Heritabilities and genetic analysis of milk yield and components in crossing project of Saudi rabbits with Spanish V-line

K A Al-Sobayil, A H Al-Homidan, M H Khalil and M A Mehaia

Department of Animal Production and Breeding, College of Agriculture and Veterinary Medicine, Al-Qassim University,
Buriedah P.O.Box 1482, Saudi Arabia
maherhkhalil@yahoo.com

Abstract

A four-year crossbreeding project involving Spanish maternal line called V-line (V) and Saudi Gabali (G) rabbits was carried out to produce six genetic groups of V, G, ½V½G, ½G½V, ¾V¼G and ¾G¼V. Inter se matings for genetic groups of ½V½G, ½G½V, ¾V¼G and ¾G¼V were also practiced. Milk yields (MY) at intervals of 0-7 days (MY7), 7-21 days (MY21), 21-28 days (MY28), and 0-28 days (TMY) and milk components (MC) at 14 days of lactation (fat, protein, lactose, ash, and total solids) were evaluated for 2141 litters of 854 does fathered by 142 sires and mothered by 351 dams. A repeatability animal model was used to estimate the corresponding parameters as the heritabilities, the differences between line V and Gabali in additive direct effects (G^I_V-G) and maternal additive effects (G^M_V-G). The individual (H^I) and maternal (H^M) heterosis, and direct recombination effect (R^I) were also estimated.

Heritabilities for MY traits were moderate, ranging from 0.18 to 0.22, while they were low or moderate and ranging from 0.09 to 0.28 for MC. The positive estimates of G^I_V-G for MY (5.6-14.5%) and MC (4.0-18.7%) were significantly high and in favour of V-line does. Estimates of G^M_V-G were in favour of V-line dams; being 222 g, 0.67% and -0.08 for MY21, total solids in milk, and fat in milk, respectively. All estimates of H^I for MY and MC were positive and most of them were significant; ranging from 9.7 to 22.7 % for MY traits (P<0.05-0.001) and 6.0 to 15.8% for MC traits (P<0.05-0.01). Similar to the trend of H^I, the estimates of H^M for MY and MC were positively moderate and ranging from 7.4 to 15.2 % for MY traits and 1.9 to 8.3% for MC. The ranges in percentages of reduction in direct heterosis were negligible and ranging from 2.2 to 5.3% for MY traits and 3.4 to 9.6% for MC. In practice, crossbred does and dams involving V-line genes in their constitutions gave favourable heterotic effects on milk traits and therefore these crossbred does and dams can produce and lactate efficiently under hot climatic conditions.

Key words: Animal model, crossbreeding, heritability, milk yield and components, rabbits

Introduction

Genetic diversity of rabbit breeds in terms of milk production offers the opportunity to increase the efficiency of doe productivity through crossbreeding. To date, genetic analysis concerning milk yield (MY) and components (MC) for crossbred rabbits raised in hot climate countries are scarce. Further, milk production and milk components are expensive to record. Other traits that are associated with them, are more directly related with production and are easier to record, such as litter size at birth or at weaning (Estany et al 1989; Rochambeau et al 1998; Gomez et al 1996; Capra et al 2000; Garcia et al 2000), litter size at weaning and individual weight at weaning (Moura et al 2001), litter size at weaning and individual weight gain (Gomez et al 2000), and litter weight at weaning (Salaun et al 2001; Garreau and Rochambeau 2003). These traits, in a great part, can replace milk yield as criteria for selection. However, selecting does directly for yields and components of milk should be of considerable interest and importance (Garreau and Rochambeau 2003; Baselga 2004; Garreau et al 2004).

The objective of our study was to estimate direct (G^I_V-G) and maternal (G^M_V-G) additive effects, direct heterosis (H^I), maternal heterosis (H^M) and direct recombination effects (R^I), as well as heritabilities, for MY and MC traits in a crossbreeding project involving Spanish V-line rabbits and Gabali Saudi rabbits.

