THE INHERITANCE OF FUSED EARS IN AN ALPACA FAMILY
G.H. Davis’, KG. Dodd&, S.M. Galloway* and G.D. Bruce’
‘AgResearch, Invermay Agricultural Research Centre, Private Bag, Mosgiel, New Zealand
‘AgResearch Molecular Biology Unit, Biochemistry Department, University of Otago, P.O. Box 56, Dunedin, New Zealand
SUMMARY
A condition where the tips of the ears are deformed, resulting in short ears, has been observed in a female alpaca imported to New Zealand from Chile and in some of her descendants. Records from 19 descendants suggest that this defect is passed from mother to all daughters, but is not expressed in males and is not passed from sires to daughters. The inheritance pattern is consistent with a sex-limited trait. The data are most consistent, in order of probability, with the following modes of inheritance: mitochondrial DNA, maternal imprinting, or a dominant autosomal gene.
Keywords: Alpaca, major gene, ears INTRODUCTION
Normal ears in huacaya alpacas (Lumupucos) are spear-shaped, curved on both borders and have a sharp tip. Congenital malformations of the ears in alpacas and llamas (Luma glumu) have been observed and are variously described as gopher ears, fused ears, curled ears, folded ears or short ears (Fowler 1996). Ear defects in camelids are rare, and it has been suggested that there is a genetic basis to this condition (Leipold et al. 1994). Frostbite, usually in neonates, has also been observed as a cause of shortened ears in camelids (Fowler 1989). The Australian International Alpaca Register and American Alpaca Regisv both list short ears as a defect precluding registration, although according to Fowler (1996) hearing is seldom impaired in affected animals.
This study investigates whether a congenital ear defect is inherited.
MATERIALS AND METHODS
In 1989, 86 female and 14 male huacaya alpacas were imported from Chile to study their production in the high country of the South Island of New Zealand at the AgResearch, Tara Hills High Country Research Station near Omarama and on a nearby commercial property. The animals were sourced from 13 villages located in the Chilean altiplano, and although the village of origin for each alpaca was known, no pedigree information was available. Pedigrees of alpacas conceived in New Zealand were recorded. In December 1994 and March 1995 two female crias were born with short ears and, because of the commercial implications of this defect, an examination of the ears in all alpacas in the flock was carried out. Between March 1995 and July 1996, ears were examined in 37 females and 11 males remaining from the original importation, plus 125 female descendants and 88 male descendants born in New Zealand.
Proc. Assoc. Advmt. Anim. Breed. Genet. Voll2 RESULTS AND DISCUSSION
In the fast two crias observed to have short ears, the tip of each ear was deformed with margins of the terminal 3-4 cm of the ears thickened and fused. In one cria the tips resembled a human ear lobe; in the other cria the thickened tips were fused to form a pouch. The deformed ears were also characterised by the presence of an extensive growth of long coarse fibres protruding from the ears. There was no evidence of impaired hearing in either animal.
Close examination of other alpacas in the flock identified two adult females with the same defect.
As in the previous cases, the ears were shortened with pronounced thickening at the tips. In both adults there was a thickened cartilaginous growth extending beyond the ‘normal’ pointed tip of the ear, but the combined length of the ear plus cartilaginous tip was 3-5 cm shorter than normal ears.
One of the females with the defect had been imported from Chile and was the ancestor of the other three affected females. In 1996, this female (the founder) had another daughter with the defect, bringing the incidence in females to 4% (5/125). In all cases both ears were deformed. None of the 99 males inspected~was affected. Figure 1 shows the founder female and her descendants.
0 =fmale
q =male . = deformed ears
. = deceased (ear type unknown)
Figure 1. Inheritance of fused ears in an alpaca family.
All living daughters and maternal line granddaughters of the founder female had deformed ears (Figure 1) and were all sired by different unrelated males. Her three sons and all other male descendants were normal. All female progeny of her sons and grandsons were also normal.
Several single locus inheritance models were tested using an odds ratio analysis (Table 1).
As all cases of the ear defect occurred in one family it appears to be genetically controlled and there could be one or a few genes responsible. One daughter of the founder female had died before the study. However, based on the incidence of the defect in all other female-line
descendants of the founder female, including a daughter of the deceased female, it is probable that her ears were deformed. The deformed ears were less conspicuous in the two adults, partly because of longer fibres growing from adult ears. For this reason the fact that the deceased female’s ears had not been recorded as deformed may simply reflect the fact that they were never closely examined.
Table 1. Odds ratio analysis comparing mitochondrial sex-limited inheritance of a putative gene (F’) for defective ears in alpacas to other inheritance models
Case Founder Model* L%l&
tl Odds”
1
genotype FF
2 F+
3 FF
4 F+
5 FF
6 F+
7 F+
8 FF
9 F+
RA -8.64 4x10”
DA -3.34 2188
RSA -8.30 2x10s
DSA -1.82 66
DSA -1.34 22
DSX -2.08 120
IA -3.36 2287
ISA -0.62 4
ISA -1.52 33
10 F SM 0 1
*D = dominant; R = recessive; I = maternal imprinting; S = sex-limited; A = autosomal; X = X- linked; M = mitochondrial.
