Heritability Estimates of Behaviors Associated With Hunting in Dogs

Heritability Estimates of Behaviors Associated With Hunting in Dogs S. M. Schmutz and J. K. Schmutz Heritabilities of traits related to game-bird hunting, measured in the natural ability test of the North American Versatile Hunting Dog Association (NAVHDA), were calculated using midparent offspring regressions for five breeds of continental hunting dogs. Heritabilities of use of nose, search, and waterwork were moderate (0.25 0.39). Heritability of pointing was high ( 0.40) in one breed but only moderate in the combined dataset. Desire, cooperation, and tracking were not significantly correlated between midparent average and offspring. One of the breeds, large munsterlander, was analyzed for improvement over the past 15 years. The NAVHDA testing system is used to select breeding stock in the large munsterlander and improvement in scores was significant. From the Department of Animal and Poultry Science (SM Schmutz) and the Department of Biology (JK Schmutz), University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B5, Canada. We wish to thank Roberta Applegate and the North American Versatile Hunting Dog Association for sending us computer printouts of natural ability test scores. We also thank Lawrence Heinrich, David Nairn, and Lori Schwab for help in data entry. Our gratitude goes to Jan Smith, Roy Crawford, and Max Rothschild for comments on an earlier draft of this manuscript. 1998 The American Genetic Association 89:233 237 Breeding the best to the best is an adage that has withstood the test of centuries. Judging from ancient carvings depicting hunting scenes, recognizable hunting dogs, and hence presumably their deliberate selective breeding, occurred over 4000 years ago (Schulze 1965). The oldest known record of a domesticated dog is based on a mandible showing the characteristics of domestication found in a cave dated 14,000 B.P. (Clutton-Brock 1995). Evidence of an association between early hominids and wolves is much older still, dated at 300,000 B.P. in north China and 400,000 B.P. in England (Clutton-Brock 1995). Our purpose in this article is to explore how appropriate the above adage is for modern breeds of versatile hunting dogs used and bred in North America in terms of hunting behaviors. Although heritabilities are reported for most of the important production traits in livestock species, few such estimates are available for dogs. One study of conformation characteristics in shepherd dogs in South Africa ( Verryn and Geerthsen 1987) showed that various body measurements of the dog had heritabilities in the range of 0.32 to 0.81. Even fewer estimates are available for behavioral traits in general and for dogs in particular. On a larger scale, the existence of a variety of dog breeds that exhibit consistent and largely unique behavioral traits (e.g., trailing, herding, protection) is classic evidence for the heritability of behavior (Scott and Fuller 1965). A recent report on Finnish spitz and English setters suggested that most hunting behaviors had low heritabilities when the authors calculated h 2 using paternal half-sib regression ( Vangen and Klemetsdal 1988). We attempted to extend the types of hunting behaviors studied in five breeds and to analyze the results of selection programs based on such performance testing in one breed. We speculate on the possibility that the pointing trait exhibited by several hunting breeds may have two different origins: (1) a prolonged halt before the pounce exaggerated through artificial selection, and (2) a pointing stance which appeared spontaneously and much earlier in chasing dogs. We believe that the mode of inheritance in these functionally similar but apparently different behaviors may influence heritability estimates. Materials and Methods We examined heritability of hunting traits in some hunting dog breeds that point, track, and retrieve birds on land and water. The data were kindly provided by the North American Versatile Hunting Dog Association (NAVHDA). This is a testing organization whose aims and practices make the data well suited for analysis (NAVHDA 1993). This organization offers three performance tests natural ability, utility preparatory, and utility but only the first was used in these analyses. The tests are noncompetitive such that each dog is evaluated against a prescribed standard. A 233