Materials and methods

The four-year crossbreeding project was started in October 2000 in the experimental rabbitry, College of Agriculture and Veterinary Medicine, El-Qassim region, King Saud University, Saudi Arabia.

Breeding plan, management, farm environment and feeding

Rabbits used in this study represent one desert Saudi breed (Gabali, G) and one exotic breed (Spanish V-line, V). The breeding plan permitted simultaneous production of ten genetic groups. Distribution of number of litters weaned in these genetic groups across different years of kindling is presented in Table 1.

A total number of 2541 litters were born by 854 does, fathered by 142 sires and mothered by 351 dams. The bucks were randomly assigned to mate the does naturally with the restriction to avoid the matings of animals with common grandparents. Young rabbits were weaned at four weeks of age. Rabbits were raised in a semi-closed rabbitry. Breeding does and bucks were housed separately in individual wired-cages. All cages are equipped with feeding hoppers and drinking nipples. In the rabbitry, the environmental conditions were monitored; temperature ranged from 20 to about 32 °C, the relative humidity ranged from 20 to 50 % and photoperiod was 16L: 8D. Rabbits were fed a commercial grower pelleted diet during the whole experimental period, which lasted 16 weeks of age. On dry matter (DM) basis, the diet contained 18.5% crude protein (CP), 8.0% crude fiber (CF), 3.0% ether extract (EE) and 6.5% ash. Feed and water were available ad libitum.

Milk yields and components

Milk yields (MY) were recorded during the first seven days (MY7), 7-21 days (MY21), 21-28 days (MY28) and for the total 0-28 days (TMY). Litter weight at birth (LWB) and litter weight at weaning (LWW) were also recorded. Milk yield of does was recorded using weigh-suckle-weigh method. MC of fat, protein, lactose, ash and total solids (g/100g) were also estimated. In the evening of the day prior to collection, the kits were separated from their mothers to prevent suckling for a period of 12 hours before sample collection in the next morning. Milk samples were collected manually by gently massaging the mammary gland after two minutes of injection with 0.1 ml of oxytocin hormone to enhance maximum contraction of myoepithelial cells. Samples were taken per doe per litter in the morning of the 15^th day of lactation. The samples were cooled and transferred immediately to the laboratory for chemical analysis. Milk sample for each litter born per doe was analysed for total solids, and ash according to procedures outlined in AOAC (1980). Fat was determined by Gerber method as described by Case et al (1985), nitrogen by the standard micro-Kjeldahl method (AOAC 1980). A nitrogen conversion factor of 6.38 was used to calculate protein content. Lactose was determined by subtraction.

Statistical analysis

Repeatability animal model (in matrix notation) used for analysing milk traits was (Boldman et al 1995):

y= Xb + Z_au_a + Z_pu_p + e

Where
y = vector of observed lactation trait for does,
b= vector of fixed effects of genetic group of doe (ten levels; see Table 1), year-season of kindling (one year season every three months), and physiological status of the doe (five levels depending on the parity order and lactation state at the moment of insemination: 1 for nulliparous, 2 for primiparous lactating, 3 for multiparous lactating, 4 for primiparous non-lactating, 5 for multiparous non-lactating);
u_a= vector of random additive effect of the does and sires,
u_p= vector of random effects of the permanent environment (permanent non-additive effect);
X, Z_a and Z_p are the incidence matrices relating records to the fixed effects, additive genetic effects, and permanent environment, respectively; and e= vector of random residual effects.

Variance components of direct additive effects, permanent environmental effects and errors were estimated by DFREML procedure using the animal model (Boldman et al 1995). The inverse of the numerator relationship matrix (A^-1) was considered; Var(u_a)= As²_a, Var(u_p)= Is²_p and Var(e)= Is²_e. Heritabilities for different traits were computed from variance components using the following equations:

The variance components estimated before should be used to solve the model and get solutions for the ten genetic groups (D_i, i= 1 to 10) and the corresponding variance-covariance matrix of the errors. This information should be used to compute later the estimable functions D_i-D₂ and their variance-covariance matrix of errors.

