Genes in diploid organisms operate singly, in pairs and in conjunction with genes at other locations throughout the nuclear DNA. Inbreeding depression and heterosis arise from the effects of gene combinations; that is, the effects of pairs of genes. Gene pairs are unique characteristics of individuals that are broken down and reformed each generation. This basic biological fact, introduced to many of us in high school biology, is the foundation of everything there is to say about this topic. Very few topics are so well rooted in a simple process.
Simplicity suffers, however, under real-world challenges of combining breeds or selecting to improve within a pure breed under a multi-trait breeding objective. This [article] attempts to explain in a rudimentary way the ways in which genes interact, transmit and recombine and the implications of those processes to breeding options available to dairy farmers.
Mechanisms of inbreeding
Inbreeding results from matings between related parents. Because breeding populations have finite size and long pedigree histories, mild inbreeding always exists by this definition. A more practical working definition of inbreeding is mating of parents more related than one would expect by chance alone. High levels of inbreeding are difficult to achieve in species where “selfing” is not possible.
A 35-year project at the Beltsville Agriculture Research Center between 1912 and 1949 produced one dairy cow with an inbreeding coefficient of over 75 percent, the highest ever recorded for bovines under experimental conditions. A single generation of mating between this cow and an unrelated sire would break down all of the inbreeding in the dam. Extreme inbreeding is difficult to achieve and easy to eliminate – if you have access to an unrelated mate.
Selection toward a single breeding objective can increase inbreeding, even in large populations. U.S. Holsteins have been under effective selection pressure for higher production and improved type since mid-1960. From 1982 until 2004, average inbreeding in a pedigree-recorded population of over 1,000,000 Holsteins increased from 1 to 5 percent. These figures may well understate actual inbreeding, as estimates are relative to a 1960 pedigree base and some pedigree information is missing in this population of grade and registered animals.
Consequences of inbreeding
Inbreeding increases homozygosity. More gene pairs become identical because they are copies of the same ancestral genes. Consequences of inbreeding include an increase in uniformity of offspring of inbred individuals through reduced variation in genetic material between germ cells. Offspring face higher frequencies of deleterious recessive gene combinations, increased inbreeding depression and greater variation in response to environmental stress. The last three effects of inbreeding are undesirable in commercial animals, while the first is of insufficient advantage to commercial producers to justify organized inbreeding programs.
While inbred animals are expected to express undesirable recessive characteristics more often than outbred animals, inbreeding does not cause “bad” alleles. Such alleles already exist in populations, almost exclusively as complete recessives, where dominant alleles suppress their expression and elimination through natural selection.
Inbreeding increases probabilities that an individual will inherit two copies of such alleles from related parents who inherited the undesirable gene from one common ancestor. While unfavorable under commercial production systems, this feature of inbreeding can be used to “purge” an inbred line of such alleles.
Inbreeding has been used to great advantage in plant species where generation intervals tend to be short, “selfing” allows rapid build-up of high levels of inbreeding, and many highly inbred lines can be developed and sustained simultaneously. Crosses of inbred lines produced hybrid corn – arguably one of the most successful advances in agriculture production in the last century. The role of inbreeding in animal breeding, however, is much more restricted and less successful.
Outbreeding – the mating of individuals less related than the average pair of animals in a population – produces opposite effects of inbreeding. Outbred individuals are less likely to express deleterious recessive alleles. Outbred animals may bear little resemblance to their parents due to breakdown of homozygous gene combinations and dominance. Outbred animals tend to be less subject to environmental stress than inbred animals. These characteristics have made outbred animals very useful under certain production systems, particularly those where reproductive efficiency is highly valued or environmental stress is not moderated by human intervention.
Two sources of homozygous gene pairs
Homozygosity is common throughout animal genomes, particularly for genetic regions related to fitness and survival. Natural selection has driven unfavorable genes from breeding populations at many loci of genes. Random drift also contributes to homozygous combinations. A limited number of ancestors, perhaps survivors of a genetic bottleneck, may have, by chance, been homozygous at specific loci of genes where genetic variation once existed.
A professor in my academic past, Dr. O. W. Robinson, called this a “founder effect.” [Bottlenecks also contribute to inbreeding and homozygosity at gene locations where genetic variation existed in founder animals.] If the possible ancestors are all homozygous for certain alleles, alleles passed to future generations will be alike, regardless of whether animals are closely related or not.
Identical alleles are referred to as “alike in state” when they were inherited from unrelated parents. Alleles that are alike because they were inherited from related parents, both of whom received a copy of the same allele from their common ancestor, are “identical by descent.” Formulas for calculation of inbreeding coefficients rely on probabilities of genes being identical by descent. Genes that are “alike in state” are ignored. Genetic effects of homozygous gene combinations are the same, regardless of whether genes are alike in state or identical by descent.
How does inbreeding happen in dairy cattle?
Most dairy farmers, given an economically acceptable choice, would avoid close inbreeding. Acceptable choices aren’t always readily available. Dairy cattle in U.S. herds are either direct descendants of bulls widely used in A.I. service or a generation removed through use of sons of A.I. bulls in natural service.
Bulls in A.I. service are used in many herds, which increases relationships between females that may be separated by time and distance. Prior to widespread use of A.I., relationships between females within a herd were likely higher than today, because many females were half siblings sired by the same bull. However, half siblings seldom existed in different herds. Such relationships are common today.
