Genetic Diversity of a Closed Population of Japanese Black in Hyogo Prefecture

Takeshi HONDA, Tetsuro NOMURA1, Moriyuki FUKUSHIMA2 and Fumio MUKAI

Faculty of , Kobe University, Nada-ku, Kobe-shi 657-8501, Japan Faculty of Engineering, Kyoto Sangyo University, Kita-ku, Kyoto-shi 603-8555,1 Japan Hyogo Prefectural North Insitute of Agriculture, Wadayama-machi, Hyogo-ken 669-5254,2 Japan

(Received March 1, 2001; Accepted June 15, 2001) Abstract The Japanese Black in Hyogo prefecture has been almost closed population. In this paper, genetic diversity of the population was estimated. The materials used were 68,781 animals born in 1955 to 1998 and their pedigree records traced back to the population in 1937 or before. To assess the diversity, three types of parameters were estimated. Founder genome equivalents (Nge) is the most comprehensive parameter, in which all the causes of the reduction of diversity are accounted for. Effective number of founders (Nef) explains the cause of reduced diversity due to unequal contributions of founders. Effective number of non-founders (Nenf) accounts for the diversity reduced by genetic drift accumulated over non-founders generations. Index of genetic diversity (GD) was estimated by GD=1-1/(2Nge). Nge decreased gradually from 26.9 in 1955 and reached 2.2 in 1998. Before 1970, Nenf showed larger values than Nef, but the order was reversed in the later years. Nenf in the recent years was close to Nge. The index GD showed a sharp decline after 1980 and reached 0.78 in 1998. The major cause of the reduced genetic diversity was considered to be the bottleneck effect due to the concentrated use of breeding animals originated from a few founders. Animal Science Journal 72 (5): 378-385, 2001 Key words: Japanese Black, Genetic diversity, Effective number of founders, Genetic contributions, Founder genome equivalents

The Japanese Black is one of the domestic beef breeding stock to the whole breed7). To maintain , with about 50,000 to 60,000 reproductive cows such prominent characteristics, the population in registered annually. Since liberalization of beef Hyogo prefecture has been almost completely closed import restriction in 1991, the production of high- to the other populations. Thus, the amount of in- quality beef has received more attention to compete breeding and relationship of the population become with the economical by imported beef. Accordingly, considerably higher, and breeders are concerned about genetic evaluation with best linear unbiased prediction a decay of genetic variability. (BLUP) under animal model was introduced in the The loss of genetic variability in domestic animals same year. Nomura et al.9) reported that both the causes some undesirable phenomena such as inbreed- increasing rate of relationships and decrease of effec- ing depressions, reduced long-term genetic responses, tive population size in the Japanese Black have been and random fluctuation of selection responses. Ge- accelerated after the initiation of BLUP evaluation. netic variability is also essential for the adaptation to Because of the high meat quality, the Japanese unexpected changes of economic and environmental Black population in Hyogo prefecture has drawn spe- conditions, such as change of consumers' preference cial attention since early times. Especially, Mikata and prevalence of a novel disease. region has slaved an important role in supplying The purpose of the present study was to estimate the Corresponding: Fumio MUKAI (fax: +81 (0) 78-803-5801, e-mail: [email protected])

Anim. Sci. J. 72 (5): 378-385, 2001 378 Genetic Diversity of Japanese Black

Table 1. Numbers of reproductive bulls and cows born in each year, and the actual number of founders (Nf)

amount of the genetic diversity and survey the genetic The ancestors with unknown parents are referred to as structure of the population in Hyogo prefecture in founders, and all of their descendants are to as non- terms of population genetic parameters derived from founders. The population of founders is the base genetic contributions of ancestors. population of pedigree analysis. All the parameters were estimated for the population of registered Materials and Methods animals born in each year from 1955 to 1998. These Pedigree records of breeding stock were kept by populations are referred to as reference populations. Registry Association and Hyogo Branch of The numbers of bulls and cows born in each year are Wagyu Registry Association. All the animals are shown in Table 1. Total number of animals in the uniquely identified by the registry numbers assigned reference populations was 68,781. by Wagyu Registry Association. Information availa- The depth of pedigree in each reference population ble for each animal are names and registry numbers of was examined by computing the number of discrete the animal and its parents, and the date and place of generation equivalents (ge)15), which is the expected birth. Although the oldest animal was traced back to number of generations from the base population to the 1871, we used the pedigree data of the animals born reference population if generations proceeded dis- after 1937, from which centralized registry system was cretely. This parameter is obtained by initiated. The data consisted of 90,694 animals.

