Microbiability of milk composition and genetic control of microbiota effects in sheep.

Recently, high-dimensional omics data are becoming available in larger quantities, and models have been developed that integrate them with genomics to understand in finer detail the relationship between genotype and phenotype, and thus improve the performance of genetic evaluations. Our objectives are to quantify the effect of the inclusion of microbiome data in the genetic evaluation for dairy traits in sheep, through the estimation of the heritability, microbiability, and how the microbiome effect on dairy traits decomposes into genetic and nongenetic parts. In this study we analyzed milk and rumen samples of 795 Lacaune dairy ewes. We included, as phenotype, dairy traits and milk fatty acids and proteins composition; as omics measurements, 16S rRNA rumen bacterial abundances; and as genotyping, 54K SNP chip for all ewes. Two nested genomic models were used: a first model to predict the individual contributions of the genetic and microbial abundances to phenotypes, and a second model to predict the additive genetic effect of the microbial community. In addition, microbiome-wide association studies for all dairy traits were applied using the 2,059 rumen bacterial abundances, and the genetic correlations between microbiome principal components and dairy traits were estimated. Results showed that in general the inclusion of both genetic and microbiome effect did not improve the fit of the model compared with the model with the genetic effect only. In addition, for all dairy traits the total heritability was equal to the direct heritability after fitting microbiota effects, due to a microbiability being almost zero for most dairy traits and heritability of the microbial community was very close to zero. Microbiome-wide association studies did not show operational taxonomic units with major effect for any of the dairy traits evaluated, and the genetic correlations between the first 5 principal components and dairy traits were low to moderate. So far, we can conclude that, using a substantial data set of 795 Lacaune dairy ewes, rumen bacterial abundances do not provide improved genetic evaluation for dairy traits in sheep.

Predicting feed efficiency traits in growing lambs from their ruminal microbiota.

Selecting feed-efficient sheep could improve the sustainability of this livestock production. However, most sheep breeding companies cannot afford to record feed intake to select feed-efficient animals. Past studies underlined the potential of omics data, including microbiota metabarcoding data, as proxies for feed efficiency. The study involved 277 Romane lambs from two lines divergently selected for residual feed intake (RFI). There were two objectives: check the consequences of selecting for feed efficiency over the rumen microbiota, and assess the predictive ability of the rumen microbiota for host traits. The study assessed two contrasting diets (concentrate diet and mixed diet) and two microbial groups (prokaryotes and eukaryotes). Discriminant analyses did not highlight any significant effect of sheep selection for residual feed intake on the rumen microbiota composition. Indeed, prokaryotic and eukaryotic microbiota compositions poorly discriminated the RFI lines, with averaged balanced error rates ranging from 45% to 55%. Correlations between host traits (feed efficiency and production traits) and their predictions from microbiota data varied between -0.07 and 0.56, depending on the trait, diet and sequencing. Feed intake was the most accurately predicted trait. However, predictions from fixed effects and BW were more accurate than or as accurate as predictions from the microbiota. Environmental effects can greatly affect the variability of microbiota compositions. Considering batch and environmental effects should be paramount when the predictive ability of the microbiota is assessed. This study argues why metabarcoding the rumen microbiota is not the best way to predict meat sheep production traits: fixed effects and BW were more cost-effective proxies and they led to similar or better predictive accuracies than microbiota metabarcoding (16S and 18S sequencing).

Genetic parameters for feed efficiency in Romane rams and responses to single-generation selection.

