Placental development in a bovine heterosis model

Abstract

Heterosis or hybrid vigor is a biological phenomenon referring to the phenotypic superiority of hybrids over their parents. Despite its economic importance, the mechanisms of heterosis are still poorly understood. Reciprocal cross Brahman (B) × Angus (A) calves display significant heterosis in birth weight, but this effect is almost entirely due to the dramatic fetal overgrowth observed in Brahman male × Angus female offspring. The reciprocal is much less affected and similar to purebred Brahman calves (Brown et al. 1993 J. Anim. Sci. 71, 3273–3279). We have generated a defined A × A (n = 20), B × A (n = 21), A × B (n = 13), and B × B (n = 15; male parent listed first) day 153 (term = 280) fetal/placental resource from artificially inseminated, estrous cycle synchronized heifers to identify components and mechanisms of heterotic fetal growth regulation. An ANOVA showed that full uterus weight (P < 0.001), fetal weight (P = 0.01), umbilical cord length (P = 0.003) and weight (P = 0.04), placenta fetalis weight (P < 0.001), total caruncle weight (P = 0.002), empty uterus weight (P < 0.001), and combined amniotic/allantoic fluid weight (P < 0.001) were significantly affected by the 4 genetic groups after adjustment for fetal sex and dam weight where required. The weight of reciprocal hybrid fetuses was intermediate to the purebred fetuses and thus did not display heterosis defined as the difference between reciprocal cross and parental means. Full uterus weight and combined amniotic/allantoic fluid weight, in contrast, displayed heterosis of 6.6% (P = 0.02) and 9.0% (P = 0.01). As in neonate calves, the heterosis effects were due to the B × A group. The t-tests demonstrated that full uterus weight in B × A was significantly greater (19.84 ± 0.43 kg) than in A × B (16.23 ± 0.47 kg; P < 0.001), A × A (17.41 ± 0.35 kg; P < 0.001), and B × B (16.76 ± 0.49 kg; P = 0.001) crosses. Combined amniotic/allantoic fluids were 12.58 ± 0.31 kg in B × A as compared to 10.93 ± 0.39 kg in A × B (P = 0.001), 10.75 ± 0.29 kg in A × A (P < 0.001), and 11.48 ± 0.36 kg in B × B (P = 0.02) crosses. We found similar superiority of the B × A group for parameters that did not fulfil the formal heterosis criterion. These include umbilical cord, placenta fetalis, empty uterus, and total caruncle weights. All but 1 of these (combined amniotic/allantoic fluid weight) were significantly correlated (r = 0.43–0.70; P < 0.001) with fetal weight. We conclude that massive changes in placental parameters underly and precede the heterosis effects in birth weight observed in Brahman × Angus crosses. Although formally designated heterosis, placental and fetal overgrowth is present in only 1 of the hybrids (B × A). This natural overgrowth phenotype is clearly distinct from the early onset overgrowth phenotypes observed after IVF and nuclear transfer cloning (Hiendleder et al. 2004 Biol. Reprod. 71, 217–223) and will be useful in the dissection of factors contributing to fetal growth and development.