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    Breed-Specific Health Strategies

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  1. Both the article and your statement are very interesting, and I of course fully agree with the IPFD statement. There are two things I would like to underline. First, dog genomics tests goes much beyond health, we should consider also the ones on morphology, population genetics, and potentially behavior and work. Those tools have also clear potential interest for dog breeding, but require standardization as well, in term of approaches, metrics, marker set and so on. Second, it may be interesting to notice, that the growing role of those tools may put the current governance of dog breeding at stake at some point, with the role of laboratory going far beyond the simple role of supply of health test: for instance we could imagine pedigree tools being replaced by equivalent genomic ones at middle/long term.
  2. National Kennel Clubs are major stakeholders in the governance and regulation of dog breeding. As such, they have been the targets of major criticism related to dog health issues. It is therefore interesting to investigate to what extent health and welfare is a priority for kennel clubs (KCs), and what are the capacities and actions implemented to deal with those issues. A survey was sent in 2017 to 40 KCs with 15 answers received from 11 European (Austria, Belgium, Denmark, France, Germany, Ireland, Latvia, The Netherlands, Norway, Sweden and the UK) and 4 non-European countries (Australia, Mexico, Uruguay, and the USA) aimed at describing and comparing information across countries in dog breed health management (Wang et al. 2018). First, in order to determine the population of dogs under the responsibility of KC, the percentages of all dogs being registered as ‘pedigree’ dogs were estimated considering the 15 surveyed KCs, as well 35 other countries, using sources such as the FCI online statistics. Across countries, the average and median percentage of the entire dog population that were registered pedigree dogs, respectively was 20% and 14%. However, there was a large variation across countries, with European Nordic countries showing, in general, a larger proportion of pedigree dogs (see Figure 1). This aspect is of importance, since it is expected that the responsibility toward general dog health, as well as the capacity to improve the situation, relates to the proportion of dogs that are at least to some extent under the influence of the KCs. When asked about the current challenges, KCs ranked exaggerated morphological features and inherited disorders as the most important issues, showing those two problems are now clearly identified as priorities (Figure 2). By contrast, issues such as economic constraints to breeding were rarely viewed as problematic for dog breeding. Kennel clubs also commented on challenges related to the difficulty to find balance between increased regulation and the risk of losing members; to achieve consensus and compliance of breeders and clubs toward breed health strategies; as well as lack of capacity regarding information provision and education. Surveyed countries showed great diversity in terms of information management, implementation of breeding strategies, recommendations, requirement, restriction and tools. Most KCs indicated that information on genealogies, breed standards and dog shows were recorded in their data base for most, if not all breeds; however, health information (e.g. screening examinations, genetic tests) was more sparsely recorded and provided to the public, both for breeds within countries and across countries (Figure 3). For instance, KCs from Austria, Australia, Denmark, France, Germany, The Netherlands, Norway, the UK and the USA provided health information status on pedigrees and in online data bases, but in general, not all breeds were covered. When considering implementation of breeding strategies, six countries indicated that there were no breeding strategies implemented by any breed clubs, while in three countries (Austria, Sweden and the Netherlands) it was reported that each breed club had its breeding strategy. Several countries indicated that they were planning to develop breeding tools and provide health information to users, and for instance, France and Belgium reported having ongoing work to develop tools to provide online pedigree with health information or estimate breeding values for complex disorders such as hip dysplasia. Although limited by the relatively low number of countries considered, this survey showed that despite large differences in their approach to breeding policies and management, the awareness to improve breeding and health of pedigree dogs was strong among the surveyed Kennel Clubs. The dog breeding world is increasingly global in scope. The understanding of both the diversity of health initiatives and the potential for coordinated actions internationally is key to further efforts to promote dog health and welfare. There is probably still a lot of progress to be made in term of information provision and collection, as well as planning breeding strategies considering dog health. In particular, finding a consensus in terms of constraints and priorities for breeding, is expected to be particularly challenging for Kennel Clubs and breed clubs in order to implement those strategies. Although the situations differ across countries, exchanges of experiences may surely help to find the most adequate solutions toward improvement of health and welfare. Reference: Wang, S., Laloë, D., Missant, F. M., Malm, S., Lewis, T., Verrier, E., ... & Leroy, G. (2018). Breeding policies and management of pedigree dogs in 15 national kennel clubs. The Veterinary Journal.
