Offspring sex proportion and lamb competition during gestation and lactation in prolific Pelibuey lambs under intensive management

R Macedo, V Arredondo*, E Cásarez, A E Esperón** and J D Hummel

FMVZ-University of Colima. Km. 40 Autopista Colima - Manzanillo, Tecomán, Colima, México. 28100
macedo@ucol.mx
* Private Consultant. Benito Juárez 220. Tecomán, Colima, México. 28930
** FES Cuautitlán - UNAM. Km. 2.5 Carretera Cuautitlán - Teoloyucan, Cuautitlán Izcalli, Estado de México, México. 54700

Summary

Two studies were conducted in Colima, Mexico with the objective to 1) evaluate the influence of type of birth, season of mating, ewe age at mating and sire on birth sex proportion and 2) evaluate the effect of lamb sexual competition during pregnancy and lactation through birth and weaning weight of prolific Pelibuey lambs. A Chi-square test was applied to evaluate 959 lamb records to observe offspring birth sex proportion. Analysis of Variance (ANOVA) for unbalanced data with a Completely Randomized Design tested 513 birth and 492 weaning weight records to evaluate sex competition during gestation and lactation.

In study 1, sex proportion was related (c²>P) with sire (4.85>0.56) and ewe age at mating (1.36>0.85), whereas no relationship was found (c²<P) between sex proportion, type of birth (0.81<0.85) and mating season (0.77<0.86). The overall sex proportion was 50.9% female lambs and 49.1% male. Two sires produced significantly more females (62.9and 59.1%). As the ewe aged, the tendency of sex proportion favoured the males in the first year; changing to female for three years, and returning to produce more males. In study 2, no evidence of sexual competition during gestation and lactation was found. Similar birth weights (P>0.05) were found in female lambs which shared pregnancy with 1 and 2 females (17.2 ± 3.00 and 15.3 ± 3.45 respectively) and those that shared gestation with 1 and 2 males (17.6 ± 3.20 and 16.2 ± 3.79 respectively), with the same tendency to pre-weaning growth rate and weaning weight of female and male lambs.

Results suggest an association between sire, ewe age at mating and offspring sex proportion of prolific Pelibuey lambs, in addition to no evidence of competition between male and female lambs were observed during gestation and lactation.

Keywords: birth weight, ewe age, hair sheep, sex, type of birth, weaning weight

Proporción de sexos y competencia durante la gestación y lactancia de corderos Pelibuey prolíficos bajo manejo intensivo

Resumen

Se realizaron dos estudios en un hato de ovinos Pelibuey prolíficos en Colima, México con el objetivo de 1) evaluar la influencia del tipo de parto, la época de empadre la edad de la oveja al empadre y el del semental sobre la proporción de sexos de la camada y 2) evaluar el efecto de la competencia entre corderos de distinto sexo durante la gestación y la lactancia a través del peso al nacimiento y el peso al destete. La proporción de sexos en la camada se evaluó analizando 959 registros individuales por medio de una prueba de Chi-cuadrada, mientras que la competencia sexual durante la gestación y la lactancia, fue medida a través de 513 pesos al nacimiento y 492 pesos al destete analizados por medio de un Análisis de Varianza para datos desbalanceados con un Diseño Completamente al Azar.

En el estudio 1, la proporción de sexos al nacimiento estuvo relacionada (c²>P) con el semental (4.85>0.56) y la edad de la oveja al empadre (1.36>0.85), mientras que no se observó relación (c²<P) con el tipo de parto (0.81<0.85) y la época de empadre (0.77<0.86). La proporción total de sexos fue 50.9% hembras y 49.1% machos. Dos sementales produjeron una proporción de hembras significativamente mayor (62.9 y 59.1%). Conforme se incrementó la edad de la oveja al empadre la proporción de hembras nacidas tendió a crecer manteniéndose así durante algunos años para posteriormente crecer la proporción de machos.

