Phenotypic and genetic analysis of milk and serum element concentrations in dairy cows.

Enhancing micronutrient (i.e., mineral and vitamin) concentrations within milk and serum from dairy cows is important for both the health of the cow and the nutritive value of the milk for human consumption. However, a good understanding of the genetics underlying the micronutrient content in dairy cattle is needed to facilitate such enhancements through feeding or breeding practices. In this study, milk (n = 950) and serum (n = 766) samples were collected from Holstein-Friesian dairy cows (n = 479) on 19 occasions over a 59-mo period and analyzed for concentrations of important elements. Additionally, a subset of 256 milk samples was analyzed for concentrations of vitamin B12. Cows belonged to 2 genetic lines (average and highest genetic merit for milk fat plus protein yield) and were assigned to 1 of 2 diets based on either a by-product or homegrown ration. Univariate models accounting for repeated records were used to analyze element and vitamin B12 data and investigate the effect of genotype and feeding system as well as derive estimates of variance components and genetic parameters. Bivariate models were used to study correlations both within and between milk and serum. Only concentrations of Hg in milk were seen to be affected by genotype, with higher concentrations in cows with high genetic merit. In contrast, element concentrations were influenced by feeding system such that cows fed the homegrown diet had increased milk concentrations of Ca, Cu, I, Mn, Mo, P, and K and increased serum concentrations of Cd, Cu, Fe, Mo, and V. Cows on the by-product diet had increased milk concentrations of Mg, Se, and Na and increased serum concentrations of P and Se. Heritability (h2) estimates were obtained for 6 milk and 4 serum elements, including Mg (h2milk = 0.30), K (h2serum = 0.18), Ca (h2milk = 0.20; h2serum = 0.12), Mn (h2milk = 0.14), Cu (h2serum = 0.22), Zn (h2milk = 0.24), Se (h2milk = 0.15; h2serum = 0.10), and Mo (h2milk = 0.19). Significant estimates of repeatability were observed in all milk and serum quantity elements (Na, Mg, P, K, and Ca) as well as 5 milk and 7 serum trace elements. Only K in milk and serum was found to have a significant positive genetic and phenotypic correlation (0.52 and 0.22, respectively). Significant phenotypic associations were noted between milk and serum Ca (0.17), Mo (0.19), and Na (-0.79). Additional multivariate analyses between measures within sample type (i.e., milk or serum) revealed significant positive associations, both phenotypic and genetic, between some of the elements. In milk, Se was genetically correlated with Ca (0.63), Mg (0.59), Mn (0.40), P (0.53), and Zn (0.52), whereas in serum, V showed strong genetic associations with Cd (0.71), Ca (0.53), Mn (0.63), Mo (0.57), P (0.42), K (0.45), and Hg (-0.44). These results provide evidence that element concentrations in milk and blood of dairy cows are significantly influenced by both diet and genetics and demonstrate the potential for genetic selection and dietary manipulation to alter nutrient concentration to improve both cow health and the healthfulness of milk for human consumption.

Immune-associated traits measured in milk of Holstein-Friesian cows as proxies for blood serum measurements.

Previous work has highlighted that immune-associated (IA) traits measurable in blood are associated with health, productivity, and reproduction in dairy cows. The aim of the present study was to determine relationships between IA traits measured in blood serum and those simultaneously measured in milk as well as their association with disease phenotypes. All animals were Holstein-Friesian cows from the Langhill research herd (n = 546) housed at the SRUC Dairy Research Centre in Scotland. Milk and serum samples were collected on 20 separate occasions between July 2010 and March 2015 and analyzed by ELISA for haptoglobin (Hp), tumor necrosis factor-α (TNF-α), and natural antibodies binding keyhole limpet hemocyanin (NAbKLH) and lipopolysaccharide (NAbLPS). Data were analyzed using mixed linear models that included pedigree information. Analyses revealed positive phenotypic correlations between milk and serum NAb (0.59 ≤ r ≤ 0.77), Hp (r = 0.37), and TNF-α (r = 0.12). Milk and serum NAb were also found to have a strong genetic correlation (0.81 ≤ r ≤ 0.94) and were genetically correlated with cow lameness (0.66 and 0.79 for milk NAbKLH and serum NAbLPS, respectively). Clinical mastitis was found to be phenotypically correlated with both milk and serum Hp (0.09 ≤ r ≤ 0.23). Serum Hp was also strongly genetically correlated with other cellular IA traits such as percent NKp46+ (a natural killer cell marker; 0.35) and percent peripheral blood mononuclear cells (PBMC; -0.90). Similarly, genetic correlations were found to exist between serum TNF-α and percent NKp46+ (0.22), percent PBMC (0.41), and percent lymphocytes (0.47). Excluding serum Hp, all milk and serum IA traits were repeatable, ranging from 0.11 (milk Hp) to 0.43 (serum NAbLPS). Between-animal variation was highest in milk and serum NAb (0.34-0.43) and significant estimates of heritability were also observed in milk and serum NAb (0.17-0.37). Our findings show that certain IA traits, such as NAbKLH and NAbLPS, found in milk and serum are strongly correlated and highlight the potential of using routinely collected milk samples as a less invasive and cost-effective source of informative data for predictive modeling of animal IA traits.

