Introduction

Sheep farming occurs throughout Mexico with regional variations in response to natural resources availability and markets¹. The Organism of National Sheep Farmer Unity (Organismo de la Unidad Nacional de Ovinocultores - UNO) encompasses producers of specialized and registered sheep breeds, coordinates the genealogical registry of breed purity, and organizes genetic improvement programs based on genetic evaluations². Selection based on the best linear unbiased predictor (BLUP), generated from genetic evaluations, favors selection of related animals, consequently increasing inbreeding³. Furthermore, levels of inbreeding and kinship are involved in genetic evaluations and BLUP predictions^4,5.

Selection schemes can allow a small number of breeder stock or select families to generate changes in population structure, increasing inbreeding levels, reducing genetic variability, and possibly resulting in genetic drift^6,7. Genetic variability determines a population’s capacity to respond to selection and genetic progress. Identifying the factors that affect genetic variability is essential when evaluating breeding strategies and deciding whether to continue with a selection scheme or take corrective actions⁸. Pedigree analysis is based on population genetic parameters and describes a population’s genetic dynamics and variability. The genetic structure of a population helps to track gene flow, providing information on the founding ancestors and their contributions to variability in the current population^9,10.

The present study objective was to analyze the pedigree and population structure of ten sheep breeds using population genetic parameters such as pedigree integrity, number of generations, kinship and inbreeding, ancestors and founders, effective number and generational interval, among others. The results can be applied in developing selection schemes aimed at optimizing population response to selection by limiting the genetic variability loss rate.

Material and methods

Analyses were done using the national genealogical registry databases for each of ten sheep breed populations: Blackbelly (BBL); Charollais (CHA); Dorper (DOR); White Dorper (DOB); Dorset (DOS); Hampshire (HAM); Katahdin (KAT); Pelibuey (PEL); Rambouillet (RAM); and Suffolk (SUF). The pedigrees incorporated individuals born between 1992 and 2018, the Table 1 describes the genealogical information analyzed, pedigree analyses were run with the ENDOG ver. 4.0 software¹¹ to evaluate the following population genetic descriptors.

Results and discussion

The precision of a population structure analysis depends on pedigree integrity and genealogical information content over generations. Incomplete information can lead to only approximate assignment of individuals to generations and inaccurate calculations of F and Ne. The present results for percentage of ancestors reflect more complete, deep genealogical information for the maternal route (Table 2). At the parents level, values ranged from 76.4 % (SUF) to 95.3 % (KAT), with an overall average of 86.0 %. The percentages of animals with unknown parents corresponded to the group of founding animals. Similar integrity levels and genealogical information content have been reported for pedigrees of the Nilagiri and Sandyno²⁴, Santa Inés²⁵ and Malpura¹⁷ breeds. In contrast, analyzed pedigrees for the Mehraban¹², Guilan²⁶ and Morada Nova⁸ had percentages of less than 60% for known parents, less than 40 % for grandparents and less than 30 % for great-grandparents. Of note is that, in all these reports the genealogical information was more extensive and complete for the maternal route, as occurred in the present study.

Pedigree integrity is linked to estimates of NCG, NTG and NEG. In the present results the maximum values were similar across the ten breeds (Table 3). However, the interbreed averages differed noticeably, with the highest values for KAT and the lowest for DOS. Population structure is the result of the selection and reproductive management strategies applied by producers. The differences observed between the analyzed populations may be attributed to sire-based reproductive management which could have implications in Ne and GI. The PS and PD values (Table 1) show to what extent breeder stock were used across generations, and the SD% and D/S estimates are related to selection intensity and pressure.

In the evaluated pedigrees the consanguineous population fluctuated from 12.3 % in DOS to 48.7 % in DOB, with an overall average of 29.7 % (Table 1). Inbreeding (F) levels ranged from 3.9 % in KAT to 14.6 % in DOB, with an 8.0 % average. The levels and trends of F and its components (ACR, Ne, fe and fa) help in evaluating the evolution of genetic variability over time. Consanguineous animals are directly affected by the effects of inbreeding depression and all the consequences that an increase in F brings with it. Given the importance of maternal effects in sheep^27,28, the possible effects of inbreeding depression also need to be evaluated through maternal inbreeding levels, using parameters such as percentage of consanguineous mothers and average inbreeding (Table 1).

In the present results F exhibited three overall trends in its evolution. First, in all the studied pedigree populations the percentage of consanguineous animals increased over time (Table 1; Figure 1), with β_P values ranging from 1.4 to 7.7 %. Second, inbreeding levels exhibited negative trends (Table 1; Figure 2), with an average β_F value of -0.412 across the ten pedigrees. Third, ARC levels have remained stable over time and within each pedigree (Figure 3). Genetic improvement strategies need to consider an adequate balance between selection intensity, inbreeding and genetic variability. The scenarios commonly observed in the evolution of F can be attributed to three general factors: use of related breeders within a numerically large population with low ARC levels; selection based on BLUP, which raises the probability of selection of related animals; and advances in reproductive technologies, which can reduce the number of parents needed to produce the next generation of breeders^3,4,10.

Figure 1 Trends of percentage of inbreeding individuals. Breeds: Blackbelly (BBL), Charollais (CHA), Dorper (DOR), White Dorper (DOB), Dorset (DOS), Hampshire (HAM), Katahdin (KAT), Pelibuey (PEL), Rambouillet (RAM) and Suffolk (SUF) 

Figure 2 Trends in average inbreeding in the consanguineous population; inbreeding is defined as homozygosis levels in individuals caused by related progenitors. Breeds: Blackbelly (BBL), Charollais (CHA), Dorper (DOR), White Dorper (DOB), Dorset (DOS), Hampshire (HAM), Katahdin (KAT), Pelibuey (PEL), Rambouillet (RAM) and Suffolk (SUF).  

