(Reprinted from The Basenji, May/June 2012)
By Robert C Lacy PhD & Carol A Beuchat PhD
In response to the paper by Thompson (2012), we wish to provide some information about issues relevant to managing the genetic health of the pedigree Basenji population. Thompson provides a valuable introduction to the principles underlying genetic management of breeding programs for rare and valuable populations. One of us (RCL) has been involved in the development and application of these concepts and methods for the preservation of endangered species for the past 30 years, and we agree with Thompson that many of the principles that have been developed for optimal management of threatened species have value also for the management of breeds of domesticated animals. However, there are also differences in the goals and feasible methods that should be considered when adapting the lessons from endangered species management to breed management. Below, we address some of the issues raised by Thompson that might need clarification or further explanation.
1) When numbers such as 5-15 founders, or no fewer than 6, have been provided by conservation geneticists as the minimum number necessary to build a viable population, the context has been emergency efforts to sustain a wildlife population or species, and the emphasis is very much on a “minimum” number. Even when the possible loss of an entire species is at risk, it is debatable (and it is vigorously debated!) if it is worth putting resources into trying to build a breeding population from fewer than 6 founders. As Thompson notes, a recommendation of 20 effective founders is typical as the starting point to rescue a population at risk of extinction (Lacy 1989). Beyond the recommended minimum of 20 effective founders, zoos must carefully consider the incremental benefit of starting with larger numbers of founders, because of the considerable cost – sometimes including even the potential to seriously damage the remaining wild population by overharvesting – of importing an additional 10 to 20 individuals of a large wildlife species that is likely difficult to capture, handle, and transport.
2) General statements about minimum number of founding individuals necessary to build a viable closed population are based on models of population genetics that assume an "ideal" population where breeding is either random or will be managed to preserve genetic diversity using a breeding strategy designed for this purpose. An example of this would be a captive zoo population of a species where reproduction is carefully managed to minimize loss of genetic diversity and changes from the original, wild traits over generations. The strategy pursued in such a management plan would be to maintain equal genetic contributions of all founders to subsequent generations, as this would maintain the maximum amount of the original genetic diversity.
In populations of animals (whether species or breeds) where management of reproduction is not focused purely on the preservation of the full range of characteristics (good and bad) of the founders, the assumptions underlying the "ideal" estimate (as above) are not met. Some of the variation brought into the population via the founders will likely be lost in the first few generations, and the number of founding individuals will need to be greater in order to provide an adequate genetic base for future breeding. Indeed, even in breeding programs for endangered species in zoos, we know that in spite of our best efforts some initial “potential founders” will not contribute to future generations, so that we need to start with more sometimes many more – wild-collected animals to achieve 20 effective founders.
This would likely even more so be the case in a population of purebred dogs for several reasons. A breeding plan designed to maintain as much of the founding genetic diversity as possible would require the collective cooperation of all breeders as it must use all existing reproductive dogs in an optimally designed and rigorously managed breeding scheme. But dog breeders have specific breeding priorities of their own, such as selection for particular traits in their dogs (e.g., color, leg length, behavioral traits), or preferences to use particular individuals in their breeding program. Their breeding options might also be constrained by geography, or by available space and other resources. The presence of known genetically based health issues will also influence breeding decisions, and selection against genes that can cause health problems (while sometimes necessary) further reduces the variation across the rest of the genes as well, because the selection by definition reduces the number of breeders contributing to the next generation. Thus, it seems highly unlikely that all custodians of breeding individuals could fully cooperate with a breeding strategy designed to ensure equal contributions of all founders to subsequent generations. With selective breeding, the genetic diversity in the founding population can be substantially reduced in just a few generations (Oliehoek, Bijma, & van der Meijden 2009; Maki 2010).
3) If a large number of founders cannot be obtained initially, or if some of those lineages are lost or under-represented in subsequent generations, or if breeder goals will necessarily include selection for desired traits and against genetic problems, then low and declining diversity of the population can later be increased or restored through the addition of new founders – if available – to the breeding stock. This can bring back genetic variants that once represented the species or breed but were lost by chance, reverse incidental fixation of deleterious genes and accumulated inbreeding, and provide the diversity necessary for continued modification and improvement through selection.
