (p 90% in both ploidy), but severity was low (on average, 0.1). Based on the average wet body mass of immature fish and losses due to sexual maturation and mortality, mono-sex stocks of male triploid fish gave the highest return per 100 juveniles stocked, followed by diploid males, diploid females, and triploid females (87.5, 83.0, 80.8, and 69.3 kg, respectively) at the earliest opportunity to harvest (i.e. when the fish first reached 0.7–1.0 kg). Therefore, all-male triploids may provide benefits to char aquaculture although their skeletal health should be addressed.publishedVersio

Effects of light source and intensity on sexual maturation, growth and swimming behaviour of Atlantic salmon in sea cages

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Adaptive photoperiod interpretation modulates phenological timing in Atlantic salmon

Photoperiod, the portion of 24-h cycle during which an organism is exposed to illumination, is an important phenological cue in many animals. However, despite its influence on critical biological processes, there remain many unknowns regarding how variations in light intensity translate into perceived photoperiod. This experiment examined how light intensity variations affect perceived photoperiod in Atlantic salmon (Salmo salar) to determine whether photoperiod interpretation is, a) fixed such that anything above a minimum detection threshold is regarded as ‘illumination’, or b) adaptive and varies with recent light exposure. To do this we compared the frequency of smoltification and sexual maturation between groups of male parr which were exposed to one of eight light regimes on a 12:12 cycling regime (12-hour day/12-hour night). The eight regimes were divided into two treatments, four with ‘High’ daytime light intensity and four with ‘Low’ daytime light intensity. The ‘High' and ‘Low' intensity treatments were each sub-divided into four groups for which the subjective ‘night’ light intensity was 100%, 10%, 1% and 0% of the daytime light intensity, with four replicate tanks of each treatment. The results show that above a minimum detection threshold, Atlantic salmon have adaptive photoperiod interpretation which varies with recent light exposure, and that adaptive photoperiod interpretation modulates the timing of the parr-smolt transformation and sexual maturation. Further, we show that photoperiod interpretation varies between closely related families. Given the influence of phenological timing on species survival, our results reveal a critical role for integration of photoperiod interpretation in attempts to understand how geographically shifting thermal niches due to climate change will affect future populations.publishedVersio

Effects of laboratory salmon louse infection on mortality, growth, and sexual maturation in Atlantic salmon

Elevated salmon louse infection pressure generated by salmon farming represents a major threat for wild Atlantic salmon (Salmo salar). This study explored the effect of salmon lice on mortality, and body and gonad growth in F1 wild Atlantic salmon. Mature males (jacks) and immature fish were either infected with two different louse infection intensities (LIIs, 0.08 or 0.35 lice g−1) or kept as uninfected controls. Fish maturation was thereafter environmentally stimulated in seawater, followed by transfer to freshwater for 38 d to simulate river ascendance. No females matured, while 99% of the initially immature males started puberty. Jacks had high, and immature and maturing fish low, seawater mortality, independent of lice. The parasites had an LII-dependent negative effect on growth in length, weight, and condition factor in seawater. In freshwater, after the lice had detached, fish that were previously infected in seawater had reduced growth in length but not weight when compared to the uninfected control. The parasites did not affect relative gonad size in any fish phenotypes. The present results show that Atlantic salmon has a complex, and unexplored, regulation of growth when recovering from lice infection under laboratory settings. Further, the results suggest that possible negative effects of salmon louse on reproductive success in Atlantic salmon is most likely governed by the reduced body size and condition. However, further work on possible effects of salmon louse on semen quality is encouraged.publishedVersio

Atlantic salmon male post-smolt maturation can be reduced by using a 3-hour scotophase when inducing smoltification