En el estudio 2, no se observó evidencia de competencia sexual durante la gestación y la lactancia entre corderos de distinto sexo. El peso al nacimiento de las hembras que compartieron gestación con 1 y 2 hembras (17.2 ± 3.00 y 15.3 ± 3.45 respectivamente) fue similar (P>0.05) al de aquellas que compartieron gestación con 1 y 2 machos (17.6 ± 3.20 y 16.2 ± 3.79 respectivamente). La misma tendencia fue observada para el peso al destete y la tasa de crecimiento predestete.

Los resultados sugieren que la proporción de sexos al nacimiento de corderos Pelibuey prolíficos bajo manejo intensivo se encuentra asociado con el semental y la edad de la oveja al empadre, mientras que no se observó evidencia de competencia sexual entre corderos de diferente sexo durante la gestación y la lactancia.

Palabras clave: edad de la oveja, ovinos de pelo, peso al destete, peso al nacimiento, sexo, tipo de parto

Introduction

Mammals usually produce approximately equal numbers of male and females siblings, but there are exceptions to this general rule, as has been observed in ruminant ungulate species, where the sex-allocation hypothesis of Trivers and Willard (1973) has provided a proportional evolutionary underpinning to adaptive changes in sex proportion.

Some studies found that in feral sheep (Ovis canadensis), density population, weather and ewe age did not affect offspring sex, whereas the lamb sex did affect the sex of the mother’s subsequent lamb (Bérubé et al 1996). Other analyses carried out in domestic sheep (Ovis aries) found that the litter size, the flock age, the lambing season (Kent 1992, Kent 1995), the breed, the nutritional level of the flock, the number of lambs weaned in the previous year (Skjervold 1979) and the time of insemination according to time of ovulation (Gutiérrez-Adán et al 1999, Rorie 1999) caused significant differences in the sex proportion of lambs. Contrarily, Lindström et al (2002), demonstrated that population growth rate, litter size, mother's age and weight, and the weather conditions during the gestation and neonatal period did not explain significant variation in the birth sex ratio.

Sex is one of the factors that affect the birth weights and the pre-weaning growth of lambs. The development of differences in birth weights of male and female lambs start during pregnancy. Although both male and female foetuses had the same number of cotyledons Rhind et al (1980) reported that the weight of cotyledons associated with male foetuses was 10.5% heavier than those associated with female foetuses. The birth weight of a female lamb that shares gestation with a male lamb is lighter than the average birth weight of two female lambs which share gestation. In contrast, the birth weight of a male lamb that shares gestation with a female lamb is heavier than the average of two male lambs which share gestation (Daza 1997).

Manipulation of maternal skewing of offspring sex proportion might have important agricultural implications as offspring of one gender might be preferred. For instance females are preferred in the dairy and breeding industries, whereas males are favoured in the mouton industry. Improving growth of female lambs, diminishing the effect of male competition from gestation up to weaning has economical advantages on sheep industry, reducing the time at first mating and at first birth of ewe lambs with the consequents savings in cost of maintenance.  

The effect of both, sex proportion and lamb competition has been widely studied in feral and wool breeds, though not in hair sheep. The aims of this study were to evaluate the influence of type of birth, season of mating, sire and ewe age at mating on birth sex proportion and to evaluate the effect of competition between foetuses during pregnancy and lactation in prolific Pelibuey lambs.       

Materials and methods

Area description 

The study was conducted on a Pelibuey purebred flock bred at the Agriculture and Forestry Training Center (CECAF) located in Tecomán, Colima, México, at 18°58'43'' north latitude, 103°52'18'' west longitude and 73 masl. Koppen´s climate classification is BS₁(h')w(w)(i') described as semiarid with 750 mm of mean annual rainfall, with a predominantly summer incidence. The dry season extends for seven months from November to May with a mean annual temperature of 26 °C.