Feeding costs represent one of the highest expenditures in animal production systems. Breeding efficient animals that express their growth potential while eating less is therefore a major objective for breeders. We estimated the genetic parameters for feed intake, feed efficiency traits (residual feed intake (RFI) and feed conversion ratio (FCR)), growth and body composition traits in the Romane meat sheep breed. In these traits, selection responses to single-generation divergent selection on RFI were evaluated. From 2009 to 2016, a total of 951 male lambs were tested for 8 weeks starting from 3 months of age. They were weighed at the beginning and at the end of the testing period. Backfat thickness and muscle depth were recorded at the end of the testing period through ultrasound measurements. Feed intake was continuously recorded over the testing period using the automatic concentrate feeders. The heritability of RFI was estimated at 0.45 ± 0.08, which was higher than the heritability of FCR (0.30 ± 0.08). No significant genetic correlations were observed between RFI and growth traits. A favourable low negative genetic correlation was estimated between RFI and muscle depth (-0.30 ± 0.15), though additional data are needed to confirm these results. The selection of low RFI sires based on their breeding values led to the production of lambs eating significantly less concentrate (3% decrease in the average daily feed intake), but with the same growth as lambs from sires selected based on high RFI breeding values. We concluded that in meat sheep, RFI is a heritable trait that is genetically independent of post-weaning growth and body composition traits. A one-generation divergent selection based on RFI breeding values highlighted that substantial gains in feeding costs can be expected in selection schemes for meat sheep breeds.

Genetic parameters of body weight, egg production, and shell quality traits in the Shan Ma laying duck (Anas platyrhynchos).

Three hundred and four female ducks of the Chinese indigenous Shan Ma breed, progeny of 11 sires and 104 dams, were used to study laying traits. Among them, 264 ducks were used to study the egg shell quality traits of eggs laid at 300 days of age. The mean age at first egg was 109 days with an average egg weight of 49.6 ± 3.7 g. Between 210 and 300 days of age, egg weight increased from 65.0 ± 3.9 g to 67.0 ± 4.2 g and the mean of the number of eggs laid up to 300 days was 161 ± 15.0. Egg length was 59.57 ± 3.01 mm and egg width was 45.02 ± 1.98 mm, leading to a shape index of 1.32 ± 0.08. Egg shell thickness was about 0.31 mm whatever the shell region, and the breaking strength was 28.80 ± 8.29 N. The heritability's estimated using restricted maximum likelihood ( REML: ) methodology were high for egg weights (ranging from 0.43 to 0.61), intermediate for the number of eggs laid (ranging from 0.38 to 0.43), and low for the age at first egg (0.13). Heritability's for egg shell quality traits varied from 0.20 for the breaking strength to 0.44 for egg length, with in-between values of 0.28 for shell thickness and 0.34 for the shape index. The number of eggs laid was not genetically correlated with the age at first egg or egg weight, but was correlated with body weight (rg = +0.54 ± 0.23). High positive correlations were found between egg weight and body weight traits, and both of these traits (except egg weight at first egg) were highly and positively correlated with egg length and width. Breaking strength was genetically correlated with egg shell thickness (rg = +0.54 ± 0.19) and the shape index (rg = +0.71 ± 0.23). These results suggest that an efficient selection strategy could be implemented to improve the egg production of the pure Shan Ma duck line.

Sex impact on the quality of fatty liver and its genetic determinism in mule ducks.

Recent changes to French regulations now allow farmers to produce "foie gras" from both male and female mule ducks. The aim of this study was to assess the quality of female fatty liver and to compare, from a phenotypic and genetic point of view, liver quality in males and females. A total of 914 mule ducks (591 males and 323 females), hatched in a single pedigree batch, were reared until 86 d of age and then force-fed for 12 d, before being slaughtered. Carcasses and livers were weighed and liver quality was assessed by grading the extent of liver veining and measuring the liver melting rate, either after sterilization of 60 g of liver or pasteurization of 180 g of liver. Sexual dimorphism was observed in favor of males, with a difference of approximately 10% in carcass and liver weights and up to 54% for the liver melting rate. Moreover, one-third of female livers showed moderate to high veining, whereas this was not the case for male livers. The fatty livers of female mule ducks are, therefore, of poorer quality and could not be transformed into a product with the appellation "100% fatty liver." According to sex and parental line, heritability values ranged from 0.12 ± 0.05 to 0.18 ± 0.07 for fatty liver weight and from 0.09 ± 0.05 to 0.18 ± 0.05 for the 2 melting rate traits. The genetic correlations between the fatty liver weight and both melting rates were high (greater than +0.80) in the Muscovy population, whereas in the Pekin population, the liver weight and melting rates were less strongly correlated (estimates ranging from +0.36 ± 0.30 to +0.45 ± 0.28). Selection for lower liver melting rates without reducing the liver weight would, therefore, be easier to achieve in the Pekin population. Finally, as the 2 melting rate measurements are highly correlated (0.91 and over 0.95 for phenotypic and genetic correlations, respectively), we suggest using the easiest method, that is, sterilization of 60 g of liver.