4) Full analysis of the population genetics of the (worldwide) pedigree of Basenjis has not been done, so there is no information about how well the genetic diversity of founders has been maintained, or about the degree of inbreeding in the existing population. A genetic analysis using pedigree information for all dogs back to founders could provide substantial insights as to the value of any additional founders. This information would also allow breeders to make the best possible decisions about the use of their breeding stock by identifying populations of dogs that are most critical to maintain in the breeding population, and the degree of imbalance in the contributions of founders to the current generation (Lacy 1989; Ballou & Lacy 1995).
5) Basenjis are one of the (very) few breeds where a large population of animals from which the founders were originally drawn still exists in Africa, and these animals have not been subject to an organized breeding program, so mating has likely been more or less random. Consequently, we can expect that in such a population, a diversity of genetic alleles will still be present. Selecting animals randomly from this well-mixed gene pool is most likely to yield a genetic subsample that reflects the actual genetic diversity in the native African dogs. If the selection of animals is not random (for example, certain traits are desired, or some traits simply do not result in dogs that will be successful breeders if brought out of Africa), or if the dogs cannot be collected across the geographic range (possibly resulting in some lineages in Africa being sampled several times), then a larger number of new founders is required to obtain a good representation of the diversity of the breed.
3) If a large number of founders cannot be obtained initially, or if some of those lineages are lost or under-represented in subsequent generations, or if breeder goals will necessarily include selection for desired traits and against genetic problems, then low and declining diversity of the population can later be increased or restored through the addition of new founders – if available – to the breeding stock. This can bring back genetic variants that once represented the species or breed but were lost by chance, reverse incidental fixation of deleterious genes and accumulated inbreeding, and provide the diversity necessary for continued modification and improvement through selection.
4) Full analysis of the population genetics of the (worldwide) pedigree of Basenjis has not been done, so there is no information about how well the genetic diversity of founders has been maintained, or about the degree of inbreeding in the existing population. A genetic analysis using pedigree information for all dogs back to founders could provide substantial insights as to the value of any additional founders. This information would also allow breeders to make the best possible decisions about the use of their breeding stock by identifying populations of dogs that are most critical to maintain in the breeding population, and the degree of imbalance in the contributions of founders to the current generation (Lacy 1989; Ballou & Lacy 1995).
5) Basenjis are one of the (very) few breeds where a large population of animals from which the founders were originally drawn still exists in Africa, and these animals have not been subject to an organized breeding program, so mating has likely been more or less random. Consequently, we can expect that in such a population, a diversity of genetic alleles will still be present. Selecting animals randomly from this well-mixed gene pool is most likely to yield a genetic subsample that reflects the actual genetic diversity in the native African dogs. If the selection of animals is not random (for example, certain traits are desired, or some traits simply do not result in dogs that will be successful breeders if brought out of Africa), or if the dogs cannot be collected across the geographic range (possibly resulting in some lineages in Africa being sampled several times), then a larger number of new founders is required to obtain a good representation of the diversity of the breed.
6) We assume that the desire to increase the genetic heterogeneity of the pedigree Basenji population is motivated at least in part by concern about the possibility of unacceptable levels of genetic diseases in the future as a consequence of the small size of the founder population and subsequent inbreeding. Such problems have arisen in many breeds (canine and otherwise) that descend from small numbers of founders or have small breeding populations, and can be difficult to counter once the problems become prevalent enough to be to make it clear that restoration of genetic variation is needed. However, one issue breeders might be concerned about is that the addition of new animals can introduce again to the breeding stock potentially deleterious genes. We do not believe that this problem will be significant enough to override the benefits of restored genetic variation. The problem is not that deleterious alleles exist – as it is the case that all animals carry some deleterious recessive alleles and a few new ones arise by mutation every generation – but rather that in a small population or one with few founders some of the deleterious alleles can be expressed in homozygous condition in a number of animals. It should be noted that natural selection continues to work on wild populations, and with much greater force and efficiency that in populations under our care, so that deleterious alleles will have been held to very low frequencies. In a large, genetically diverse population, therefore, the probability of producing offspring that are homozygous for the disease allele is very low.
Especially for Basenjis, which in Africa are subject to strong natural selection when they fend for themselves, it is reasonable to expect that in the absence of evidence to the contrary, the animals should be genetically healthy, and a checkup from a veterinarian should satisfy to catch anything that might become a problem. Again, the key to managing health issues is maintaining the genetic diversity of the breeding dogs. If a deleterious allele does become common enough to be a problem for the breed, selection against that allele might be practiced, but we need to recognize that such selection will also reduce the genetic diversity across the rest of the genes, and any beneficial traits carried by the dogs that are removed from breeding will be lost (Lacy 2000). Thus, having high diversity within the breeding stock is essential both to minimize expression of deleterious traits and to allow selection to be practiced when desired without inadvertently jeopardizing the genetic health of the breed.