Animals and management

The ewes were grazed in an agro forestry system which included Mexican lime trees (Citrus aurantifolia) and tropical grasses such as Star grass (Cynodon plectostachyus), Guinea grass (Panicum maximum) and other native grasses (eg. Paspalum sp. and Axonopus sp.). The ewes were supplemented with a concentrate containing 2.80 Mcal ME/kg DM, 18.8% CP. The concentrate contained cracked corn (59.0%), wheat bran (14.0%), commercial pelleted proteic meal (8.70%), sugarcane molasses (7.00%), coconut meal (4.40%), canola meal (2.00%), calcium carbonate (2.20%), ammonia (1.35%), sodium chloride (0.95%) and mineral premix (0.40%). The concentrate was fed at the following rates: 1.5 kg/day at mating (flushing) and early pregnancy (35 days), 150 g/day at intermediate pregnancy (75 days), 250 g/day at late pregnancy (40 days) 2.0 kg/day at early lactation (30 days) and 550 g/day at late lactation (60 days).

Ewes were mated in a controlled system with one male serving 20 ewes every 35 days. Ewe lambs were mated when they reached 70% of their mature body weight whereas for multiparous ewes it was at the time of weaning (80 days after lambing). The average body condition of the ewes was 2.4 and 3.0 -using the 5-point scale described by Russel et al (1969)- at the beginning and at the completion of mating, respectively. Body condition at lambing was 3.5.

Seven days before mating, ewes were dewormed with albendazole (10 mg/kg LW) and twenty days before lambing, they were vaccinated against enterotoxaemia and pneumonia with a live tissue culture vaccine.

Lambs were creep fed after they reached seven days of age up to weaning with a pelleted feed containing 17% CP, 3% fat and 2.5% CF. The average amount, of creep feed consumed by the lambs, was estimated to be 100 g/day. Average age of lambs at weaning was 83 days. The lambs were weighed at birth and weaning. Pre-weaning growth rates were calculated by taking the difference within the period from birth to weaning and dividing it by the time interval in days. Lamb weight at weaning was adjusted to 80 days of age.

Statistical analyses

Nine hundred and fifty-nine lamb records using Chi-square test with the statistical package SPSS (1997) were used to analyse the offspring birth sex proportion. Data analysis included the effect of type of  birth (single, twin, triplet, quadruplet), mating season (spring, summer, autumn, winter), sire (1,2,3,4,5,6,7) and ewe age at mating (<12 months, 12-24 months, 24-36 months, 36-48 months, >48 months).

The competition, between the foetuses during gestation and lambs during lactation of different sexes, was measured comparing the birth and weaning weight as well as pre-weaning growth rate. The means of 513 birth and 492 weaning weights and the pre-weaning growth rate records were compared using Analysis of Variance (ANOVA) for unbalanced data with a Completely Randomized Design including the effect of general mean, treatment and experimental error. The difference between means was compared using the Tukey test. Statistical significance was accepted at the 5% level. Nineteen experimental treatments were compared using the combinations of type of birth (single, twin, triplet, quadruplet) and sex (female, male), as shown in Table 1.

Results and discussion

Offspring sex proportion

The type of birth did not have an affect on sex proportion as single, twin, triplet or quadruplet litters contained similar number of males and females. Sex proportion was independent of the season of mating. Ewes were likely to produce more males when conception took place in autumn. There was a slight trend for ewes to produce more males if they are mated younger than 12 months and older than 48 months. Ewes mated at intermediate age produce more females. Sex proportion was strongly associated with sire. Ewes mated to sires 3, 1 and 5 produced a significantly female-biased offspring (12.0%, 8.20% and 4.11% more females than the flock average respectively), while only the ewes mated to sires 2 and 4 produced more males than females (Table 2).

The results obtained in this study suggest that the type of birth has no influence on the sex proportion of the progeny of Pelibuey sheep. Male-female proportion from single, twin, triplet and quadruplet litters hardly varied (3.23%). However, lamb sex proportion may have varied in others breeds, as has been suggested for Suffolk sheep (Kent 1995) in which, ewes with single lambs produced significantly more males (53.0%) than ewes with triplets (45.5% male).