Furthermore, selection toward a generally similar and stable breeding objective by A.I. studs caused the same animals to appear as parents of bulls in A.I. Two sires in the U.S. Holstein population from the 1960s, Round Oak Rag Apple Elevation and Pawnee Farm Arlinda Chief, became highly influential through extensive use as sires of sons, sires of bull mothers, and through heavy use of successful progeny-tested descendents. The February 2007 Holstein Red Book reported that Elevation and Chief were responsible for 15.2 and 14.7 percent of all the genes carried by Holstein bulls likely to be used as A.I. sires this year.
Matings of these current A.I. bulls to cows and heifers in the current Holstein population (daughters of these bulls themselves or of their sires) will certainly produce many gene combinations that are homozygous by reason of “identity by descent” from Elevation and Chief. It would be very difficult to construct a mating between truly unrelated animals in U.S. Holsteins provided remote generations were probed for relationships. Elevation and Chief appear very rarely in the first four generations of today’s A.I. bulls, but appear again and again in generations seven through ten.
Options to avoid inbreeding
Avoiding inbreeding entirely is highly restrictive, if it is possible at all. Dairy cattle of pure breed origin must serve a functional purpose in production of dairy products. Profit-oriented herd managers want productive cattle, have the tools (progeny testing, sire evaluations, etc.) to differentiate between more and less productive choices and will logically favor a subset of the purebred population for breeding purposes. Rather than “avoiding” inbreeding, a more workable option would be to reduce or control major undesirable effects of inbreeding.
Several steps can be taken to reduce relationships without unduly compromising genetic progress toward economically justifiable goals. The key concept would be to recognize that maximum genetic progress comes at a high price in inbreeding depression and in restriction of future options to maintain some genetic diversity.
The most important decisions to control inbreeding and obtain most (but not all) benefits of selection are made by managers of A.I. young sire sampling programs. These managers respond to demands from semen purchasers, so the family of important decision makers to moderate effects of inbreeding is inclusive. I suggest the following approaches be considered:
•Limit the number of sons of the “top” sire of sons in any given time period. Use an expanded list of sires of sons, with particular interest in bulls with divergent pedigrees.
•Limit the use of the most popular bull mothers or bull-mother families. This objective parallels the expanded list of sires of sons above. E.T. and other reproductive technologies give us the power to use the best females too much.
•Diversity of breeding objectives stimulates diversity of genetic background. Separate selection indices for intensive management conditions and grazing herds are an example of such diversity and should be pursued by dairy producers.
•The industry, and in particular, individual dairy farmers through semen purchases, should embrace with enthusiasm inclusive selection indices directed towards improvement of lifetime economic merit. Such indices offer opportunity for prospective parents with divergent pedigrees to find a role in genetic improvement programs.
Success begets success (and increases relationships) through use of pedigree information in genetic evaluations. Yet, Mendelian segregation remains a powerful tool for genetic improvement. Sampling divergent pedigrees (with the unavoidable reduction in genetic merit) must be rewarded in the marketplace.
Ultimately, dairy producers will demand, and pay for, pedigree diversity. Payment may be through higher semen prices for bulls with unique pedigrees (but potentially lower genetic merit than “mainstream” genetics) or through use of unrelated parents from another breed in a crossbreeding program. Independence of dairy producers in the U.S. will lead to a variety of approaches in the years to come.
Options to utilize heterosis through crossbreeding
Heterosis arises from favorable gene combinations. Gene combinations are not equally important to all traits in dairy cattle or other species. Furthermore, more genetically divergent breeds are more likely to generate more heterosis than breeds with more similar genetic backgrounds. Traits subject to small amounts of inbreeding depression (perhaps somatic cell score is one such example) are expected to show less heterosis, as inbreeding depression results from the breakdown of favorable gene combinations.
Producers should be realistic about the benefits of heterosis for any trait and for specific pairs of breeds before finalizing expectations for crossbreeding. We know very little about heterosis for specific breed combinations for most traits in dairy cattle. For some important traits such as productive life and fertility, even general heterosis is not well established.
Dairy producers should anticipate that benefits of additive genetic merit of individual breeds are more important to performance of a particular cross than is heterosis. This is not to discount the benefits of heterosis. However, heterosis alone should not be expected to overcome breed weaknesses in individual traits.
The best rule for planning crossbreeding programs is to choose breeds carefully. Producers who don’t like one of the breeds they use in a cross probably won’t like the crossbred, either.
Selection within pure breeds remains a viable option for producers wishing to improve traits that can also be modified through crossbreeding. Results, however, will be more slowly attained than for crossbreeding, and perhaps much more slowly attained for traits where breed additive merit differs greatly and heterosis is substantial. Selection, however, imparts a permanent advantage that accumulates and builds over generations. Benefits from favorable gene combinations convey only to the individual and must be recreated each generation through mating plans.
Inbreeding in pure breeds motivates interest in crossbreeding but perhaps a more powerful force has been deterioration in health and fertility traits. Had breeding plans that included fitness traits been in effect (and effective) for the past 40 years, current interest in crossbreeding might have been greatly reduced, if existing at all. Under current conditions, however, breed differences in size, calving ease, fertility and production traits encourages many producers to consider crossbreeding programs for commercial milk production.
Breeders devoted to their favorite pure breeds are encouraged to implement and to carefully follow selection plans that improve lifetime economic merit of the dairy cow. This effort requires selection pressure on the lowly-heritable, slow-to-change, difficult-to-measure fitness traits. Breeders opting to utilize crossbreeding programs should choose breed combinations carefully, use progeny-tested, purebred A.I. bulls and use the same selection for lifetime economic merit as purebred enthusiasts. Finally, crossbreeding programs should follow plans that maintain favorable combinations of breed additive merit and minimal recombination loss. PD
References omitted but are available upon request at firstname.lastname@example.org
—Excerpts from 4th Biennial W.E. Petersen Symposium Proceedings