Especially for Basenjis, which in Africa are subject to strong natural selection when they fend for themselves, it is reasonable to expect that in the absence of evidence to the contrary, the animals should be genetically healthy, and a checkup from a veterinarian should satisfy to catch anything that might become a problem. Again, the key to managing health issues is maintaining the genetic diversity of the breeding dogs. If a deleterious allele does become common enough to be a problem for the breed, selection against that allele might be practiced, but we need to recognize that such selection will also reduce the genetic diversity across the rest of the genes, and any beneficial traits carried by the dogs that are removed from breeding will be lost (Lacy 2000). Thus, having high diversity within the breeding stock is essential both to minimize expression of deleterious traits and to allow selection to be practiced when desired without inadvertently jeopardizing the genetic health of the breed.
7) Thompson (2012) discusses the often-cited number of 50 and correctly notes that this refers to a recommendation for a minimum effective population size, not the minimum number of founders. For the reasons discussed above, achieving the recommended 20 effective founders, might require fewer or more than 50 initial imported animals. The recommendation of 50 as a minimum effective population size derives from a desire to minimize the accumulation of inbreeding subsequent to the founder generation.
The definition that Thompson gives for effective population size is correct only under very specific and idealized circumstances. Effective population size is not, in general nor in most populations, "the current number of breeding individuals in a population that contribute genes to succeeding generations." Effective population size is the number of breeding animals in a theoretical random breeding population that would experience the same rate of change in allele frequencies, or the same degree of inbreeding, as seen in the actual population (Lacy 1995). The number of breeding animals will be close to the effective population size only if breeding is truly random. Of course, in any real breeding program, breeding is far from random and some lineages contribute more to the population as a whole than others, because breeders select for specific traits or are limited in their choice of sire. In pedigreed dog breeds, the effective population size will likely be substantially smaller than the actual number of breeding animals, and this leads to more rapid loss of the genetic diversity that was brought in via the original founders.
The recommendation of a minimum effective population size of 50 is equivalent, mathematically, to a recommendation to keep the rate of increase in the coefficient of inbreeding below 1% per generation. This recommendation arises from the centuries of experience of animal breeders regarding what level of inbreeding can be accepted for a moderate number of generations without incurring risk of genetic damage in the form of higher frequency of genetic defects and lower overall average fitness of individuals. High levels of inbreeding have well documented deleterious effects including reduced fertility, decreased litter size, lower birth weight, lower survival, decreased resistance to disease, and decreased tolerance of environmental stress (Charlesworth & Willis 2009; Keller & Waller 2002; Lacy 1997; Ryan et al. 2002). Not every inbred animal will be affected, but the probability of problems increases and the average level of performance declines. Moreover, it is not predictable which lineages will suffer from inbreeding problems, and selection programs aimed at reversing inbreeding problems usually have only limited effectiveness (Lacy 2007).
8) Whenever possible, within breeding programs for rare wildlife species we start to seek out new animals to boost genetic diversity again whenever the cumulative mean inbreeding level increases to about 5% or more. When cumulative inbreeding levels reach 10% or higher, we consider the need for new animals to be urgent. For example, the Association of Zoos and Aquariums recently decided to open up breeding of even endangered species to exchange with private breeders who are not accredited members nor bound by association policies that require registry of animals in studbooks, when the breeding population mean inbreeding rises above 10% -- unless a plan is in place to quickly bring in new founders to restore the lost variation to the more tightly controlled population.
The definition that Thompson gives for effective population size is correct only under very specific and idealized circumstances. Effective population size is not, in general nor in most populations, "the current number of breeding individuals in a population that contribute genes to succeeding generations." Effective population size is the number of breeding animals in a theoretical random breeding population that would experience the same rate of change in allele frequencies, or the same degree of inbreeding, as seen in the actual population (Lacy 1995). The number of breeding animals will be close to the effective population size only if breeding is truly random. Of course, in any real breeding program, breeding is far from random and some lineages contribute more to the population as a whole than others, because breeders select for specific traits or are limited in their choice of sire. In pedigreed dog breeds, the effective population size will likely be substantially smaller than the actual number of breeding animals, and this leads to more rapid loss of the genetic diversity that was brought in via the original founders.