Different approaches could be adapted to explain the effect of the mating season on sex proportion in feral and extensive production system. A first hypothesis could be related to seasonality changes in both food availability and quality with variation in maternal diet and hence, with maternal body condition. Empirical results, however, are inconsistent within sheep breeds and species. Some authors concluded that high quality mothers (ewes with better body condition and body mass) should produce more sons, while low quality mothers (ewes with poor body condition and body mass) should produce more daughters (Clutton-Brock et al 1984; Kent 1995). Contrary, authors found that ewes were not significantly more likely to conceive sons in years when they were heavy (48% mean proportion of males) than in years when they were lighter (45%) than their average adult mass, concluded that sex proportion was independent of ewe body condition (Blanchard et al 2005).  

“Differential maternal investment” theory related changes in population density with changes in food availability with the different cost that ewes incurred in raising a son or a daughter. This theory assumes that ewes provide more maternal care to sons than to daughters and predict that mother nursing sons incur greater reproductive cost than ewes that raise a daughter. Although ewe mass gain during lactation and subsequent winter body mass lost were independent of lamb sex. The year after weaning a son, ewes were more likely to have a daughter than a son. A high population density accentuates the great cost to raise a son and ewes were unable to recover from this investment following the weaning of the male lamb. This higher cost of sons was also associated with a low probability of producing male lambs in consecutive years as well as altering the sex of lambs produced could be an adaptive strategy for ewes to avoid sustaining the high cost of sons in consecutive years (Festa-Bianchet 1989, Bérubé et al 1996).  

Rosenfeld and Roberts (2004) indicate that other mechanisms that favour one sex over the other can operate after fertilization has occurred. Differences in the rate of development or in the sensitivity to conditions of XX versus XY embryos within the female reproductive tract cause a selective loss of embryos of one sex prior to placentation. Such selection might be favoured by particular nutritional components or developmental asynchrony between the embryos and uterus. Selective fetal resorption/abortion is the final possible means of skewing offspring sex proportion. Kohlmann (1999) found that male embryos have higher mortality than female when carried by a female in poor condition.

A last approach to explain the effect of mating season on offspring sex proportion is the association of this variable with the prevailing climate around the time of conception. Studies in dairy cattle showed that a male calf was more likely to be born following periods of elevated air temperature, greater evaporation or both. A 1°C increase in average maximum air temperature from the average (18.3°C), during the week immediately prior to conception, was associated with a 1-percentage unit increase in the probability of a male calf being born (from 52 to 53%). A corresponding 1°C increase in average minimum air temperature was reflected in a 0.5-percentage unit increase in the probability of a male calf being born. The probability of a male calf being born increased by 2.9 percentage units with each additional millimetre of evaporation per day (Roche et al 2006).

The relationship of ewe age at mating and birth sex proportion, which in this study favoured the males in the first year; changing to female for three years, and returning to produce more males, was inverse to that reported by Kent (1995) in Suffolk sheep.

Results of his study confirm that spermatozoa are the main source of variation and determination of genetic sex. Several hypotheses, none of which have been rigorously tested, have been proposed to explain skewing of sex proportion in mammals. The timing of insemination has long been held to affect sex proportion in species that ovulate spontaneously, particularly in livestock (Clutton-Brock and Iason 1986). Sperm of one sex might be more capable in effecting fertilization once the egg has been reached, depending on factors such as the condition of the female reproductive tract and the penetrability of the zona pellucida, which likely vary according to the time of ovulation relative to time of insemination. Depending on maturational state at the time of fertilization, the oocyte might preferentially bind X or Y bearing sperm. Significant differences in the sex proportion were obtained when Gutiérrez-Adán et al (1999) compared the sex of the offspring of ewes inseminated during the 5 h preceding ovulation (more females) with those inseminated during the 5 h after ovulation (more males). Rorie (1999) confirmed that early insemination skews the sex proportion toward females, while late insemination favours males.

Likewise, sperm of one sex might have differential motility or make their way more directly to the oocyte than the other depending on the conditions prevailing in the reproductive tract of the impregnate female, e.g. state of the cervical mucus, vaginal pH relative to the precise time at which copulation occurred in relation to the estrus. One class of sperm might have intrinsic physiological differences in viability, capacitation, or the dynamics of the acrosome reaction (Madrid-Bury et al 2003).