Correction: Predicting the Potential for Natural Recovery of Atlantic Salmon (Salmo salar L.) Populations following the Introduction of Gyrodactylus salaris Malmberg, 1957 (Monogenea).

[This corrects the article DOI: 10.1371/journal.pone.0169168.].

Estimating genetic and phenotypic parameters of cellular immune-associated traits in dairy cows.

Data collected from an experimental Holstein-Friesian research herd were used to determine genetic and phenotypic parameters of innate and adaptive cellular immune-associated traits. Relationships between immune-associated traits and production, health, and fertility traits were also investigated. Repeated blood leukocyte records were analyzed in 546 cows for 9 cellular immune-associated traits, including percent T cell subsets, B cells, NK cells, and granulocytes. Variance components were estimated by univariate analysis. Heritability estimates were obtained for all 9 traits, the highest of which were observed in the T cell subsets percent CD4+, percent CD8+, CD4+:CD8+ ratio, and percent NKp46+ cells (0.46, 0.41, 0.43 and 0.42, respectively), with between-individual variation accounting for 59 to 81% of total phenotypic variance. Associations between immune-associated traits and production, health, and fertility traits were investigated with bivariate analyses. Strong genetic correlations were observed between percent NKp46+ and stillbirth rate (0.61), and lameness episodes and percent CD8+ (-0.51). Regarding production traits, the strongest relationships were between CD4+:CD8+ ratio and weight phenotypes (-0.52 for live weight; -0.51 for empty body weight). Associations between feed conversion traits and immune-associated traits were also observed. Our results provide evidence that cellular immune-associated traits are heritable and repeatable, and the noticeable variation between animals would permit selection for altered trait values, particularly in the case of the T cell subsets. The associations we observed between immune-associated, health, fertility, and production traits suggest that genetic selection for cellular immune-associated traits could provide a useful tool in improving animal health, fitness, and fertility.

Predicting the Potential for Natural Recovery of Atlantic Salmon (Salmo salar L.) Populations following the Introduction of Gyrodactylus salaris Malmberg, 1957 (Monogenea).

Gyrodactylus salaris (Monogenea, Platyhelminthes) is a notifiable freshwater pathogen responsible for causing catastrophic damage to wild Atlantic salmon stocks, most notably in Norway. In some strains of Baltic salmon (e.g., from the river Neva) however, the impact is greatly reduced due to some form of innate resistance that regulates parasite numbers, resulting in fewer host mortalities. Gyrodactylus salaris is known from 17 European states; its status in a further 35 states remains unknown; the UK, the Republic of Ireland and certain watersheds in Finland are free of the parasite. Thus, the parasite poses a serious threat if it emerges in Atlantic salmon rearing regions throughout Europe. At present, infections are generally controlled via extreme measures such as the treatment of entire river catchments with the biocide rotenone, in order to remove all hosts, before restocking with the original genetic stock. The use of rotenone in this way in EU countries is unlikely as it would be in contravention of the Water Framework Directive. Not only are such treatments economically and environmentally costly, they also eradicate the potential for any host/parasite evolutionary process to occur. Based on previous studies, UK salmon stocks have been shown to be highly susceptible to infection, analogous to Norwegian stocks. The present study investigates the impact of a G. salaris outbreak within a naïve salmon population in order to determine long-term consequences of infection and the likelihood of coexistence. Simulation of the salmon/ G. salaris system was carried out via a deterministic mathematical modelling approach to examine the dynamics of host-pathogen interactions. Results indicated that in order for highly susceptible Atlantic strains to evolve a resistance, both a moderate-strong deceleratingly costly trade-off on birth rate and a lower overall cost of the immune response are required. The present study provides insights into the potential long term impact of G. salaris if introduced into G. salaris-free territories and suggests that in the absence of external controls salmon populations are likely to recover to high densities nearing 90% of that observed pre-infection.