Improving residual feed intake of mule progeny of Muscovy ducks: genetic parameters and responses to selection with emphasis on carcass composition and fatty liver quality.

In France, about 95% of the fatty liver production comes from mule ducks, an infertile hybrid cross between female common ducks (Anas platyrhynchos) and Muscovy drakes (Cairina moschata). As a hybrid, genetic improvement of the performance of mule ducks is achieved by selection of the parental populations. Feed represents two-thirds of the total costs of duck production; thus, the breeders' main concern is to improve the birds' feed efficiency without impairing their capacity to be overfed after the growing period. To obtain insight into this economically important trait, we designed a divergent selection experiment for Muscovy sires on the basis of the residual feed intake (RFI) of their male mule progeny. Residual feed intake represents the fraction of feed intake that cannot be explained by maintenance and production requirements. Data comprised records from generations 0 to 2 with 227 Muscovy sires of 2,016 mule ducks. Growth and fat deposition were measured individually for all mule ducks. Half-sib mule ducks were placed together in 1 small pen, and the feed consumption was recorded for each pen; all half-sibs therefore had the same feed intake estimates. Heritability of RFI was high (0.83 ± 0.42), and after 2 generations of selection, the differences between lines in terms of RFI (contrast of 9.13 g/d, representing 0.76 phenotypic standard deviation; P < 0.0001) and feed conversion ratio (contrast of 0.08, representing 0.28 phenotypic standard deviation; P = 0.0003) were marked. In regard to carcass traits, the low-RFI line (high-efficiency animals) had heavier legs (476 vs. 463 g; P < 0.0001) and magret muscles (268 vs. 262 g; P = 0.001) than the high-RFI line (low-efficiency animals). No differences were observed for either the liver weight or the melting rate between the 2 lines (P > 0.46). Selection on RFI thus improves the feed efficiency of animals without impairing their capacity to produce fatty liver.

Detailed analysis of the individual feeding behavior of male and female mule ducks.

The feeding behavior of 19 mule ducks (males and females) bred in a group was studied during their growth phase (between 3 and 8 wk of age) using the recording system for waterfowl feeding behavior developed in our lab. The basic feeding behavior data obtained allowed us to confirm on the one hand the reliability of our tool and, on the other hand, to compute food intake traits per day (ADFI, number of visits, and time spent feeding per day), per visit (feed intake per visit, visit duration, and visit feeding rate), and per meal (meal size, meal duration, and meal feeding rate). Daily feed intake increased with age (130 to 248 g/d) while the time spent feeding decreased from 14 to 5.5 min/d. Because the duration of visits remained stable (average 45 s), this reflected a decrease in the number of visits per day. At the same time the feed intake per visit and the feeding rate per visit increased sharply with age. The same trend was observed at the meal level for both the feed intake and the feeding rate. Feed intake did not differ between males and females, but the time spent feeding was significantly greater for females than for males (10.8 and 8.9 min per day and 53 and 37 s per visit for females and males, respectively), leading to significantly greater feeding rate for males (30 g/min) than for females (24 g/min). Grouping visits in meal events minimized the differences between genders as the meals tended to comprise fewer visits for females. Under the hypothesis of a genetic link between feeding behavior during growth and force-feeding ability of ducks, genetic selection of these behavioral traits could be included in breeding programs to improve the force-feeding capacity of mule ducks.