  3. I would clarify some of the question as it may be misleading if interpreted not properly. There are two big issues related to breeding in relation to dog health: the selection of morphological features detrimental to dog health, and the reduction of genetic basis. In your first bullet point about important issue, I would therefore precise that the brachycephalic issue is an illustration of this first problem, otherwise it looks as if brachycephalic breed are the only breeds with morphological issues. Thanks for this interesting post !
  4. This make a lot to read =D... I will try to comment these different posts, as soon as I find some time... Maybe a first question: what about the role of veterinarian for the education of dog owners?
  5. Published a few months ago, a study of Marsden et al. (2016) used whole sequence data of 90 canids to investigate the importance of population bottleneck, inbreeding and artificial selection of the health of the dog. In order to investigate this issue, the authors compared sequences from breed dogs, village dogs, and gray wolves, measuring (i) the proportion of amino acid changing variants, as an indicator of genetic load, and (ii) the number of Mendelian disease genes, considering genes already identified in dogs and human. Several interesting results were found. Based on their measurement of amino acid changing variants (corresponding in general to mutations with deleterious effects), it has been estimated that dogs carry between 2 and 3% more deleterious alleles than wolves, which is comparable to the genetic load in the non-African human population (around 1-3%). This seems surprising, as dog breeds may appear to have undergone more severe bottlenecks during their demographic history than human populations. Also, the authors found that bottlenecks during domestication and breed creation were more responsible of the current genetic load in dogs than recent inbreeding. On the other hand, it appears that genomic regions under selection (also called selective sweeps), were enriched in disease-related genes. This enrichment could be either explained by the fact that genes controlling artificially selected traits in dogs could also confer Mendelian diseases, or to a linkage between genomic regions where disease genes and genes under selection are. On the basis on these different results, the authors concluded that artificial selection incidentally reduced dog fitness. Also, given the fact that repeated population bottlenecks and small effective population size seemed to have more impact on accumulation of weakly deleterious variation than recent inbreeding (i.e., mating between close relatives), the focus should be more on maintaining large population size, than avoiding inbreeding. Given the number of studies that showing the impact of recent inbreeding of fitness and selected traits in dog (Ólafsdóttir and Kristjánsson, 2008; Urfer, 2009, Leroy et al. 2014) or other domestic species (Leroy 2014), I would nevertheless disagree with this last recommendation. It would be therefore be interesting to investigate why the results of this genomic study differ from more phenotype-oriented ones. There are several potential explanations, one being that the traits investigated in those latter studies are under different genetic mechanisms that the one studied here. In any case, we may expect that further studies will confirm, refute or further clarify these first interesting results. References Leroy, G. 2014. Inbreeding depression in livestock species: review and meta-analysis. Animal Genetics 189, 177-182. Leroy G., Phocas F., Hedan B., Verrier E., Rognon X. 2015. Inbreeding impact on litter size and survival in selected canine breeds. The Veterinary Journal. Marsden, C. D., Ortega-Del Vecchyo, D., O’Brien, D. P., Taylor, J. F., Ramirez, O., Vilà, C., ... & Lohmueller, K. E. 2016. Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs.Proceedings of the National Academy of Sciences, 113(1), 152-157. Ólafsdóttir, G.Á., Kristjánsson, T., 2008. Correlated pedigree and molecular estimates of inbreeding and their ability to detect inbreeding depression in the Icelandic sheepdog, a recently bottlenecked population of domestic dogs. Conservation Genetics 9, 1639-1641. Urfer, S.R., 2009. Inbreeding and fertility in Irish Wolfhounds in Sweden: 1976 to 2007. Acta Veterinaria Scandinavica 51, 21.