Anim. Sci. J. 72 (5): 378-385, 2001 379 HONDA, NOMURA, FUKUSHIMA and MUKAI

sity of the reference population. ge=1/NΣN j=1Σni i=11/2gij, All the causes of the reduction of genetic diversity where nj is the total number of ancestors of animal j in are fully accounted for by founder genome equivalents the reference population, gij is the number of genera- (Nge). This parameter is estimated by tions between animal j and its ancestor i, and N is the number of animals in the reference population15). Nge=1/ΣN i=1ΣN j=1 aij/N2, Genetic diversity in a closed population is decayed by three different causes, i. e. unequal genetic contribu- where aij is additive relationship coefficient between tion of founders, Mendelian sampling in meiosis, and individual i and j. The denominator is the average of the bottleneck effect3). The unequal genetic contribu- full additive relationship matrix A (including recipro- tion is of special importance in a population under cal and diagonal elements)3, 5). artificial selection, because genetic improvement is The third type of effective number of animals, the attained at the expense of reduced contributions of effective number of non-founders (Nenf), accounts genetically inferior founders16). Mendelian sampling only for the effects of Mendelian samplig and bottle- is an inevitable cause for reduction of genetic diversi- necks. This effective number is obtained from the ty, when parents are heterozygotes. Loss of genetic relation3) diversity due to the bottleneck effect will also be important under the intensive use of a few popular 1/ Nge=1/Nef+1/Nenf. (1) sires. According to Lacy4, 5),the amount of genetic diver- To assess the amount of genetic diversity and clarify sity (GD) or expected heterozygosity8) in the reference the relative importance of three causes of the reduc- population relative to the base population is estimated tion, we first estimated three types of effective num- by bers of animals, i. e. effective number of founders, GD=1-1/2Nge. founder genome equivalents, and effective number of non-founders. The effective number of founders The lowest value is estimated at 0.0 when Nge is only (Nef) is estimated by 0.5. Analogously, the genetic diversity estimated by

Nef=ΣNi i=1 GD*=1-1/2Nef

(Ci/N)2, accounts only for the decay due to unequal contribu- where Nf is the number of founders, N is the number tions of founders3). From equation (1), the differ- of animals in the reference population, and ci is the ence of these two indices of genetic diversity is sum of direct relationships between founder i and GD*-GD=1/2Nenf. animals in the reference population4, 11). In this study, we defined ci/N as genetic contributions of This difference represents the amount of the genetic founder i, so that it can be considered as expected diversity reduced by Mendelian sampling and bottle- frequencies of alleles derived from founder i in the necks, which is theoretically equivalent to the amount reference population. The effective number of of genetic drift accumulated over non-founder founders is affected only by the variation of genetic generations3). contributions among founders. In an extreme case Results and Discussion where all the founders give an exactly same contribu- tion, Nef is equal to the actual number of founders, Nf The information about generations traced back (for Nf in the reference population, see Table 1). from the reference populations to founders can be Since Nef does not take account of the effect of genetic seen in Fig. 1. During the period of 1955 to 1998, drift caused by Mendelian sampling and bottlenecks in the number of discrete generation equivalents in- subsequent generations, it overestimates genetic diver- creased from 3.6 to 7.9, meaning that the average

Anim. Sci. J. 72 (5):378-385, 2001 380 Genetic Diversity of Japanese Black

Fig. 1. The number of discrete generation equivalents and maximum number of

generations traced from population in each year.

generation interval was about 10 years in this period. effective number, founder genome equivalents (Nge), Maximum number of generations traced back from gradually decreased from 26.9 in 1955, and reached animals in 1955 and 1998 to the base population were 2.2 in 1998, implying that the genetic diversity in the 7 and 16, respectively. current population would be equivalent to the diversi- Distributions of inbreeding coefficient of each ty in a random mating population derived from only 2 animal and additive relationship coefficient among a -3 non -related founders . The relative importance of pair of animals in the reference populations of 1960, the causes of the reduction in Nge can be inferred from 1970, 1980, 1990 and 1998 are presented in Fig. 2. the behaviors of effective numbers of founders and Although the shapes of both distributions skewed non-founders (Nef and Neaf). In early years before positively in 1960, they became approximately normal 1970, Nenf showed larger values than Nef. But in the in the later years. The average inbreeding coeffi- later years, the order was reversed, and Nenf in recent cients in the five sampled years were 0.03, 0.05, 0.08, years showed values close to Nge. These results show 0.14 and 0.19, respectively. Compared to the current that although the variation of genetic contributions inbreeding level (<0.06) in the whole Japanese Black among founders is an important cause of reduced Nge population9), inbreeding level of the recent Hyogo in the early period, the major cause of the recent population was extremely high. The average additive reduction is genetic drift accumulated over non- relationships in the five sampled years were 0.05, 0.12, founder generations. 0.20, 0.36 and 0.45, respectively, indicating that the In the recent work of Boichard et al.2), Nef for three expected relationship between randomly chosen two cattle breeds in France, i. e., Abondance, Normande, individuals in the current population is comparable to and Limousine, were estimated to be 69, 132 and 790, the relationship between full-sibs. Since drastic respectively. The corresponding estimates of Nge changes in inbreeding and relationship were observed were 17, 22 and 206, respectively. Solkner et al.13) in the last 40 years, investigations about genetic diver- reported that Nef and Nge for four Austrian cattle sity and genetic structure were carried out in this breeds, i.e., Simmental, , Pinzgauer and period. Grauvieh, varied from 66.2 to 220.8, and from 20.8 to The changes of three effective numbers of animals 94.3, respectively. Estimate of Nef for UK Holstein- are presented in Fig. 3. The most comprehensive Friesian population by Roughsedge et al.12) was 93.