The recommendation of a minimum effective population size of 50 is equivalent, mathematically, to a recommendation to keep the rate of increase in the coefficient of inbreeding below 1% per generation. This recommendation arises from the centuries of experience of animal breeders regarding what level of inbreeding can be accepted for a moderate number of generations without incurring risk of genetic damage in the form of higher frequency of genetic defects and lower overall average fitness of individuals. High levels of inbreeding have well documented deleterious effects including reduced fertility, decreased litter size, lower birth weight, lower survival, decreased resistance to disease, and decreased tolerance of environmental stress (Charlesworth & Willis 2009; Keller & Waller 2002; Lacy 1997; Ryan et al. 2002). Not every inbred animal will be affected, but the probability of problems increases and the average level of performance declines. Moreover, it is not predictable which lineages will suffer from inbreeding problems, and selection programs aimed at reversing inbreeding problems usually have only limited effectiveness (Lacy 2007).
8) Whenever possible, within breeding programs for rare wildlife species we start to seek out new animals to boost genetic diversity again whenever the cumulative mean inbreeding level increases to about 5% or more. When cumulative inbreeding levels reach 10% or higher, we consider the need for new animals to be urgent. For example, the Association of Zoos and Aquariums recently decided to open up breeding of even endangered species to exchange with private breeders who are not accredited members nor bound by association policies that require registry of animals in studbooks, when the breeding population mean inbreeding rises above 10% -- unless a plan is in place to quickly bring in new founders to restore the lost variation to the more tightly controlled population.
Thompson (2012) mistakenly describes the goal of 90% of the diversity of the source population (equivalent to cumulative inbreeding no greater than 10%) as the goal for starting a population, whereas the 90% criteria is actually widely applied as the limit for acceptable genetic decay over the long-term (e.g., 100 years) for a viable population designed to sustain and represent the source population. I.e., 10% loss of diversity is not the benchmark for an acceptable starting point, but rather is often defined as an end point below which a population should not be allowed to descend, or as the point at which quick action should be taken to obtain new founders to restore variation.
While conservation biologists do aim to start breeding programs of wildlife with at least 20 effectively contributing breeders (i.e., 97.5% of source diversity), we recognize that after a number of generations of propagating a small breeding stock, we often cannot avoid losing some or even much of the diversity that had been present in the founders. The goal of never dropping below 90% of the source population diversity drives both the recommendation to start with much more diversity than this, and the recommendation to maintain an effective population size greater than 50 so that further losses are no more than 1% per generation. A simple calculation shows that if the starting diversity is about 97.5% and 1% is lost in each subsequent generation, then the population can be sustained above the 90% goal for only 7-8 generations. Although this short-term strategy often is acceptable for endangered species breeding programs that are designed to be a temporary reserve for a species until they can be returned to a better protected wild habitat (e.g., as has been done with condors, black-footed ferrets, Mexican wolves, and red wolves), presumably people who sustain special breeds of dogs are interested in longer term preservation. Therefore, good genetic management will require more initial founders, a much larger breeding population allowing slower inbreeding, more rigorous control over breeding based on pedigree rather than expressed traits, and/or periodic replenishment of diversity with new founders.
While conservation biologists do aim to start breeding programs of wildlife with at least 20 effectively contributing breeders (i.e., 97.5% of source diversity), we recognize that after a number of generations of propagating a small breeding stock, we often cannot avoid losing some or even much of the diversity that had been present in the founders. The goal of never dropping below 90% of the source population diversity drives both the recommendation to start with much more diversity than this, and the recommendation to maintain an effective population size greater than 50 so that further losses are no more than 1% per generation. A simple calculation shows that if the starting diversity is about 97.5% and 1% is lost in each subsequent generation, then the population can be sustained above the 90% goal for only 7-8 generations. Although this short-term strategy often is acceptable for endangered species breeding programs that are designed to be a temporary reserve for a species until they can be returned to a better protected wild habitat (e.g., as has been done with condors, black-footed ferrets, Mexican wolves, and red wolves), presumably people who sustain special breeds of dogs are interested in longer term preservation. Therefore, good genetic management will require more initial founders, a much larger breeding population allowing slower inbreeding, more rigorous control over breeding based on pedigree rather than expressed traits, and/or periodic replenishment of diversity with new founders.