  6. I remember in the early months of my PhD to have assisted with a seminar by Raymond Coppinger on dog behaviour. At the beginning of his talk, he told the assembly that all comments and contributions would be welcome, providing the participant did not begin with “my dog did…”. Over the last years, I have begun to think that this comment from Coppinger is the perfect illustration of one the biggest misunderstandings between dog breeders/owner and scientists, that I would call the sampling effect. Coppinger's meaning was the following: you cannot make a generalization for the whole species, based on the sole example of your own dog. I think this applies not only to behaviour, but also to a lot of traits related to health. With complex traits, to be able to make generalizations, you need to analyse data on a very large number of dogs… I will take the effect of inbreeding on longevity as an example. How many people have I heard saying “I have known many dogs with high inbreeding that have lived a healthy and long life”? Well, guess what, they are surely right… The preceding figure plots the longevity and inbreeding from more than 6,000 Britanny Spaniel (data from Leroy et al. 2015). This plot is not really impressive by itself. If you consider the five dogs on the right side, with inbreeding close to 40% (remembering that 25% corresponds to a mating between full-sibs), one dog died at the age of 9 years, and four died between 15 and 17 years, the average longevity being around 11 years. So, based on this example, people might conclude that after all, if they can see such inbred dogs live, for most of them, such a long life, then maybe inbreeding does not affect longevity. Well, guess what, they would be completely wrong… Wrong, because of the sampling effect, wrong because when considering complex phenomenon such as inbreeding and longevity, you cannot generalize from a small number of examples. You need a lot of data, not on a few dozen… You need at least several hundred, and if possible several thousand. Applying a simple linear regression of inbreeding on longevity to the same data, the impact is clear: for each 10% increase in inbreeding, longevity decreases by about 1 year. More elaborate models, taking into account the specific distribution of data, breeder or animal effect, confirmed this negative impact (Leroy et al. 2015). But the thing is that, as illustrated by the two figures, longevity is affected by a large number of other factors, related to genetics or environment. This is why it requires a lot of dogs to have an estimation of the global effect of inbreeding on the trait. The individuals cited above were inbred and lived relatively long lives. But they must be considered outliers, in this example, and their experience is not enough to impact the findings for the whole population. By providing this example, my intent is not to criticize the expertise of dog breeders. The message would be more to underline the importance of confronting and sharing one's own experience, to be open to contradictory opinions, and try to gather data and analyse results in all objectivity. In the dog world, we still have a lot of work to do in that extent. References: Leroy, G., Phocas, F., Hedan, B., Verrier, E., & Rognon, X. (2015). Inbreeding impact on litter size and survival in selected canine breeds. The Veterinary Journal, 203(1), 74-78.
  7. As in other domestic species, a large number of traits of selective interest are of complex inheritance, meaning the phenotype expressed by a given individual is determined by an undetermined number of genes, and more or less impacted by its environment. The efficiency of a selection programme on those traits is depending on several factors, including the heritability of the trait, i.e. the part of phenotypic variation which can be related to genetic variation. In livestock species, statistical approaches have been developed and are used to provide estimated breeding values (EBVs), i.e. estimates of the genetic level of an animal, regarding a specific trait. For this, phenotypic measures are taken and combined among related animals to differentiate impact of genes from effect of environment. In dogs, a classical example of complex trait is the extent of hip dysplasia, probably the most common disorder within the species, with incidence above 10% in 45% of breeds according to OFA. A recent literature review of Soo and Worth (2015) investigated the diagnosis and approaches against hip dysplasia across the world. Currently three radiographic schemes are used as clinical diagnosis, namely the FCI one (based on the objective measurement of subluxation using the Norberg angle) in Europe, the BVA (British Veterinary Association) one in UK, and the OFA one in USA, based on subjective criteria. The figure below provides estimates of heritabilities reported in the above study. Whatever the system chosen, heritabilites have been estimated above 0.15 in most breeds, indicating that adequate breeding programmes should improve the status of breeds relative to hip dysplasia. What about efficiency of breeding programmes and EBVs? Despite the fact some EBVs have been already