Genetic model and estimation of crossbreeding effects

The Dickerson's genetic model (Dickerson 1992) was used to explain the performances of the different genetic groups. The genetic model take into account the direct additive effects of the line or breed (e.g. G^I_G, for Gabali), the maternal additive effects (e.g. G^M_V, for line V), the individual (H^I) and maternal (H^M) heterosis between Gabali and line V and the direct recombination effect (R^I). Because of linear dependence between the equations of the fixed factors, estimable functions used are D_i-D₂ that allow to estimate the following combinations of parameters of the Dickerson's genetic model: G^I_V-G = G^M_V - G^I_G; G^M_V-G =G^M_V- G^M_G, H^I, H^M and R^I. Table 2 shows the coefficients of the previous combination of parameters for the functions D_i-D₂ that are used with their variance-covariance matrix of errors to get generalised least square estimates of G^I_V-G, G^M_V-G, H^I, H^M and R^I, their standard errors and the corresponding Student's t-test.

Results and discussion

Actual means and variations

To characterize the experiment phenotypically, means, standard deviations, minimum and maximum values for milk traits are presented in Table 3.

However, wide phenotypic variations in all traits were observed. >From producers point of view, milk yield and milk components showed moderate lactational performances particularly for hot climate areas. In hot countries, little lower values for milk yield were reported by Khalil and Afifi (2000) and much lower values by Lahari and Mahjan (1984), Khalil (1994) and Abd El-Aziz et al (2002). Cowie (1969) reported that Dutch does (as a small breed) produced less milk in the first six weeks of lactation than New Zealand White does (3820 gram v. 6940 gram). Lukefahr et al (1983) in USA found that New Zealand White was superior to Californian rabbits in lactational yield. Lahari and Mahajan (1984) in India reported that differences in daily milk yield at 21 days of age among Grey Giant (GG), Soviet Chinchilla (SC), White Giant (WG), New Zealand White (NZW) and Russian Angora (RA) were not significant but GG had the highest yield (189 g per day) followed by RA (147g), SC (139g), WG (134g) and NZW (116g). El-Sayiad et al (1994) with New Zealand White (NZW) and Californian (CAL) rabbits in Egypt stated that the differences between the two breeds in fat, protein, lactose, ash and energy of milk were not significant; the estimates were 14.0, 13.6, 1.9, 2.1% and 87.9 kJ/100g in NZW and 14.0, 14.3, 2.0, 2.2% and 89.9 kJ/100g in CAL for fat, protein, lactose, ash and energy of milk, respectively. Such discrepancies among reports may be due to the strain of breed used, breed x environment interaction or different experimental methods.

Total differences between genetic groups

Deviations of each genetic group from Gabali (D_i-D₂) for different milk traits are presented in Table 4. These deviations are interesting to show the global performance of the V-line, the Gabali breed and their different crosses in order to identify their possibilities to be used as pure stock or as a simple cross or to be used as synthetic line. For all milk traits, V-line rabbits recorded better lactational performance compared to Gabali rabbits (Table 4). Clear differences among the ten genetic groups were notified for fat, protein and total solids in milk.

The highest percentages of total solids (fat, lactose and protein) were recorded for (¾G¼V)² group (31.0 %), while the least values were recorded for G group (27.3%). In most cases (MY7, MY21, MY28 and TMY), genetic group of (¾V¼G)² or (¾G¼V)² gave higher milk yield and components compared to the other genetic groups (Table 4). The above mentioned results indicate that involving V-line genes in crossbreeding program with Gabali rabbits was associated with an improvement in the lactational performance of the crossbred does obtained.

Additive and permanent environmental effects and heritability estimates

Ratios of variance components of direct additive effect (heritabilities, h²) and permanent environment (p²) to the phenotypic variances are presented in Table 5.

Heritabilities for yield traits were moderate, ranging from 0.18 to 0.22, while they were low or moderate and ranging from 0.09 to 0.28 for milk components (Table 5). However, the estimates of heritability obtained in the present study for milk traits are within the ranges of estimates cited in the literature (Lahiri and Mahajan 1984; El-Maghawry et al 1993; Ayyat et al 1995; Lukefahr et al 1996; Khalil et al 2005).