BLog,, of the likelihood calculated over the whole family, conditional on model and genotype of founder female, and assuming that the frequency of the F allele in the population is 0.01. The allele frequency has little effect on the likelihoods except for the recessive models.
‘Odds ratio of case 10 compared to current case.
Because the five affected females have different sires, all with normal ears, it is most unlikely that this defect has been inherited from the males. The absence of other unrelated affected animals suggests that the gene frequency in this flock was very low. Therefore, the defect is most unlikely to be due to a recessive gene because the affected females had different unrelated sires and these would all have to carry the gene. The fact that no males in this family had the defect strongly suggests that the condition is sex-limited.
The defect is possibly inherited cytoplasmically in association with mitochondrial DNA which is transmitted to all progeny by females, but not by males. Our data are entirely consistent with the sex-limited mitochondrial inheritance model. However, reported cases of traits affected by mitochondrial genes are rare, although there is some evidence in milk production traits in cattle (Huizinga et al., 1986; Tess et al., 1987). Although a sex-limited mitochondrial DNA pattern of inheritance may be justified statistically, we have no physiological explanation for this phenomenon.
Proc. Assoc. Advmt. Anim. Breed. Genet. Vol12
Another possible mode of inheritance is maternal imprinting, but there are few cases where segregation could be observed. Our data are 4 - 33 times less likely under sex-limited maternal imprinting than sex-limited mitochondrial inheritance (Table 1).
If the defect was due to a dominant sex-limited gene on an autosome, the founder female could be either heterozygous or homozygous. If she was heterozygous, half her offspring would carry the gene but it would be expressed only in females. At the next generation, half the female progeny of affected females and half the female progeny of male carriers would be affected - half the male progeny of both groups would be carriers. Although the data in Fig 1 are consistent with this hypothesis, they are unlikely as there are no normal females in the female-line descendants and no evidence of normal male descendants producing affected female offspring.
If the founder was homozygous for a dominant sex-limited autosomal gene, all daughters would be affected and all sons would be carriers. The gene would segregate at the next generation as described in the previous paragraph. Fig 1 shows that both female-line granddaughters were affected and both male-line granddaughters were normal. This is consistent with the expected 50% (2/4) of the second generation females being affected, but there would need to be some normal second generation females in the female-line, and some affected second generation females in the male-line to confirm this mode of inheritance. The probability of the founder being homozygous is unknown because we have no data on the frequency of the defect in the village of origin in Chile.
Although the defect has appeared only in females, it seems unlikely that the inheritance is X- linked. If it was a dominant sex-limited X-linked gene, half the daughters of a carrier female would be affected. Our data would be unlikely under this hypothesis. Furthermore, a sex-limited X-linked gene would result in half the daughters of a carrier female expressing the gene (in this family all daughters of affected females carried the gene), and all daughters of a carrier male expressing the gene (daughters from both male descendants of the founder female were all normal).
Short malformed ears in cattle due to inherited defects described as ‘notched ears’ (MacDonald 1957) and ‘crop ears’ (Scheider et al. 1994) are believed to be inherited by single autosomal genes with incomplete dominance. McDonald’s (1957) description of affected cattle as exhibiting
‘coarse hair, heavy cartilaginous tips, and ribbing, and a slab-like appearance due to a reduction in development of both anterior and posterior margins of each ear as the tip was approached’ could also describe the defect observed in this alpaca family. An autosomal gene with incomplete dominance causing shortened ears has also been observed in dogs (Lauvergne et al. 1987) and goats (Schumann 1956). Further progeny records are needed to define the mode of inheritance of this ear defect in alpacas.
REFERENCBS
Fowler, M.E. (1989) “Medicine and Surgery of South American Camelids”. Iowa State University Press, Ames.
Fowler, M.E. (1996) Lfumus 10 (3): 9.
Huizbga, W.A., Kwm, S., McDaniel, B.T. and Polite&, R.D. (19$6) Lb&#, Prod Sci. 15 (1); 11.
Lauvergne, J.J., Renieri, C. and Audiot, A. (1987) J. Hcz~d. 78: 307.
Leipold, H.W., Hiraga, T. and Johnson, L.W. (1994) Vet CZinics ofNorth America 10 (2): 401.
McDonald, MA. (1957) J.H&ed 48: 244.
Scheider, A., Schmidt, P. and Distl, 0. (1994) &l. Munch. Tierard Es&r. 107: 348.
Schumann, H. (1956) &erl. A4mch Tierurztl. Wkchr. 69: 252.
Tess, M,W., Remie&,.C. and Robisoa, O.W. (1987) J, dnim. Sci. 65: 675.