developed a long time ago in Germany for the German shepherd dog, most of the selection has been based until now on the basis of radiographic screening, i.e. the phenotype of the dogs. Different retrospective studies have observed only limited progress over the last years, despite more than 40 years of screening. Using the OFA data base, Hou et al. (2013) estimated that between 1989-2003, a limited genetic improvement has been observed, equivalent to 16.4% of the phenotypic standard deviation. For the UK, Lewis et al. (2010) has observed a 13% improvement in hip scores over the 10-year study period. However, pre-screening by owners, effectively removing information from the worst-affected animals and resulting in only better radiographs being shared/ recorded, has been viewed as a strong bias, being one of the main factors incriminated for such a limited progress. [Editor's note: this is less of a problem in registries where hip dypslasia screening is mandatory for all dogs used in breeding, e.g. Sweden and Finland. See link below.)] This has led specialists to recommend the use of EBVs instead of phenotypic evaluation solely, as the EBV allows a more accurate identification of dogs with more healthy genetic status. Different studies (Lewis et al. 2010, Malm et al. 2013) has estimated that a selection based on EBVs should improve the genetic progress on hip dysplasia by around 20%. Consequently, in the last years, several countries such as Sweden and UK have proceeded to the implementation of EBVs in their breeding scheme. In that extent, the recent blog post of Katarina Mäki on the genetic progress against hip dysplasia since the implementation of EBV in Finland in 2002 is quite instructive. And other traits? Hip dysplasia is certainly not the only trait for which EBVs could have some use. For elbow dysplasia, for instance, EBVs are also computed in the Mate Select tool of UK Kennel club. The recent study of Lappalainen et al. (2015) on intervertebral disc calcification in Dachshunds in Finland provides another interesting example of this. With heritability around 0.5, there is clear indication of potential genetic progress on the trait, the improvement over the last years having been limited, in relation to the fact that only 10% of dogs have screening. It appears that the Finnish Kennel Club hopes to develop EBV on the disease for its breeders, which may be expected to increase the genetic progress relative to this disease. Regarding behavioural traits, use of EBVs could be a way to improve the selection of dogs. However, as underlined in a previous post, the generally low heritability of those traits, rarely higher than 15%, may constitute a serious limitation to genetic progress. And in the future? Of course, one important opportunity in the future is related to the use of genomic information in relation to complex traits. In livestock species, a growing number of traits, usually estimated through classical EBVs, are now estimated through genomic selection, largely improving accuracy. This requires however a large reference population and a good knowledge of the genome of the species. Taking the example of hip dysplasia, several candidate genes have been identified with potential impact on hip dysplasia (Soo et al. 2015). In the future, it may be expected that genomic information could be used either to support classical EBV estimation (marker-assisted selection) or even replacing it (genomic selection). This would allow, among other benefits, to provide an estimate of breeding values at an earlier age, differentiating litter mates based on their respective genome. The technic would however need further improvement before any implementation. References Hou, Y., Wang, Y., Xuemei Lu, X., Zhang, X., Zhao, Q., Todhunter, R. J., & Zhang, Z. (2013). Monitoring hip and elbow dysplasia achieved modest genetic improvement of 74 dog breeds over 40 Years in USA. PloS one, 8(10), e76390. Lappalainen, A. K., Mäki, K., & Laitinen-Vapaavuori, O. (2015). Estimate of heritability and genetic trend of intervertebral disc calcification in Dachshunds in Finland. Acta Veterinaria Scandinavica, 57(1), 1-6. Lewis, T. W., Blott, S. C., & Woolliams, J. A. (2013). Comparative analyses of genetic trends and prospects for selection against hip and elbow dysplasia in 15 UK dog breeds. BMC genetics, 14(1), 16. Malm S, Sørensen AC, Fikse WF, Strandberg E. (2013) Efficient selection against categorically scored hip dysplasia in dogs is possible using best linear unbiased prediction and optimum contribution selection: a simulation study. Journal of Animal Breeding and Genetics 130, 154–64. Soo, M., Sneddon, N. W., Lopez-Villalobos, N., & Worth, A. J. (2015). Genetic evaluation of the total hip score of four populous breeds of dog, as recorded by the New Zealand Veterinary Association Hip Dysplasia Scheme (1991–2011).New Zealand veterinary journal, 63(2), 79-85. Wilson, B. J., Nicholas, F. W., James, J. W., Wade, C. M., Tammen, I., Raadsma, H. W., ... & Thomson, P. C. (2012). Heritability and phenotypic variation of canine hip dysplasia radiographic traits in a cohort of Australian German shepherd dogs. PloS one, 7(6), e39620.