Table 1. Selected criteria that are used by judges to evaluate the performance of dogs in the field relative to maximum and minimum scores typically given in that category Trait Score Judging criteria Use of nose 4 Dog repeatedly gives indication of the location of scent left behind by a running bird whose course was observed by the judges; dog scents game at considerable distance; dog checks old scent briefly and moves on quickly; dog finds high proportion of the planted birds. 1 Converse of above. Also dog points but bird cannot be found. Search 4 Dog s purposeful demeanor suggests eagerness to find game; dog moves at pace matched to density of plant cover and wind conditions. 1 Converse of above. Also dog unwilling to move out from proximity of handler. Retrieve from water 4 Dog enters water directly and swims twice in a row in response to a canvas or plastic retrieving dummy and encouragement by the handler. A medium score of 1 2 is given if a dead bird is required to entice the dog into the water. 0 Dog refuses to enter water or refuses on second throw. Pointing 4 Dog establishes an intense posture for at least 2 s upon scenting but not seeing a bird. When dogs point more than once, performance is averaged but the best performance is given extra weight. 0 Dog scents a bird but shows no hesitation and causes it to fly or captures it. Tracking 4 Dog marks the bird s track repeatedly and apparently persists in using such scent to locate a running bird. 0 Dog marks scent of bird at least once but shows no intention of using such scent to guide its course of running. Desire to work 4 Dog s demeanor suggests that it intends to absolve all tasks to the best of its abilities. 1 Converse of above. Also dog is fearful of birds; dog exhibits prolonged comfort behaviors instead of hunting. Cooperation 4 Dog maintains visual contact and adjusts its search to the route taken by the handler without showing signs of not cooperating to find game for the handler. Simple obedience (e.g., coming when called) is not expected of dogs in this test of natural ability. 1 Dog leaves area to hunt on its own. primary purpose of these tests is to provide an indicator of performance to aid dog breeders in their choice of breeding stock and dog buyers in selection of pups. Tests are conducted throughout North America, principally in spring and fall for that region but in effect throughout the calendar year. The natural ability test is designed to evaluate a young dog s (16 months or younger) natural inclination to hunt. Each dog is judged on how it performs certain prescribed tasks, including searching independently for game, pointing galliform birds which are planted in the running Table 2. Mean scores of pups in each category of the NAVHDA natural ability test out of a possible 4 points (112 for total score) and their standard deviations Trait Nose Search Waterwork Pointing Tracking Desire Cooperation shorthaired (n 80) 3.31 0.77 3.32 0.82 3.61 0.12 3.28 1.18 2.78 1.35 3.06 0.89 3.14 0.79 wirehaired (n 99) 3.27 0.76 3.08 0.88 3.53 0.94 3.28 1.22 2.77 1.34 2.98 0.84 3.04 0.84 Griffon (n 75) 3.17 0.76 2.81 1.08 3.49 1.11 3.22 1.22 2.80 1.24 2.85 0.96 2.95 0.85 Large munsterlander (n 86) 3.28 0.77 3.02 0.93 3.59 0.84 2.68 1.44 3.17 1.16 3.11 0.89 3.09 0.79 Pudel (n 144) 3.34 0.66 3.25 0.80 3.48 1.00 3.64 0.79 2.75 1.28 3.24 0.74 3.01 0.75 Weighted a total score 90.93 18.5 89.44 18.4 86.22 20.7 88.42 20.11 92.63 14.8 a Weights for the traits are nose 6, search 5, waterwork 5, pointing 4, tracking 2, desire 4, cooperation 2. field, retrieving from water, and following the track of a released pheasant (Phasianus colchicus). In addition, other aspects are judged throughout the test, including a dog s use of nose for scenting game, its desire to hunt, and its willingness to cooperate with the handler. Use of nose, for example, is evaluated by the number of birds found, the distance at which these are located, the demeanor of the dog in search, and whether it uses its nose to guide the search or simply runs aimlessly. We used data from the natural ability test rather than the higher level tests because in natural ability a young dog s performance is least influenced by training or exposure. In the natural ability test handlers are discouraged from influencing a dog s performance and only a minimum of commands and coaching is allowed. Each dog is judged by a team of three approved judges for at least 40 min of intensive observation during the three tasks: searching and pointing, retrieving, and tracking. Reported scores