Routine Karyotyping Reveals Frequent Mosaic Reciprocal Chromosome Translocations in Swine: Prevalence, Pedigree, and Litter Size

Abstract

In the routine commercial karyotype analysis on 5,481 boars, we identified 32 carriers of mosaic reciprocal translocations, half of which were carrying a specific recurrent translocation, mos t(7;9). An additional 7 mosaic translocations were identified through lymphocyte karyotype analysis from parents and relatives of mosaic carriers (n = 45), a control group of non-carrier boars (n = 73), and a mitogen assessment study (n = 20), bringing the total number of mosaic carriers to 39 cases. Mosaic translocations in all carriers were recognized to be confined to hematopoietic cells as no translocations were identified in fibroblasts cells of the carriers. In addition, negative impact on reproduction was not observed as the fertility of the carriers and their relatives were comparable to breed averages, and cryptic mosaicism was not detected in the family tree. This paper presents the first study of mosaic reciprocal translocations identified in swine through routine screening practices on reproductively unproven breeding boars while presenting evidence that these type of chromosome abnormalities are not associated with any affected phenotype on the carrier animals. In addition, the detection of recurrent mosaic translocations in this study may emphasize the non-random nature of mosaic rearrangements in swine and the potential role of genomic elements in their formation. Chromosome translocations in a mosaic state are rarely reported in domestic animal species. To date, over 200 constitutional chromosome rearrangements have been reported in the domestic pig 1 , while only four mosaic abnormalities are previously documented for this species 2,3. The discrepancy in reports is mainly due to the fact that constitutional chromosome rearrangements are present in each individual cell, including germ cells, thus adversely affecting reproduction in otherwise phenotypically normal carriers 4-6. Therefore, the primary focus of cytogenetic screening programs in domestic animal species is the identification of constitutional chromosome abnormalities, and the removal of carrier animals from the breeding population 7. As such, cytogenetic screening programs are continually being performed on the domestic pig, which have allowed for accurate estimates of the prevalence and rate of formation for constitutional rearrangements in this species 6-8. Between 0.5-1.5% of reproductively unproven young boars are estimated to be carriers of constitutional chromosome rearrangements, with reciprocal chromosome translocations being the most prevalent chromosome structural abnormality reported so far 1,6-9. Typically, routine karyotype analysis, which differentiates normal from abnormal chromosome constitutions, is based on the careful analysis of at least two optimal Giemsa banded karyotypes (GTG-banded), predicated on constitutional chromosome abnormalities being present in any single somatic cells 10,11. As such, chromosome

Balanced Chromosomal Rearrangements Associated with Hypoprolificacy in Australian Boars (Sus scrofa domesticus)

“…Our cytogenetic screening in purebred boars in a commercial nucleus pig herd from Australia identified a comparatively higher (6.38%) prevalence of reciprocal translocations. This prevalence rate is similar to several other published reports in other commercial herds spanning multiple countries, such as France (0.47% in 7700 young boar), Canada (0.58% in 5481 boars), Spain (3.8% in 849 pigs) [3,6,7]. Our data also suggest an association of reduced reproductive success in the hypoprolific boars with reciprocal chromosome translocations (Table 1).…”

“…The semen quality assessment methods used in boar studs in Australia do not detect chromosomal rearrangements, such as RTs. The results reported in this study have identified a high incidence (6.38%) of these rearrangements in a commercial Australian boar population and appear to be higher than in other pig populations (<1-4%) [3,6,7]. A minimum of 30 matings across multiple sows is a common practice in genetic nucleus herds to ensure no maternal confounding factors are affecting terminal sire performance.…”

“…Despite a large number (more than 140) of chromosomal rearrangements reported from France's swine population in the early 2000s [3], novel rearrangements are still being reported from different swine populations all over the world [4,6,7]. The present study identified three novel chromosomal rearrangements that can be characterised as the causative agent of hypoprolificacy as well as probable sterility.…”

“…Ducos et al [3] reported that the prevalence of balanced structural rearrangement in France's swine population is 0.47%. In another recent study, Rezaei et al [6] reported a 0.58% prevalence in the Canadian swine population. A comparatively higher prevalence rate was estimated in the Netherlands (0.7%) and Spain (3.3%) swine populations [4,7].…”

“…Chromosomal abnormalities, mostly balanced structural rearrangements, are known to be the source of several clinical conditions in livestock, such as congenital malfunction [1,2]. Several studies have reported a number of structural rearrangements in pigs [3][4][5][6][7] that are associated with hypoprolificacy (reduction in litter size). Reciprocal translocations (RTs) relate to the balanced chromosomal rearrangement or exchange of uneven chromosomal fragments leading to the development of genetically 'unbalanced' sperm.…”