  8. For most dog breeders, behavior represents a major challenge. It is indeed one of the main fields of interest in terms of breeding. In a survey we made with French breeders a few years ago (Leroy et al. 2007), behavior was ranked as a breeding goal after morphology, but before health and work. Yet, although the influence of genes on behavioral traits, which are illustrated by the large behavioral differences between breeds, cannot be denied, those traits are also largely impacted by education and environment, which makes selection of those traits difficult. A recent study (Hradecká et al. 2015) tried to make a reappraisal on the heritability of behavioral traits in dogs, i.e. of the proportion of behavior variation that can be attributed to genes. For this 1763 heritability estimations from 48 studies were gathered in a meta-analysis study, traits being classified into five categories: Environment interaction, herding, hunting, play and psychical characteristics. As showed in the following table, whatever the categories, heritabilities were found to be low, ranging between 9 and 15%. In other words, according to this study, depending on trait categories, around 9-15% of within breed observed variability could be explained by gene differences. Heritability of traits for different categories according to Hradecká et al. (2015) meta-analysis Category Heritability Environment interaction 0.154 Herding 0.099 Hunting 0.154 Play 0.093 Psychical characteristic 0.123 This low heritability has several consequences relative to breeding and welfare issues. First, it underlines the importance of education. It is of course not a surprise, but when coming to behavior, breeders should rely more on their capacity at providing an environment optimal for the behavioral development of the puppies than to genetics. Secondly, improving the behavior of a breed through selection is not going to be an easy task. Two shortcuts may, however, be considered. First, if the improvement of behavior of the breed is an absolute necessity, maybe the genes of interest can be found outside the breed. Heritabilities are, indeed, in general estimated within breeds, so they do not take into account differences across breeds. It may also be wondered if genomics could be of some help. Given the complexity of behavioral traits, it is expected that even the small proportion of variability which is genetic involves a large number of genes, possibly with small and indirect effects. Yet in the last years, several studies have been able to identify gene variants impacting behavior. Some examples: In Belgian Shepherd breed, Lit et al. (2013) identified a mutation in dopamine transporter gene, single copy carriers showing seizures, loss of responsiveness to environmental stimuli, episodic aggression, and hyper-vigilance. When considering disorders related to behavior, several genes have been identified to underlie some inherited forms of epilepsy (see Ekestedt et al. 2013). A recent comparative analysis between pointing and non-pointing dog breeds allowed researchers to identify two gene candidates that could contribute to pointing behavior in hunting dogs (Akkad et al. 2015).In German Shepherd Dogs, a Chinese study (Yang et al. 2015) has linked the genotypes for some olfactory receptors to the olfactory ability of those dogs. Although interesting, it may be argued that some of these findings (e.g., for instance, the last one) do not directly relate to behavior. But actually, the behavior is connected to a wide range of morphological and physiological mechanisms, and it may be expected, for instance, that olfactory capacity impacts the environment interaction and hunting capacities of dogs. It is, however, important to underline that results should always be replicated and confirmed, especially if there are conflicting findings. Also, results may only be of interest or applicable to some breeds or populations. Nevertheless, it may be expected that in the next years, some gene test(s), more or less relevant, will be developed for selection on behavior. As for all other developments in diagnostic molecular genetics, the test(s), their validity, potential impact and application within breeding strategies will need to be carefully considered. References: Akkad, D. A., Gerding, W. M., Gasser, R. B., & Epplen, J. T. (2015). Homozygosity mapping and sequencing identify two genes that might contribute to pointing behavior in hunting dogs. Canine Genetics and Epidemiology, 2(1), 1-13. Ekenstedt, K. J., & Oberbauer, A. M. (2013). Inherited epilepsy in dogs. Topics in companion animal medicine, 28(2), 51-58. Hradecká, L., Bartoš, L., Svobodová, I., & Sales, J. (2015). Heritability of behavioural traits in domestic dogs: A meta-analysis. Applied Animal Behaviour Science, 170, 1-13. Leroy, G., Verrier, E., Wisner-Bourgeois, C., & Rognon, X. (2007). Breeding goals and breeding practices of French dog breeders: results from a large survey. Revue de Médecine Vétérinaire, 158(10), 496. Lit, L., Belanger, J. M., Boehm, D., Lybarger, N., Haverbeke, A., Diederich, C., & Oberbauer, A. M. (2013). Characterization of a dopamine transporter polymorphism and behavior in Belgian Malinois. BMC genetics, 14(1), 45.