are reached by consensus. Judges undergo an apprenticeship for a few years and refresher courses every 3 years to maintain standardization in the judging system. Judges hunt with versatile dogs and must continue to run dogs in the tests as handlers on a periodic basis. All judges receive annual updates of testing information for their manual, from which criteria used for judging the various traits are excerpted ( Table 1). A dog s performance is scored from 0 to 4 in each category, although 1 is the lowest score typically given in some categories (Table 1). To rank a dog s overall performance and to give credit to the more valued traits, each score is then multiplied by a weighted index number ( Table 2) (NAVHDA 1993). We examined data from 1455 dogs, in 485 families of pup-sire-dam. The dogs were from five breeds, including 80 shorthaired s, 99 wirehaired s, 75 wirehaired pointing griffons, 87 large munsterlanders, and 144 pudels. Data for large munsterlanders were from dogs tested between 1977 and 1996 and for other breeds from 1983 to 1992. For the few dogs which were run more than once, we used only the best score. We believed midparent offspring regression to be the most appropriate method (Falconer 1976), and only used scores from dogs that had both parents entered in NAVHDA tests. Midparent offspring regression was used to calculate heritabilities (r h 2 ), with midparent calculated as the average score of the two parents ( Falconer 1976). Age and sex of the pup were used as additional variables in the regression analysis. Standard errors for heritability estimates were calculated using the formula (Falconer 1976): sampling variance. Sampling variance 1/(number of parents 2) [(variance of the parents/variance of the offspring) r 2 ]. In some analyses only the large munsterlander dataset was used because we had more complete information on this breed. Large munsterlander scores were plotted over the last several years with matched control dogs, that is, a dog of another random breed that ran in the same 234 The Journal of Heredity 1998:89(3)

Table 3. Heritabilities of hunting traits measured in the NAVHDA natural ability test based on midparent and offspring regressions, corrected for age and sex of the pup Trait Nose Search Waterwork Pointing Tracking Desire Cooperation shorthaired 0.35 0.11* 0.48 0.07* 0.13 0.01 0.25 0.22 0.48 0.09* 0.31 0.12* 0.22 0.12 wirehaired 0.32 0.12 0.31 0.10* 0.32 0.28* 0.13 0.22 0.14 0.12 0.14 0.10 0.34 0.11* Griffon 0.33 0.08* 0.18 0.12 0.30 0.10 0.13 0.09 0.13 0.08 0.21 0.10 0.06 0.09 0.19 0.12 0.19 0.11 0.24 0.16 0.31 0.11* 0.80 0.10 0.22 0.11 0.25 0.11 Large munsterlander Pudel 0.19 0.07* 0.12 0.08 0.31 0.09* 0.10 0.15 0.17 0.06 0.05 0.08 0.09 0.07 Overall 0.02 0.04 0.19 0.05* 0.17 0.07* 0.18 0.08* 0.07 0.06 0.10 0.05 0.13 0.04* Weighted total score 0.35 0.13* 0.27 0.14 0.22 0.10 0.33 0.13* 0.08 0.08 0.09 1.13 * Significant at the 95% level. test, to see if there was breed improvement in performance over time. Large munsterlanders were used because testing is mandatory in this breed prior to breeding and is used as a selection criterion; only dogs which pass are bred. Most handlers ran a pup only once or twice, but a small number of handlers ran many pups. Natural ability scores of dogs run by handlers who had run at least three dogs were analyzed relative to their consecutive running order by that handler to try to estimate the effect of experience of the trainer on pup performance. Results The mean scores and standard deviations for 485 pups of five breeds for which we also had test records for both parents are listed in Table 2. The standard deviations varied considerably among traits. In some traits (use of nose, search, desire, and cooperation) zeros were rarely if ever given, in contrast to other traits where zeros were relatively common. Heritabilities based on 485 offspring/ midparent regression coefficients are shown in Table 3 by breed and for the combined dataset across breeds. A multiple regression was run to account for the age and sex of the pup. Use of nose, search, waterwork, cooperation, and total score showed a significant heritability in at least two of the breeds tested ( Table 3). Heritabilities were low to moderate in all cases, except for searching and tracking in shorthaired s where it was high ( 0.40). No significant heritability for desire or tracking was found in any breed except shorthaired s, where they were moderately heritable. The natural