Figure 3 Trends of average additive genetic relatedness coefficient. Breeds: Blackbelly (BBL), Charollais (CHA), Dorper (DOR), White Dorper (DOB), Dorset (DOS), Hampshire (HAM), Katahdin (KAT), Pelibuey (PEL), Rambouillet (RAM) and Suffolk (SUF) 

The KAT, PEL and RAM pedigree populations had the highest growth rates in consanguineous population (Table 1; Figure 1). The DOB and DOR pedigrees had the largest negative trends in F while DOB and CHA had the highest ARC values. The variation in the present results coincides with a diversity of F values reported elsewhere. For example, F values were near zero in a study of seven sheep populations in France²⁹, but positive in a study of six breeds from Canada¹⁰. Positive trends in F and ARC have also been reported for the breeds Finnsheep³⁰, Merino¹⁷ and Malpura¹⁸.

The concept of realized effective population size (Ne) was developed based on ideal population guidelines and is a basic concept in the design of genetic conservation and/or improvement programs. It reflects the accumulation of genetic relationships between individuals, making it possible to predict changes in F levels. In addition, it quantifies changes in genetic variance through genetic drift and changes in gene frequencies³¹. The breeding structure and reproductive demographics of the evaluated sheep populations differed from ideal population approaches, but, when applied, realized Ne tends to adjust for some of these differences³². Low Ne levels are associated with decreased genetic variability, increased crossing between related individuals, allele fixation and the greatest reduction in selection response³³. A Ne value <50 is cause for concern; when developing pedigree populations, Ne values ≥50 are preferable since these imply the presence of more F levels ≤1%³⁴. Even higher Ne values are recommended for populations subject to genetic improvement because these optimize selection response but with a minimal increase in F³⁵. Six of the evaluated pedigree populations had Ne values between 50 and 73.5 (Table 3), indicating that any increases in F will be ≤1%. However, four populations had Ne values between 12.2 and 36.8, highlighting the need for close monitoring of F and ARC values, and their possible consequences in genetic improvement. The highest six Ne values in the present results are within previously reported ranges. In a report on forty sheep breeds evaluating Ne estimation methods the value range was 38 to 675, with a 191 average³². A series of studies evaluating the pedigree of a total of fifteen sheep populations found Ne estimates ranging from 55 to 276^29,30,36,37.

The genetic relationships between founders and fe represent initial genetic variability, since the founders’ contribution to pedigree variability is the set of genes which has remained intact through generations³⁸. The number of individuals explaining 50% of pedigree variability was 7 in DOB, 13 in CHA and 44 in SUF (Table 3). Low ancestor numbers explaining pedigree variability is associated with higher F and ARC values. The effective number of ancestors (fa) includes the possible causes of losses of genetic variability. In general, fe>fa; a wider discrepancy between them indicates that fewer founders are participating in the pedigree over the generations. The fe/fa ratio represents differential breeding management, considering any bottlenecks a population may have experienced. Higher ratio values indicate that most of the ancestors were founders, without bottlenecks³⁹. In the present results the fe/fa ratio ranged from 1.2 to 2.0, a range which coincides with those reported for the breeds Baluchi¹⁶, Afshari⁴⁰, Kermani³⁶, Moghani³⁷ and Morada Nova⁸.

The ARC can be seen as a summary of a population’s breeding management, while F represents the crossing of related animals but does not explain why these crosses occurred. In the relationship between fe and F, a founder’s ARC indicates the percentage of a population originating in her or him¹¹. Use of the ARC allows design of crosses by maintaining certain levels of F in the progeny. In the present results ARC levels remained unchanged and F levels did not increase (Figures 2 and 3). However, over time the breed stock came from a small number of families, tended to be genetically related and was selected from within herds, with minimal interherd genetic flow (Figure 1).

Generational interval (GI) is vital in validating losses of genetic variability and genetic progress over time. Selection intensity, which is associated with SD% and D/S, tends to reduce the GI but produces losses in genetic variability given the minimal contribution of this breed stock to the population^9,38. Average estimated GI in the present study was 3.45 yr with a 3.0 to 4.15 yr range, and no substantial differences between the four pairings (Table 4). The highest GI estimates were for the RAM and SUF pedigrees and the lowest for BBL and DOR. A study of seven sheep breeds in France reported an estimated average GI of 3.5 years and a range of 1.9 to 5.0²⁹; lower average GI values have been reported for Xalda sheep (2.9 yr)¹⁹ and Somali sheep (2.1 yr)⁴¹.

Conclusions and implications

The present pedigree evaluation represents a summary of the results of producers’ genetic and breeding management strategies. It is useful in designing genetic selection programs because it contemplates the relationship between selection response and increases in inbreeding, including their consequences. The trends did not differ greatly between the ten evaluated pedigree populations: inbreeding levels tended to decrease, with negative slopes (P<0.05); genetic relationships were stable over time; and the consanguineous population increased, with positive slopes (P<0.05). The KAT, PEL and RAM populations had high consanguineous population growth rates. Inbreeding was highest in the DOB and DOS populations, and genetic relationships were highest in DOB and CHA. Effective population size estimates were lowest in the BBL, CHA, DOB, and SUF populations, highlighting the need to monitor the evolution of inbreeding and its possible implications in these pedigrees.