  9. I fully agree with you about the difficulty to change breed standards, I have only limited knowledge at it, but I heard that depending on breeds and their origins, the precision and place that is let for interpretation vary a lot, which would probably impact the efficiency of a change in standard. Relatively to your last question on where could the dogs improving the dog morphology come from, as a geneticist, I would answer this would depend of the gene pool on the breed, as well as the genetic complexity of the trait. Just supposing the inheritance of your trait is polymorphic and you have a large population, it should be possible to select toward a better morphology, even if currently no dogs are showing the phenotype your require. In cattle, some breeds produce currently 10,000 litter per years, largely due to selection, while 50 years the production was less than half of this. Yet the less simple in your trait inheritance, and the smallest in your population, the less chance you will have to make things move without relying on crossbreeding. In the case of skull shape, I think several candidate gene have been identified, which may help in selecting or introgressing some alleles of interrest in future, with development of adequate genetic tests... Schoenebeck, J. J., & Ostrander, E. A. (2013). The genetics of canine skull shape variation. Genetics, 193(2), 317-325.
  10. This makes me remember that in the XIXth century, the main association for animal welfare in France (SPA Societe Protectrice des Animaux) supported horse meat consumption (Pierre, 2003, L’hippophagie au secours des classes laborieuses, Communications, 74:177-200.), for the same very reasons that make some people currently support horse slaughter in USA...
  11. Selection on exaggerated morphological features is probably one of the most important problem facing purebred dogs, one of the difficulties being to identify precisely how those morphological traits are affecting the health of the dogs. The recent study of Packer et al. (2015) however provides a very interesting example and suggestions on what could be done relative to the brachycephalic issue. It indeed illustrates nicely how Brachycephalic Obstructive Airway Syndrome (BOAS), a chronic debilitating syndrome seen frequently in brachycephalic dogs, is connected, in a non-linear manner, with the shortening of muzzle length. According to this study BOAS occurred only in dogs whose muzzle length was less than half the cranial length. A majority of dogs which had this craniofacial ratio lower than 0.2 were found to be affected. The study found also that thick neck girth, obesity and neutering increased the risk for BOAS. With this craniofacial ratio, breed clubs now have a good indicator that could be used to reduce the incidence of this condition. It is clear that some good work could be made through the promotion of dogs with longer muzzle or even, inserting some condition on this ratio into the standard. As shown in the article, for some breeds, such as the Japanese Chin, it would probably be difficult to improve this ratio to needed values relative to BOAS but efforts have to be made any way, using crossbreeding if necessary. If stakeholders from the dog world do not move on this, it is clear that, at some point, some one else will, and it won’t necessarily be for the good of their breeds. References: Asher, L., Diesel, G., Summers, J. F., McGreevy, P. D., & Collins, L. M. (2009). Inherited defects in pedigree dogs. Part 1: Disorders related to breed standards. The Veterinary Journal, 182(3), 402-411. Packer, R. M., Hendricks, A., Tivers, M. S., & Burn, C. C. (2015). Impact of Facial Conformation on Canine Health: Brachycephalic Obstructive Airway Syndrome. PloS one, 10(10), e0137496. Credit picture: I. Horvath
  12. Interresting... do you have some knowledge of organizing structure?
  13. That's the kind a study that can help to support breeding policies toward more healthy dogs. I would like to have opinion of specialist of morphology on it...
  14. Of course you can link it . I think for breeders it may provide useful information on their breeds, the problem being that interpretation may be sometimes difficult. Information of progeny distribution can give idea on what efforts should be made to have a more balanced use of reproducers at the kennel scale. If the sires of a given breeders provide on average 40 dogs, while the mean is the breed is 15, maybe the breeder should think about enlarging the number of sire he use for instance. In the case of Bernese Mountain Dog, the impact of importations is obvious for me, as both observed and expected inbreeding are decreasing. Indeed, it is probable that especially after several generations of importations, there is a bias in the absence of kinship measured in the freshly imported dogs.
  15. Thanks for your feedback ! I would tend to think that one good judge on this would be the comparative increase of kinship (their expected inbreeding). If kinship also stabilized I would bet more on importations, otherwise it could be indeed change in breeding practice. In the two examples here I would guess you are probably right. In other cases (Bearded collie I would not be so sure. Fully agree also that the links between effective population size and breed health should be clarified. That does not mean it has no interest . Same thing for outcrossing: the more we will have of successful examples, the more people will be open to it as a tool.
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