ability test is meant to judge young dogs who have had relatively little training but some hunting exposure. Nevertheless, training may be an important variable. To address the effect of training we used 203 scores of pups whose handlers had run at least three dogs in natural ability tests. The regression of which dog in the series run by a handler (i.e., first or third or tenth) and total score was not significant (r 0.12, P.09), although a slight trend existed ( Figure 1). Repeatability is another measure that is often used as an indication of how heritable a trait is. Twenty-eight dogs were run twice or more, but the correlation between their two consecutive scores was not significant (r 0.02, P.92). Dogs run a second time in this test are not a random sample however, so this is not surprising. Some dogs that do not do well the first time are given more training and entered again, since a passing score for this test is required by some breed clubs prior to breeding. Using selection following the NAVHDA scoring system, the total score of the 137 large munsterlanders born in North America which were run in the natural ability test increased over the years (Figure 2a) (r 0.18, P.03), indicating phenotypic improvement. Matched controls of pups of other breeds run in the same test did not show this improvement over time (r 0.02, P.81) (Figure 2b), indicating that the effect is not due to test standards becoming easier. Discussion Moderate heritability of use of nose, search, waterwork, and cooperation can be assumed since data in at least two different breeds showed significant results. Vangen and Klemetsdal (1988) found a heritability of 0.11 for bird finding ability and 0.17 for searching ability in Finnish spitz. Use of nose with head held high, that is, high-style, as in English s is thought to be dominant over the style of several continental breeds, such as large munsterlanders and wirehairs, where the nose is lower to the ground and as sensitive to ground scent as airborne scent (Marchlewski 1930; Whitney 1932). This was based on crosses of English s and bloodhounds. Whitney (1932) concluded that water love was inherited as a dominant from crosses of Newfoundlands and bloodhounds. Such older studies tried to force behavioral patterns into Mendelian modes of single-gene inheritance which are probably not appropriate, but the data do suggest heritability. Krushinski (1962) suggested that the instinct to retrieve was heritable. The standard errors of the estimates of heritability for pointing were quite high (Table 3) which may be related to different origins of this behavior. Pointing is believed to have been developed as an overemphasized pause in the stalk of game which was encouraged by training and selected by breeders. Setters were a specialist branch of s that were selected for their low-lying posture during pointing so that a net could be thrown over them to catch the birds. Simultaneously an acute sense of smell was selected for to maximize the finding of game. Whitney (1932) described that pointing was not completely dominant to moving in on game in the F 1 when crossing a pointing breed to a Newfoundland or bloodhound. Somewhat surprisingly, the heritability estimate for tracking was significant in only one of the breeds tested. Midparent offspring regressions were all very low. Mean scores for tracking were not high. It is possible that there is minimal variation in this trait for selection to act upon. Tracking is primarily used in bird hunting for crippled birds. Several classic studies examined tracking behaviors in dogs. Baying on trail is characteristic of certain breeds such as hounds. There is disagreement in the literature over the inheritance pattern of this trait. Marchlewski (1930) states that silent is dominant over loud on trail, but Whitney (1932) says the reverse. Neuhaus (1957) found differences in the olfactory threshold to butyric acid among different breeds. Whitney (1955) believed tracking ability was related more to a dog s determination to persist than olfactory abilities. Schnitzer et al. (1962) support this with data from repeated trials on rabbit tracks of beagles, basenjis, Shetland sheepdogs, and wire-haired fox terriers. The beagles had the best performance throughout, whereas the terriers improved performance. Although only shorthaired s showed a moderate heritability Schmutz and Schmutz Heritability of Traits in Dogs 235