9) Inbreeding levels in some dog breeds are already substantially higher than 10% (Leroy et al 2009; Leroy 2011). Although we are not aware of the value for Basenjis, we would expect that it is probably higher than 10% as well. For perspective, a mean inbreeding level of 10% is the equivalent of having the genetic diversity that would be provided by only 5 founders – which would not seem to be a very good representation of the breed. So for the pedigree Basenji, which is an unmanaged population (i.e., there is no single authority responsible for making breeding decisions), and which has limited opportunities for introducing new breeding stock on a regular and continuing basis, we would recommend that breeders should not forego the opportunity to add new animals whenever dogs representing the breed can be added to the breeding programs. This will help to maintain the genetic diversity in the population as a whole in the face of the conflicting demands on breeders.
For all purebred dogs (and wildlife species, for that matter), the goal is healthy animals that represent the breed well and can continue to respond to selection. Selecting only for breedspecific traits without also actively working to sustain the underlying genetic diversity needed to produce a healthy dog would ultimately result in failure. Two well established and even fundamental principles of genetic management are that (1) accumulated inbreeding almost inevitably causes reduced fitness and performance in a sexually reproducing species, and (2) variation is necessary to allow successful selection for desired traits or against deleterious traits. With adequate knowledge of the ancestry and current genetic structure of the breed, and some prudent breeding strategies, breeders can achieve their breeding goals while protecting the health of their animals and safe-guarding the future of the breed. Pedigree analysis software is available for assessing the effective population size, the loss of genetic variation to date, the rate of accumulation of inbreeding, and the potential benefits of adding new founders (Lacy, Ballou, & Pollak 2012). Genetics management advisors who are experienced in pedigree analysis for zoos would likely be available to assist by providing analyses and advice to Basenji and other dog breed groups. Regularly updating the genetic analysis of the population as new individuals are added by birth or introduction, and revisiting the breeding plan in light of new information, is the best strategy to assure the health of the breed for the long term.
For all purebred dogs (and wildlife species, for that matter), the goal is healthy animals that represent the breed well and can continue to respond to selection. Selecting only for breedspecific traits without also actively working to sustain the underlying genetic diversity needed to produce a healthy dog would ultimately result in failure. Two well established and even fundamental principles of genetic management are that (1) accumulated inbreeding almost inevitably causes reduced fitness and performance in a sexually reproducing species, and (2) variation is necessary to allow successful selection for desired traits or against deleterious traits. With adequate knowledge of the ancestry and current genetic structure of the breed, and some prudent breeding strategies, breeders can achieve their breeding goals while protecting the health of their animals and safe-guarding the future of the breed. Pedigree analysis software is available for assessing the effective population size, the loss of genetic variation to date, the rate of accumulation of inbreeding, and the potential benefits of adding new founders (Lacy, Ballou, & Pollak 2012). Genetics management advisors who are experienced in pedigree analysis for zoos would likely be available to assist by providing analyses and advice to Basenji and other dog breed groups. Regularly updating the genetic analysis of the population as new individuals are added by birth or introduction, and revisiting the breeding plan in light of new information, is the best strategy to assure the health of the breed for the long term.
Robert C. Lacy, Senior Conservation Scientist, Chicago Zoological Society Committee on Evolutionary Biology, University of Chicago Science Advisor, SSC Conservation Breeding Specialist Group, International Union for the Conservation of Nature.
Carol A. Beuchat, Founder and Scientific Director, Institute of Canine Biology.
Carol A. Beuchat, Founder and Scientific Director, Institute of Canine Biology.
REFERENCES
Ballou, J.D.. & R.C. Lacy. 1995. Identifying genetically important individuals for management of genetic diversity in pedigreed populations. Pp 76-111 in J.D. Ballou, M. Gilpin, & T. Foose (eds). Population Management for Survival & Recovery: Analytical Methods and Strategies in Small Population
Conservation. Columbia Univ. Press, NY.
Charlesworth, D. & J.H. Willis. 2009. The genetics of inbreeding depression. Nature Reviews 10:783-796.
Keller, L.F. & D.M. Waller. 2010. Inbreeding effects in natural populations. Trends in Ecology & Evolutions 17: 230-241.
Lacy, R.C. 1989. Analysis of founder representation in pedigrees: Founder equivalents and founder genome equivalents. Zoo Biology 8:111-124.
Lacy, R.C. 1995. Clarification of genetic terms and their use in the management of captive populations. Zoo Biology 14:565-578.
Lacy, R.C. 1997. Importance of genetic variation to the viability of mammalian populations. Journal of Mammalogy 78:320¬ 335.
Lacy, R.C. 2000. Should we select genetic alleles in our conservation breeding programs? Zoo Biology 19:279-282.