Similar to the trend of direct additive effect (heritabilities, h²), the ratios of permanent environment effects were moderate and ranged from 0.23 to 0.28 for milk yields, while these ratios were low and ranging from 0.06 to 0.12 for milk components. However, high contribution of permanent environment to variation of milk traits may have considerable adverse effects on heterosis of these traits.

Direct (G^I) and maternal (G^M) breed additive effects

Estimates of G^I_V-G for most milk yields and components were significantly moderate or high in favour of V-line rabbits (Table 6). Line V is a maternal line of rabbits selected for litter size at weaning, being the animals genetically evaluated by a BLUP methodology under an animal-repeatability model (Estany et al 1989).

Estimates of G^I_V-G were found to be 59, 242, 122, and 395 grams in MY7, MY21, MY28, and TMY, respectively. The figures attained for milk components were 1.24, 0.47, 0.38, 0.13 and 1.22 % higher in fat, protein, lactose, ash and total solids in V-line does compared to G does, respectively. This superiority of V-line does in G^I_V-G is in agreement with its long history of selection for litter size at weaning and its high average for this trait (Estany et al 1989). This might be due to increased milk production levels in V-line does compared to G does. Therefore, V-line rabbits could produce and lactate efficiently under hot climatic conditions of Saudi Arabia. Lukefahr et al (1983 and 1996) in USA showed that estimates of direct additive effects for milk yield traits were mostly in favour of New Zealand White rabbits compared to Californian rabbits. In crossbreeding experiments carried out in Egypt, Abd El-Aziz et al (2002) found that estimates of direct additive effects for milk production were mostly in favour of New Zealand White relative to Gabali rabbits.

Most estimates of G^M_V-G for milk yields (MY7, MY28 and TMY) and components (protein, fat, lactose, and ash of milk) were in favour of V-line dams (Table 6). Estimates of G^M_V-G were in favour of V-line dams and found to be 222 g and 0.67% and 0.63 % for MY21, total solids in milk and fat of milk, respectively. However, most of the Egyptian findings (Khalil et al 1995; Khalil and Afifi 2000; Abd El-Aziz et al 2002) reported a general trend indicating that does mothered by exotic breeds (e.g. V-line, Californian, Chinchilla, etc.) recorded better performance than does mothered by native breeds (e.g. Baladi and Giza White rabbits). These results do not disagree with the fact that using V-line as a dam breed could produce high performances in lactational performance compared to other dam breeds.

Direct (H^I) and maternal (H^M) heterosis

Estimates of H^I indicated that crossbred does were associated with heterotic effects in milk yields and components (Table 7).

The estimates of H^I in crossbred does, all significant, were obtained in terms of 109, 250, 191, 550 grams in MY7, MY21, MY28, and TMY and 0.97, 0.95, 0.32, 0.13 and 1.91% in fat, protein, lactose, ash and total solids, respectively. The estimates of H^M were, in general, significant, being 150, 187, 127, and 449 grams in milk yield traits and 0.24, 0.89, 0.17, 0.05 and 1.71 % in milk components traits. These results indicate that crossbred does and dams gave favourable heterotic effects on milk yields and components. Lukefahr et al (1996) in USA showed that heterotic effect for milk production was 9.2% in crossing New Zealand White rabbits with Californian. Results of Khalil and Afifi (2000) revealed that crossing Gabali rabbits with NZW was associated with negative low non-significant heterotic effects on milk yields during the first 21 days of suckling and the whole period of lactation. Abd El-Aziz et al (2002) reported that direct heterotic effects on milk production traits were non-significant (0.12 to 2.4 %).

Direct recombination effects (R^I)

Estimates of R^I for all lactation traits (Table 8) were non-significant and indicate that epistatic recombination losses for these traits in crossbred does were negligible.