Figure 1. Scattergram, with regression line, of the scores of dogs run in natural ability relative to the order in a series run by a handler to attempt to address the effects of training. for desire in this study, English setters also had a moderate heritability (0.22) ( Vangen and Klemetsdal 1988). Methods of Analysis Midparent offspring regression is considered a powerful measure of heritability (Falconer 1976) and its use in this study lends credibility to the heritabilities found. A recent analysis of hunting behavior data on Finnish spitz was analyzed by a similar method ( Vangen and Klemetsdal 1988) and by an animal model approach using restricted maximum likelihood (REML) ( Karjalainen et al. 1994). The REML analysis did not find significant heritabilities for most traits, but the more traditional, half-sib regression analysis did. Evolution of Hunting Behaviors As a background to a study of the inheritance of behaviors, it may be pertinent to consider the evolution of such behaviors. Some behaviors exhibited by modern hunting dogs may be actions that were part of the behavioral repertoire of ancestors; other actions may be largely the result of artificial selection. A search for prey was presumably common among canine ancestors. However, the speedy and energetically expensive search pattern exhibited by many modern pointing dogs seems not to be observed in nature (Lulack J, personal communication). Similarly, while retrieving (for provisioning young or in play) may be expected of canine ancestors, the soft mouth retrieve of a meal-deprived hunting dog has probably been influenced by artificial selection. Hoarding food by burying (Henry 1986) is apparently common in wild canids, but has been effectively selected against in retrievers. Budiansky (1992) provides convincing reasoning to suggest that the ancestral canines themselves indirectly initiated the process of domestication. A modern-day parallel may be commensals, such as the rock dove (Columba livia) and the house mouse (Mus domesticus), that have evolved their patterns of existence such that they depend on rural or urban environments. Thus such a loose association may have been the precursor for domestication and this could explain why certain animals were readily domesticated while others were not. Similarly the practice of harvesting game birds over a pointing or setting dog was probably not conceived by humans without first observing the dogs own stalking action. We suspect that the pointing trait may have two origins. This diverse origin may affect heritability estimates. Pointing behavior is frequently viewed as a prolonged halt immediately preceding a pounce (Lorenz 1953). The ancestral halt was presumably exaggerated through artificial selection. The crouched stance with head and tail held low supports this interpretation. Such a pointing style is exhibited by many pointing dogs of mainly European continental origin. English s and setters exhibit the second type of pointing, a proud stance on point, with tails erect and heads high. This style of pointing is also frequent in those breeds of continental versatile dogs that have experienced a considerable infusion of English and setter genes. The English was derived from a Spanish forerunner that was imported to y as early as 1467 (Eggert 1984) and the British Isles about 1600 (Shaw 1984). This dog presumably originated in the Middle East and/or northern Africa. As early as about 400 B.C., according to the Greek historian Xenophon, and about 100 A.D., according to the Roman Plinius the Second, pointing was part of the behavioral repertoire of some dogs (Schulze 1965). Xenophon describes a hound pointing a rabbit as an anomalous behavior, suggesting that this behavior was not purposefully selected for. If pointing indeed has two origins, this genetic heterogeneity may lead to an underestimation of heritability values. Kreiner et al. (1992) studied heritabilities of Austrian dog breeds that specialize in tracking and flushing and found low heritabilities of most traits using parent-offspring regressions. They did not find significant heritabilities when they analyzed several different breeds simultaneously but did find a few significant heritabilities when the breeds were analyzed separately. This problem was not so pronounced in our dataset, which suggests that these five breeds are very similar to each other. This is supported by the similarity of mean scores across the breeds (Table 2). Traits that showed significant heritabilities in two breeds