Photoperiod regulates the occurrence of unwanted male post-smolt maturation during the production of large (>100 g) Atlantic salmon (Salmo salar) smolts. However, the optimal daylength for triggering smoltification, but not male puberty, has yet to be established. We used either continuous light (24:0 light/dark) or long days (18:6 and 21:3) after a six week “winter” zeitgeber (12:12) to induce smoltification in fish of around 120 g reared at 16 °C. The fish were sampled 1, 2, 3, and 6 weeks after the initiation of the three different photoperiod treatments (n = 153 males in total with 9–18 males/photoperiod/time point). As expected, the smoltification indicator gill Na+/K+-ATPase (NKA) was significantly (p < 0.05) elevated and peaked 2 to 3 weeks after the initiation of the different photoperiods. Pubertal males were identified in all treatments via the combined use of relative testis size and histology, plasma 11-ketotestosterone, changes in body condition, and growth rate. The total incidence of puberty was significantly higher among males on continuous light at 33% (n = 16/49) compared to 10% (6/61) and 12% (5/43) in 21:3 and 18:6, respectively. The incidence of puberty increased over time in all photoperiods, with 62% (8/13), 19% (3/16), and 38% (3/8) of the males from 24:0, 21:3, and 18:6 pubertal at week 6, respectively. The mean weight of males that went on to initiate puberty was significantly higher (13%) at the beginning of the trial compared to those that remained immature (mean weight, 127 vs 112 g, respectively), but there was no initial difference in body condition. Puberty significantly reduced gill NKA by 35% compared to immature males at week six but had no effect at earlier time-points. Photoperiod had no effect on the female GSI, and they were all considered immature. In conclusion, the incidence of male puberty during smoltification is regulated by photoperiod and leads to an earlier decline in a key indicator of seawater readiness. As such, photoperiods with a short scotophase (21:3 or 18:6) following the winter zeitgeber in a square-wave (long-short-long day) smolt regime are recommended to limit the incidence of male puberty.publishedVersio

A comparison of triploid and diploid Atlantic salmon (Salmo salar) performance and welfare under commercial farming conditions in Norway

Avoiding genetic interactions between wild and farmed Atlantic salmon is regarded as one of the major requirements for a sustainable salmon aquaculture industry. For this reason, farming functional sterile triploids has been suggested as a possible solution. However, knowledge about how triploids cope under commercial conditions is lacking. In the present study, we compared the performance of diploid and triploid Atlantic salmon among four Norwegian aquaculture companies. Diploid and triploid groups of the same genetic line were farmed in western, mid, and northern Norway under commercial conditions from seawater transfer until slaughter.Overall, triploid salmon exhibited reduced survival, higher incidence of emaciated fish, and scored, on average, a lower quality rating during primary processing. The results highlight the need for further research on how to improve the welfare and performance of triploid salmon in commercial aquaculture operations.publishedVersio

Triploid Atlantic salmon × brown trout hybrids have similar seawater growth and welfare issues as triploid Atlantic salmon, but both were heavier at harvest than their diploid counterparts

Interspecific hybridisation may improve the farm performance of sterile triploid salmonids via heterosis (i.e. hybrid vigour). We assessed growth over the final 293 days in seawater, and harvest quality, in diploid and triploid Atlantic salmon (Salmo salar) × brown trout (Salmo trutta) hybrids compared to diploid and triploid Atlantic salmon. We measured vertebral deformities, cataracts, flesh colour, gut mass, and body shape at harvest. In triploids, hybridisation had no effect on harvest size, vertebral deformities, cataracts, or body shape, but did improve fillet colouration (Mean digital SalmoFan™ score [95% CI]: 24.6 [24.4–24.9] and 26.0 [25.7–26.2] for triploid salmon and triploid hybrids, respectively) and lower relative gut size (34% lower). Compared to diploid salmon, triploid salmon were significantly heavier at harvest, triploid hybrids tended to be heavier (Post-hoc, least square means, p = 0.08), whereas diploid hybrids were 83% lighter (Mean mass [g] at harvest [95% CI]: 2676 [2470–2898], 3395 [3134–3679], 462 [401–534], and 3086 [2832–3363] for diploid salmon, triploid salmon, diploid hybrids, and triploid hybrids, respectively). However, both triploid groups had a significantly higher incidence of fish with one or more deformed vertebra (Mean % [95% CI]: 23 [14–35], 60 [47–71], 38 [20–60], and 44 [31–57] % in diploid salmon, triploid salmon, diploid hybrids, and triploid hybrids, respectively), more severe cataracts (Mean cataract score [95% CI]: 3.0 [2.7–3.3], 3.5 [3.2–3.8], 2.2 [1.7–2.6], 3.6 [3.3–4.0] for diploid salmon, triploid salmon, diploid hybrids, and triploid hybrids, respectively), and a smaller relative gut size (21% smaller) compared to diploid counterparts. In conclusion, triploid hybrids have no growth advantage over triploid salmon and suffer from similar welfare issues while only benefiting from increased fillet colour.publishedVersio