Moreover, these estimates of R^I were mostly different to estimates of H^I (Table 7). These negligible estimates of R^I indicate that there is a potential advantage to use crossbred does and bucks including V-line genes to develop parental lines (maternal and paternal lines having more available heterosis) to be used in hot climate countries. However, informations in the literature concerning estimates of R^I for lactation traits in rabbits are scarce or not available and consequently no comparison with the present results was attempted. In general, the two-locus model of heterosis reflects dominance effect and half additive-by-additive interaction effects whereas the recombination effect included only half of the additive-by-additive interaction effects (Dickerson 1992).

Conclusions

Moderate heritabilities for lactation traits obtained from rabbits raised in the present study lead to conclude that lactation traits could be practically implemented efficiently (as selection criteria) in selection programs to synthesize new maternal lines of rabbits favourable for hot climate.

The favourable estimates of direct and maternal heterosis for milk production and composition traits obtained from crossing V-line with Saudi Gabali rabbits would be an encouraging factor for the rabbit producers in hot countries to use crossbred does and dams on commercial scale; i.e. crossing V-line with Saudi rabbits was associated with an improvement in milk production along with a reduction in conversion ratio of milk to litter gain.

Non significant recombination effects for most milk yields and components gave an impression to conclude that crossbred does resulting from crossing V-line with native breeds of rabbits in hot climate countries could be effective to develop synthetic maternal lines characterized by high milk production associated with rich components and consequently higher productivity in does could be attained.

Acknowledgments

This project is supported by a great grant (ARP: 18-62) from King Abdulaziz City for Science and Technology in Saudi Arabia. We are appreciated for the efforts of Mr. M. H. Abo El-Fadel for collecting, sampling and editing the data and for Mr. S. El-Khadragy for analyzing chemically the milk samples.

References

Abd El-Aziz M M, Afifi E A, Bedier Nayera Z, Azamel A A and Khalil M H 2002 Genetic evaluation of milk production and litter weight traits in Gabali, New Zealand White rabbits and their crosses in a newly reclaimed area of Egypt. In: Proceedings of the 3^rd Scientific Conference on Rabbit Production in Hot Climates, Hurghada, 8-11 October 2002, 103-116, Egypt.

AOAC 1980 Official Methods of Analysis. 13^th Edition, Association of Official Agricultural Chemists, Washington, D. C., USA.

Ayyat M S, Marai I F M and El-Sayiad G H A 1995 Genetic and non-genetic factors affecting milk production and preweaning litter traits of New Zealand White does under Egyptian conditions. World Rabbit Science, 3: 119-124.

Baselga M 2004 Genetic improvement of meat rabbits: Programmes and diffusion. In: Proceedings of the 8^th World Rabbit Congress, 7-10 September 2004, Puebla, Mexico, pp 1-13.

Boldman K G, Kriese L A, Van Tassell C P and Kachman S D 1995 A manual for use of MTDFREML. A set programs to obtain estimates of variances and covariance [DRAFT]. U.S. Department of Agriculture, Agricultural Research Service, USA.

Capra G, Blumetto O and Elizalde E 2000 Meat rabbit production in Uruguay. In: Proceedings of the 7th World Rabbit Congress, Valencia, Spain, 4-7 July 2000, Volume B: 51-58.

Case R A, Bradley R L and Williams R R 1985 Chemical and physical methods. In: Standard Methods for the Examination of Dairy Products. Richardson G H, Editor, 15^th Edition, American Public Health Association, Washington, D. C., USA, pp.327-402.

Cowie A T 1969 Variations in the yield and composition of the milk during lactation in the rabbit and the galactopoietic effect of prolactin. Endocrinology 44:28.

Dickerson G E 1992 Manual for evaluation of breeds and crosses of domestic animals, Food and Agriculture Organization of the United Nations, Rome, PP 47.

El-Maghawry A M, Soliman A M and Khalil M H 1993 Doe milk production as affected by some genetic and environmental factors in New Zealand White and Californian rabbits under Egyptian conditions. Egyptian Journal Rabbit Science 3: 141-150.

El-Sayiad Gh A, Habeeb A A M and El-Maghawry A M 1994 A note on the effects of breed, stage of lactation and pregnancy status on milk composition of rabbits. Animal Production 58:153-157.