Reservoir hosts for Gyrodactylus salaris may play a more significant role in epidemics than previously thought.

BACKGROUND: Gyrodactylus salaris Malmberg, 1957 has had a devastating impact on wild Norwegian stocks of Atlantic salmon Salmo salar L., and it is the only Office International des Epizooties (OIE) listed parasitic pathogen of fish. The UK is presently recognised as G. salaris-free, and management plans for its containment and control are currently based on Scandinavian studies. The current study investigates the susceptibility of British salmonids to G. salaris, and determines whether, given the host isolation since the last glaciation and potential genetic differences, the populations under test would exhibit different levels of susceptibility, as illustrated by the parasite infection trajectory over time, from their Scandinavian counterparts. METHODS: Populations of S. salar, brown trout Salmo trutta L., and grayling Thymallus thymallus (L.), raised from wild stock in UK government hatcheries, were flown to Norway and experimentally challenged with a known pathogenic strain of G. salaris. Each fish was lightly anaesthetised and marked with a unique tattoo for individual parasite counting. A single Norwegian population of S. salar from the River Lærdalselva was used as a control. Parasite numbers were assessed every seven days until day 48 and then every 14 days. RESULTS: Gyrodactylus salaris regularly leads to high mortalities on infected juveniles S. salar. The number of G. salaris on British S. salar rose exponentially until the experiment was terminated at 33 days due to fish welfare concerns. The numbers of parasites on S. trutta and T. thymallus increased sharply, reaching a peak of infection on days 12 and 19 post-infection respectively, before declining to a constant low level of infection until the termination of the experiment at 110 days. CONCLUSIONS: The ability of S. trutta and T. thymallus to carry an infection for long periods increases the window of exposure for these two hosts and the potential transfer of G. salaris to other susceptible hosts. This study demonstrates that G. salaris can persist on S. trutta for longer periods than previously thought, and that the role that S. trutta could play in disseminating G. salaris needs to be considered carefully and factored into management plans and epidemics across Europe.

Reproductive trade-offs may moderate the impact of Gyrodactylus salaris in warmer climates.

Gyrodactylus salaris is a notifiable freshwater ectoparasite of salmonids. Its primary host is Atlantic salmon (Salmo salar), upon which infections can cause death, and have led to massive declines in salmon numbers in Norway, where the parasite is widespread. Different strains of S. salar vary in their susceptibility, with Atlantic strains (such as those found in Norway) exhibiting no resistance to the parasite, and Baltic strains demonstrating an innate resistance sufficient to regulate parasite numbers on the host causing it to either die out or persist at a low level. In this study, Leslie matrix and compartmental models were used to generate data that demonstrated the population growth of G. salaris on an individual host is dependent on the total number of offspring per parasite, its longevity and the timing of its births. The data demonstrated that the key factor determining the rate of G. salaris population growth is the time at which the parasite first gives birth, with rapid birth rate giving rise to large population size. Furthermore, it was shown that though the parasite can give birth up to four times, only two births are required for the population to persist as long as the first birth occurs before a parasite is three days old. As temperature is known to influence the timing of the parasite's first birth, greater impact may be predicted if introduced to countries with warmer climates than Norway, such as the UK and Ireland which are currently recognised to be free of G. salaris. However, the outputs from the models developed in this study suggest that temperature induced trade-offs between the total number of offspring the parasite gives birth to and the first birth timing may prevent increased population growth rates over those observed in Norway.