Lamb competition

Type of birth affects birth weight, weaning weight and pre-weaning growth rate, whereas the sex of the lambs did not influence these variables. In spite of sex, no differences in growth were found within lambs that were born in twin (T3, T4, T5, T6), triplet (T7, T8, T9, T10, T11, T12) and quadruplet litters (T13, T14, T15, T16, T17, T18, T19).

No evidence of competition during gestation and lactation was found between male and female lambs within a litter. Birth and weaning weight of female lambs that shared gestation and lactation (T3) were similar to those that shared gestation and lactation with a male lamb (T4). The same trend was observed in triplet female lambs that shared gestation and lactation with two male lambs (T9) compared with those that shared pregnancy and lactation with two female lambs (T7), as well as quadruplet female lambs that shared gestation and lactation with three female lambs (T13) and with three male lambs (T16).

In the case of males, those that shared gestation and lactation with a female lamb (T6) were not heavier at birth or at weaning than those that shared gestation and lactation with another male lamb (T5). Males from triplet litters that shared gestation and lactation with two males (T10) and those that shared with two female lambs (T12) showed similar birth weights, weaning weights and pre-weaning growth rates (Table 3).

The uniformity of birth weight between male and female lambs which share pregnancy with lambs of different gender could be explained by the high level of supplementation offered to the ewe during gestation. That suggests that in spite of competition, a greater amount of nutrients were available to enhance growth especially during late gestation in which 70% of the total foetal growth takes place (Russel 1982). Evidence of foetal competition, reported by Daza (1997) and McLaren (1980), was observed in ewes under grazing production systems with significantly less supplementation.

Although some authors hypothesize that early development of gonads and testosterone production are the main factors which promote superior growth of the male fetus (Boris et al 1970; Alexander 1974), no differences on birth weight were observed between male and female lambs within the same type of birth. Overall superiority of male performance was recorded previously in this flock by Macedo y Arredondo (2006).   

No evidence of female lamb disadvantage during lactation could be explained due to an ample supply of concentrate to enhance milk production and the access to creep feeding starting the first week of life which increases until 2 weeks before weaning when the lamb is consuming 250 g. Another explanation, “the advantage daughter hypothesis” predicts that ewes that are able to provide a high level of care, invest more maternal care in daughters rather than sons which affects more the fitness of daughters (Hewison and Gaillard 1999).  Furthermore, interactive behaviour and spatial relationships observed in mouflon lambs during weeks 2 - 6 of lactation with their mothers and peers showed that female lambs often avoided interactions with other lambs and tended to stay close to their respective mothers, while male lambs interacted more with peers and were more often at some distance from their mothers. This suggest that female lambs had more opportunities to suckle in spite of male competition (Guilhem et al 2006)

Hogg et al (1992) indicated that sons in Rocky Mountain bighorn sheep obtained a larger maternal subsidy, weighed more at birth (an index of relative prenatal expenditure) and tended to suckle more between 40 and 100 days of age (an index of relative postnatal expenditure). Obregón et al (1992) explained that during the first week of a lamb’s life, mothers ended 38.6% of the attempts to suck when the lamb was a male and 75.0% of them of female lambs.

Whereas sons did not appear to receive more milk than daughters (Festa-Bianchet 1988), in big horn sheep the duration of lactation is more important for sons than for daughters: male lambs orphaned before weaning had smaller adult body size compared to non-orphan males, while no difference was found between orphan and non-orphan females (Festa-Bianchet et al 1994). 

Conclusions

• Results suggest that under intensive productive conditions sire and ewe age at mating affect birth sex proportion of prolific Pelibuey lambs with no effect of type of birth and season of mating.

  
  

• No evidence of competition, between male and female lambs measured through birth and weaning weight, was observed during gestation and lactation.

Acknowledgments

Authors are very grateful to CECAF, A. C. for supporting this study. Project “Efecto del sexo y del tipo de parto sobre la productividad de un hato de ovinos Pelibuey prolíficos bajo condiciones intensivas en el trópico”. PROMEP 173371 81516 0.

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Received 25 June 2007; Accepted 6 October 2007; Published 12 December 2007

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