Estany J, Baselga M, Blasco A and Camacho J 1989 Mixed model methodology for estimation of genetic response to selection in litter size in rabbits. Livestock Production Science 21: 67-75.

Garcia M L, Blumetto O, Capra G, Vicente J S and Baselga M 2000 Vitrified embryo of two selected Spanish rabbit lines to Uruguay. In: Proceedings of the 7th World Rabbit Congress, Valencia, Spain, 4-7 July 2000, World Rabbit Science, 8 Supp. 1: 139-142.

Garreau H and Rochambeau H de 2003 La sélection des qualités maternelles pour la croissance du lapereau. In: 10^èmes Journées de la Recherche Cunicole, Paris, 19-20 Novembre 2003: 61-64.

Garreau H, Piles M, Larzul C, Baselga M and Rochambeau H de 2004 Selection of maternal lines: Last results and prospects. In: Proceedings of the 8^th World Rabbit Congress, 7-10 September 2004, Puebla, Mexico, pp 14-25.

Gomez E A, Rafel O, Ramon J and Baselga M 1996 A genetic study of a line selected on litter size at weaning. In: Proceedings of the 6^th World Rabbit Congress, Toulouse, France, 9-12 July 1996, 2: 289-292.

Gomez E A, Rafel O and Ramon J 2000 Preliminary genetic analysis of Caldes line: A selection experiment for a global objective. In: Proceedings of the 7^th World Rabbit Congress, Valencia, Spain, Volume A: 417-423.

Khalil M H 1994 Lactational performance of Giza White rabbits and its relation with pre-weaning litter traits. Animal Production, 59: 141-145.

Khalil M H and Afifi E A 2000 Heterosis, maternal and direct additive effects for litter performance and post-weaning growth in Gabali rabbits and their F₁ crosses with New Zealand White. In: Proceedings of the 7th World Rabbit Congress, Valencia, Spain, 4-7 July 2000, Volume A: 431-437.

Khalil M H, Afifi E A, Youssef Y M K and Khadr A F 1995 Heterosis, maternal and direct genetic effects for litter performance and reproductive intervals in rabbit crosses. World Rabbit Science, 3(3):99-105.

Khalil M H, Garcia M L, Al-Dobaib S N, AL-Homidan A H and Baselga M 2005 Genetic evaluation of pre-weaning litter traits and feed conversion in crossbreeding project involving Saudi rabbits and spanish V-line. 4^th International Conference of Rabbit Production in Hot Climate, 24-27 February, Egypt.

Lahari S S and Mahajan J M 1984 Milk yield and mothering ability in rabbits. Indian Journal of Animal Science 54(1): 137-138.

Lukefahr S, Hohenboken W D, Cheeke P R and Patton N M 1983 Characterization of straightbred and crossbred rabbits for milk production and associative traits. Journal of Animal Science, 57(5):1100- 1107.

Lukefahr S D, Cheeke P R and Patton N M 1996 Heritability of milk production and 21-day litter weight and litter size in purebred and crossbred rabbits using an animal model. In: Proceedings of the 6^th World Rabbit Congress, Toulouse, France, 9-12 July 1996, 2: 319-324.

Moura A S A M T, Costa A R C and Polastre R 2001 Variance components and response to selection for reproductive, litter and growth traits through a multi-purpose index. World Rabbit Science, 9: 77-86.

Rochambeau H de, Duzert R and Tudela F 1998 Long term selection experiments in rabbit. Estimation of genetic progress on litter size at weaning. In: Proceedings of the 6^th World Congress on Genetics Applied to livestock Production, Armidale, NSW, Australia, 11-16 January 1998, Volume, 26: 112-115.

Salaun J M, Garreau H, Thebault R G, Allain D and Rochambeau H de 2001 Selection pour le poids total de lapereaux par femelle et par an dans une souche de lapins Castor Rex. In: 9è^mes Journées de la Recherche Cunicole, Paris, 28-29 Novembre 2001: 221-224.