Anim. Sci. J. 72 (5): 378-385, 2001 381 HONDA, NOMURA, FUKUSHIMA and MUKAI

Fig. 2. Distributions of inbreeding coefficients (A) and additive relationships (B) in five sampled years.

Comparison with these published estimates character- Genetic contributions summed up by the birth place izes the extremely limited genetic diversity in the of founders are illustrated in Fig. 5. The category of Japanese Black population of Hyogo prefecture. Others' reflects the sum of contributions of founders' The changes of genetic contributions of founders born except in Mikata and Kinosaki regions, and are summarized in Fig. 4, in which the cumulative contributions of founders with unknown birth place values of genetic contributions of the first five, the are classified into the category of 'Unknown'. After second five and the third ten founders most 1980 the contribution of founders in Mikata region represented in each reference population are shown. increased almost linearly, and reached 95.6% in 1998, The sum of three cumulative contributions, i. e., the showing that the genetic composition of the current cumulative contribution of twenty founders, increased population is strongly dependent on the founders in sharply from 46.8% in 1955 to 88.3% in 1998. Fur- Mikata region. In cotrast, the contribution of found- thermore, large part of the increase was due to the first ers in Kinosaki region to the population in 1970 was five founders. These results clearly show the acceler- 15.6%, but in the following years it decreased gradu- ation of the selective use of breeding animals ally and reached 2.1% in 1998. Descendants from originated from a few founders. founders in Kinosaki region will be an important

Anim. Sci. J. 72 (5): 378-385, 2001 382 Genetic Diversity of Japanese Black

Fig. 3. Changes of founder genome equivalents Fig. 4. The cumulative value of genetic contri- (Nge), effective number of founders (Nef), and butions of twenty founders most represented in each effective number of non-founders (Nenf) in the year. reference populations from 1955 to 1998.

Fig. 5. Classification of genetic contributions by the birth place of founders. The category of 'Others' stands for founders born except in Mikata and Kinosaki regions, and the 'Unknown' for founders whose birth place could not be specified. genetic resource that could supply genetic variability though he was not a founder, his genetic contribution to the population. to the population in 1998 was 42.4%. The contribu- Table 2 shows the genetic contributions of several tions of all the representative founders in important founders in two major lines, 'Nakadoi-line' 'Nakadoi -line' increased 1.5 to 3.4 times during this in Mikata region and 'Shiroichi-line' in Kinosaki period. In contrast, the contributions of founders in region14), to the population in 1970 and 1998. In 'Shiroichi -line' decreased to less than 0 .5%. both years, the contributions of 'Fukue' and '14th The changes of two indices of genetic diversity, GD Kayano' were extremely higher than the other found- and GD*, are presented in Fig. 6. The index GD ers. This was due to the exceptionally high contribu- showed a sharp decline after 1980 and reached 0.78 in tion of their famous son, 'Tajiri', born in 1939. Al- 1998. The difference between GD and GD* also

Anim. Sci. J. 72 (5): 378-385, 2001 383 HONDA, NOMURA, FUKUSHIMA and MUKAI

Table 2. Genetic contributions of representative founders in the 'Nakadoi-line' and 'Shiroichi-line' to the populations of 1970 and 1998

Fig. 6. Change of genetic diversity (GD) in the Fig. 7. Percentage of animals sired by five bulls reference populations from 1955 to 1998. most intensively used in each year.

sharply increased after 1980, suggesting that the de- production, such as fertility, maternal ability and feed crease of GD after 1980 is largely due to the effect of efficiency. The increased rate of inbreeding and the genetic drift. The major cause of the genetic drift consequent loss of genetic diversity may also have can be seen from Fig. 7, in which the percentage of negative effects on the sustainability of the population. animals sired by five bulls most intensively used in For example, Belousova and Kudrjavtsev1) reported each year is illustrated. From 1980 to 1985, the that calf crop and viability of the European-bison percentage showed a sharp increase, and reached population was affected by its genetic diversity. 83.6% in 1990. Thus, it is concluded that the drastic In a closed population where genetic diversity is increase of the amount of genetic drift is caused by diminishing, it is very difficult to avoid the increase of bottlenecks due to the intensive use of a few sires inbreeding by simple mating control, because the in- originated from limited founders in Mikata region breeding due to the limited size of population accumu- (see also Fig. 5 and. Table 2). lates inevitably with the advance of generations. The As reviewed by Pirchner10), there are many evi- simplest way to recover genetic diversity is to intro- dences for the deleterious effects of the increased rate duce animals from the other populations. However, of inbreeding on traits related to the efficiency of beef breeders in Japan generally appreciate the

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