Detection of QTL controlling metabolism, meat quality, and liver quality traits of the overfed interspecific hybrid mule duck.

The mule duck, an interspecific hybrid obtained by crossing common duck (Anas platyrhynchos) females with Muscovy (Cairina moschata) drakes, is widely used for fatty liver production. The purpose of the present study was to detect and map single and pleiotropic QTL that segregate in the common duck species, and influence the expression of traits in their overfed mule duck offspring. To this end, we generated a common duck backcross (BC) population by crossing Kaiya and heavy Pekin experimental lines, which differ notably in regard to the BW and overfeeding ability of their mule progeny. The BC females were mated to Muscovy drakes and, on average, 4 male mule ducks hatched per BC female (1600 in total) and were measured for growth, metabolism during growth and the overfeeding period, overfeeding ability, and the quality of their breast meat and fatty liver. The phenotypic value of BC females was estimated for each trait by assigning to each female the mean value of the phenotypes of her offspring. Estimations allowed for variance, which depended on the number of male offspring per BC and the heritability of the trait considered. The genetic map used for QTL detection consisted of 91 microsatellite markers aggregated into 16 linkage groups (LG) covering a total of 778 cM. Twenty-two QTL were found to be significant at the 1% chromosome-wide threshold level using the single-trait detection option of the QTLMap software. Most of the QTL detected were related to the quality of breast meat and fatty liver: QTL for meat pH 20 min post mortem were mapped to LG4 (at the 1% genome-wide significance level), and QTL for meat lipid content and cooking losses were mapped to LG2a. The QTL related to fatty liver weight and liver protein and lipid content were for the most part detected on LG2c and LG9. Multitrait analysis highlighted the pleiotropic effects of QTL in these chromosome regions. Apart from the strong QTL for plasma triglyceride content at the end of the overfeeding period mapped to chromosome Z using single-trait analysis, all metabolic trait QTL were detected with the multitrait approach: the QTL mapped to LG14 and LG21 affected the plasma cholesterol and triglyceride contents, whereas the QTL mapped to LG2a seemed to impact glycemia and the basal plasma corticosterone content. A greater density genetic map will be needed to further fine map the QTL.

Feed efficiency in the laying duck: appropriate measurements and genetic parameters.

The objective of this study was to characterize residual feed intake (RFI) in common laying ducks by a) adjusting position and duration of the measurement period and b) estimating genetic parameters of RFI. The feed intake (FI), BW, and egg mass laid (EML) were recorded for 64 I444 common ducks at the beginning (-35 wk of age) and the middle (41-48 wk of age) of the laying curve. Much feed wastage was observed at the beginning of the laying curve and led to biased FI data. However, when laying was well-established, weekly and fortnightly FI measurements were well correlated phenotypically (Rp from 0.84 to 0.92 and from 0.91 to 0.94, respectively for weekly and fortnightly FI) with the measurements over the whole 2-mo period. Regarding egg mass laid, phenotypic correlations between the one-week measurements and the measurements over the whole 2-mo period were more variable than those for FI, ranging from 0.74 to 0.94, and similar to whatever was the period of measurement. The RFI was investigated in a second experiment based on 384 common female ducks, for which FI, EML, BW, and BW gain were recorded at 39 wk of age. The RFI was determined by multiple regression of FI on metabolic BW and EML. Heritability values of FI and RFI were 0.34 and 0.24, respectively. In addition, if the heritability values obtained for BW (0.65) and BW gain (0.09) were consistent with studies in chickens, the very low EML estimates (0.06) were unexpected. The RFI was strongly genetically linked to FI (Rg = +0.89) but appeared to be independent from BW. Selection based on RFI should therefore reduce the FI of animals without clearly modifying the other components. Moreover, the correlated responses on reproductive traits seem favorable because lower RFI values increase the number of eggs produced per year as well as the hatchability and fertility rates.