Lacy, R.C. 2007. Understanding inbreeding depression: 20 years of experiments with Peromyscus mice. Pages 327-329 in F.W. Allendorf and G. Luikart. Conservation and the Genetics of Populations. WileyBlackwell, New York.
Lacy, R.C., J.D. Ballou, & J.P. Pollak. 2012. PMx: software package for demographic and genetic analysis and management of pedigreed populations. Methods in Ecology and Evolution 3:433-437.
Leroy, G. 2011. Genetic diversity, inbreeding and breeding practices in dogs: results from pedigree analyses. Veterinary Journal 189:177-182.
Leroy, G., E. Verrier, J.C. Meriaux, & X. Rognon. 2009. Genetic diversity of dog breeds: within-breed diversity comparing genealogical and molecular data. Animal Genetics 40:333-343.
Maki, K. 2010. Population structure and genetic diversity of worldwide Nova Scotia Duck Tolling Retriever and Lancashire Heeler dog populations. Journal of Animal Breeding and Genetics 127:318-326.
Oliehoek, P.A., P. Bijma, & A. van der Meijden. 2009. History and structure of the closed pedigreed population of Icelandic Sheepdogs. Genetics Selection Evolution 41:39.
Ryan, K.K., R.C. Lacy, and S.W. Margulis. 2002. Impacts of inbreeding on components of reproductive success. Pages 82-96 in: W. V. Holt, A. R. Pickard, J. C. Rodger, and D. E. Wildt, eds. Reproductive Science and Integrated Conservation. Cambridge University Press, Cambridge, UK.
Thompson, J. 2012. How many founders does it take to make a breed? The Modern Basenji 2: 26-27.
Ballou, J.D.. & R.C. Lacy. 1995. Identifying genetically important individuals for management of genetic diversity in pedigreed populations. Pp 76-111 in J.D. Ballou, M. Gilpin, & T. Foose (eds). Population Management for Survival & Recovery: Analytical Methods and Strategies in Small Population
Conservation. Columbia Univ. Press, NY.
Charlesworth, D. & J.H. Willis. 2009. The genetics of inbreeding depression. Nature Reviews 10:783-796.
Keller, L.F. & D.M. Waller. 2010. Inbreeding effects in natural populations. Trends in Ecology & Evolutions 17: 230-241.
Lacy, R.C. 1989. Analysis of founder representation in pedigrees: Founder equivalents and founder genome equivalents. Zoo Biology 8:111-124.
Lacy, R.C. 1995. Clarification of genetic terms and their use in the management of captive populations. Zoo Biology 14:565-578.
Lacy, R.C. 1997. Importance of genetic variation to the viability of mammalian populations. Journal of Mammalogy 78:320¬ 335.
Lacy, R.C. 2000. Should we select genetic alleles in our conservation breeding programs? Zoo Biology 19:279-282.
Lacy, R.C. 2007. Understanding inbreeding depression: 20 years of experiments with Peromyscus mice. Pages 327-329 in F.W. Allendorf and G. Luikart. Conservation and the Genetics of Populations. WileyBlackwell, New York.
Lacy, R.C., J.D. Ballou, & J.P. Pollak. 2012. PMx: software package for demographic and genetic analysis and management of pedigreed populations. Methods in Ecology and Evolution 3:433-437.
Leroy, G. 2011. Genetic diversity, inbreeding and breeding practices in dogs: results from pedigree analyses. Veterinary Journal 189:177-182.
Leroy, G., E. Verrier, J.C. Meriaux, & X. Rognon. 2009. Genetic diversity of dog breeds: within-breed diversity comparing genealogical and molecular data. Animal Genetics 40:333-343.
Maki, K. 2010. Population structure and genetic diversity of worldwide Nova Scotia Duck Tolling Retriever and Lancashire Heeler dog populations. Journal of Animal Breeding and Genetics 127:318-326.
Oliehoek, P.A., P. Bijma, & A. van der Meijden. 2009. History and structure of the closed pedigreed population of Icelandic Sheepdogs. Genetics Selection Evolution 41:39.
Ryan, K.K., R.C. Lacy, and S.W. Margulis. 2002. Impacts of inbreeding on components of reproductive success. Pages 82-96 in: W. V. Holt, A. R. Pickard, J. C. Rodger, and D. E. Wildt, eds. Reproductive Science and Integrated Conservation. Cambridge University Press, Cambridge, UK.
Thompson, J. 2012. How many founders does it take to make a breed? The Modern Basenji 2: 26-27.
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