also did so in the combined breed analysis, with the exception of use of nose, which did have wider variance in mean scores across the breeds. It would appear that genetics are important, in fact critical, for some traits such as use of nose to find game. Selection schemes on the basis of scores such as those resulting from testing systems such as NAVHDA s should allow dog breeders to maintain and improve such traits ( Figure 1). The generally low to moderate heritabilities for hunting dog behaviors recorded in this ( Table 3) and other studies probably reflects the advanced state of development in these breeds. Through centuries of selection, genetic variability may have been much reduced, giving propor- 236 The Journal of Heredity 1998:89(3)

Figure 2. (a) Scattergram, with regression line, of all of the scores of large munsterlanders run in natural ability illustrating improvement over time. (b) Scattergram of scores of a matched pup of any other breed run in the same test, illustrating that testing standards did not decrease over time. tionately greater powers in variance analyses to environmental influences. This is consistent with the predictions made by Falconer (1976) and the observations of Dudley (1977) after long term selection for oil and protein in corn. A large proportion of improvement in hunting dog performance can be achieved through training, thereby molding environmental influences on dog behavior. References Budiansky S, 1992. The covenant of the wild. New York: William Morrow. Clutton-Brock J, 1995. Origins of the dog: domestication and early history. In: The domestic dog its evolution, behaviour, and interactions with people (Serpell J, ed). Cambridge: Cambridge University Press; 7 20. Dudley JW, 1977. 76 generations of selection for oil and protein percentage in maize. In: Proceedings of the international conference on quantitative genetics (Pollack E, Kempthorne O, Bailey TB, eds). Ames, Iowa: Iowa State University Press; 459 473. Eggert B, 1984. Die Jagd in Bayern: von der Vorzeit bis zur Gegenwart. Rosenheim, y: Rosenheim Verlagshaus Alfred Förg GmbH. Falconer DS, 1976. Introduction to quantitative genetics. London: Longman. Henry DJ, 1986. Red fox: the catlike canine. Washington, D.C.: Smithsonian Institute Press. Karjalainen L, Ojala M, Vilva V, 1994. Estimates of heritability for measures of hunting performance in the Finnish spitz. Proceedings of the 5th World Congress of Genetic Applications in Livestock Production, Guelph, Ontario, Canada; 165 168. Kreiner M, Stur I, Mayhofer G, Muller S, 1992. Heritabilität und Merkmalskorrelationen von Verhaltensmerkmalen bei vier österreichischen Brackenrassen. J Anim Br Genet 109:425 432. Krushinski LV, 1962. Animal behaviour: its normal and abnormal development. New York: Consultants Bureau. Lorenz K, 1953. Man meets dog. Harmoundsworth, England: Penguin Books. Marchlewski T, 1930. Genetic studies on the domestic dog. Bull de l Acad Polon des Sciences et des Lettres. Série B: Sciences Naturelles (II):117 145. NAVHDA, 1993. NAVHDA aims, programs and test rules. Arlington Heights, Illinois: North American Versatile Hunting Dog Association. Neuhaus W, 1957. Unterschiede in der Riechschärfe bei Hunden. Z Vergl Physiol 40:65 72. Schmutz JK, 1992. Roots of the versatile hunting dog in history. Gun Dog Oct/Nov:89 92. Schnitzer SB, Fuller JL, Schnitzer ME, 1962. Breed differences in locating hidden persons and animals (abstract). Am Zool 2:446. Schulze H, 1965. Jaghunde-einst und jetzt. Hannover, y: Landbuch-Verlag. Scott JP and Fuller JL, 1965. Dog behavior the genetic basis. Chicago: University of Chicago Press. Shaw V, 1984. The classic encyclopedia of the dog. New York: Bonanza Books. Vangen O and Klemetsdal G, 1988. Genetic studies of Finnish and Norwegian test results in two breed of hunting dogs. Proceedings of the VI World Conference on Animal Production, Helsinki, Finland. Verryn SD and Geerthsen JMP, 1987. Heritabilities of a population of shepherd dogs with a complex interrelationship structure. Theor Appl Genet 75:144 146. Whitney LF, 1932. Inheritance of mental aptitudes in dogs. Proc Sixth Int Cong Genet 2:211. Whitney LF, 1955. Bloodhounds and how to train them. New York: Orange Judd. Winge O, 1950. Inheritance in dogs with special reference to hunting breeds. Ithaca, New York: Comstock Publishing. Received January 21, 1997 Accepted July 10, 1997 Corresponding Editor: Bruce S. Weir Schmutz and Schmutz Heritability of Traits in Dogs 237