A functional genomic approach to the study of the milking ability in dairy sheep.

To understand the mechanisms underlying milk ability and more precisely the kinetics of milk emission, we compared teat transcriptome profiles from Lacaune ewes in the tails of the milk flow phenotypic distribution. Two different arrays containing respectively 1896 and 13 168 PCR products selected from several tissue-specific cDNA libraries, including mammary gland, allowed the identification of 73 differentially expressed genes between teats from high and low milk flow ewes. Genes involved in muscle contraction were identified as over-expressed, and genes encoding collagen were found to be under-expressed in teats from low milk flow ewes. We confirmed this underexpression of COL1A1 and COL1A2 in low-milk flow ewes using RT-qPCR. These results suggest that milking ability may be due to the capacity of the teat sphincter to relax during mechanical milking. We propose that an optimal condition for mechanical milking may require proper relaxation of the teats. To our knowledge, this is the first transcriptomic analysis studying milking ability, using udder tissue for gene expression profiling, which demonstrates that mechanical milking ability is not only determined by morphological features but also by tissue composition.

Genetic parameters of product quality and hepatic metabolism in fattened mule ducks.

Genetic parameters of traits related to hepatic lipid metabolism, carcass composition, and product quality of overfed mule ducks were estimated on both parental lines of this hybrid: the common duck line for the maternal side and the Muscovy line for the paternal side. The originality of the statistical model was to include simultaneously the additive genetic effect of the common ducks and that of the Muscovy ducks, revealing a greater genetic determinism in common than in Muscovy. Plasma metabolic indicators (glucose, triglyceride, and cholesterol contents) were heritable, in particular at the end of the overfeeding period, and heritabilities increased with the overfeeding stage. Carcass composition traits were highly heritable in the common line, with values ranging from 0.15 for liver weight, 0.21 for carcass weight, and 0.25 for abdominal fat weight to 0.32 for breast muscle weight. Heritabilities of technological outputs were greater for the fatty liver (0.19 and 0.08, respectively, on common and Muscovy sides for liver melting rate) than for the pectoralis major muscle (between 0.02 and 0.05 on both parental sides for cooking losses). Fortunately, the processing industry is mainly facing problems in liver quality, such as too high of a melting rate, than in meat quality. The meat quality appraisal criteria (such as texture and cooking losses), usually dependent on pH and the rate of decline of pH, were also very lowly heritable. This study demonstrated that genetic determinism of meat quality and ability of overfeeding is not similar in the common population and in the Muscovy population; traits related to fattening, muscle development, and BW have heritability values from 2 to 4 times greater on the common line than on the Muscovy line, which is relevant for considering different selection strategies.

Comparison of nonlinear and spline regression models for describing mule duck growth curves.

This study compared models for growth (BW) before overfeeding period for male mule duck data from 7 families of a QTL experimental design. Four nonlinear models (Gompertz, logistic, Richards, and Weibull) and a spline linear regression model were used. This study compared fixed and mixed effects models to analyze growth. The Akaike information criterion was used to evaluate these alternative models. Among the nonlinear models, the mixed effects Weibull model had the best overall fit. Two parameters, the asymptotic weight and the inflexion point age, were considered random variables associated with individuals in the mixed models. In our study, asymptotic weight had a greater effect in Akaike's information criterion reduction than inflexion point age. In this data set, the between-ducks variability was mostly explained by asymptotic BW. Comparing fixed with mixed effects models, the residual SD was reduced in about 55% in the latter, pointing out the improvement in the accuracy of estimated parameters. The mixed effects spline regression model was the second best model. Given the piecewise nature of growth, this model is able to capture different growth patterns, even with data collected beyond the asymptotic BW.