A Strategy for Maintaining High Fertility and Hatchability in a Multiple-Trait Egg Stock Selection Program1

A Strategy for Maintaining High Fertility and Hatchability in a Multiple-Trait Egg Stock Selection Program1 R. S. GOWE,2 R. W. FAIRFULL, I. McMILLAN,2 and G. S. SCHMIDT3 Centre for Food and Animal Research, Agriculture Canada, Ottawa, Ontario, Canada, K1A 0C6 ABSTRACT Commercial poultry breeders need to select for a wide array of traits, and conventionally they are included in a selection index. There are problems in determining economic weights and the assumptions of additivity for fertility and hatchability. The approach taken for the long-term multiple trait selection study reported here was to maintain the original high levels of these traits by culling potential breeding males and females on the basis of their parent family records. Only the lowest 10% of families were culled with no positive selection among the remaining families. As a result, selection differentials were low and averaged .40% for fertility and 1.14% for hatchability for the six selected strains. This maintained high fertility and hatchability levels over the whole study, so that the regressions for fertility and hatchability (as deviations from controls) were nonsignificant except for a small, significant increase in fertility over the last 10 yr. Mean inbreeding levels at the end of the study varied between 21.8 and 26.2% for the four strains selected for 29 or 30 yr and from 9.9 to 11.6% for the two strains selected for 11 generations. There was no evidence that inbreeding depression affected selection because breeding males and females selected each generation were as inbred as the average bird in each strain. The culling procedure used was effective in maintaining the two reproductive traits so that most of the selection pressure could be applied to the other economic traits. (Key words: nonlinear heritability, selection, fertility and hatchability, layers, inbreeding) 1993 Poultry Science 72:1433-1448

INTRODUCTION Commercial poultry breeders must consider so many traits that have some economic importance that it is difficult to apply sufficient selection pressure on the key traits to make the genetic gain needed for commercial success. In egg stock selection programs the key traits are egg

Received for publication November 30, 1992. Accepted for publication March 31, 1993. Centre for Food and Animal Research Contribution Number 2096. 2 Centre for Genetic Improvement of Livestock, Department of Animal and Poultry Science, University of Guelph, Guelph, ON, Canada, NIG 2W1. 3 On leave from: National Centre for Swine and Poultry Research, EMBRAPA, P. O. Box 21, 89.700-000 Concordia, Santa Catarina, Brazil.

production rate, sexual maturity, viability at all ages, egg size, eggshell strength, feed efficiency, fertility, and hatchability. Other traits such as albumen quality, freedom from blood spots, body weight, eggshell color, eggshell shape, and eggshell surface texture are generally of less economic importance unless a strain exhibits specific problems. Less selection pressure can usually be applied to these latter traits, as the final commercial product is a threeway or four-way cross and minor deficiencies in one parental line will normally be corrected in the final commercial product. With such a large number of traits, it is important to avoid placing more selection pressure on a trait than is required, so that selection intensity on the primary traits can be maintained.

1433

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GOWE ET AL.

Selection index theory assumes no major genes, additive gene action, and linear or quadratic economic weights. Indices work best when genes are at intermediate frequencies. Recessive genes with large negative effects and at very low frequency seriously violate index assumptions, and this appeared to be true of fertility and hatchability in the current study. Also, heritability estimates are dependent on gene frequency. Thus, a gene with an intermediate frequency will make a larger contribution to heritability than it would at a low frequency. These factors indicate that indices may not be the most efficient method to maintain high levels of fertility and hatchability. In a long-term selection study with Leghorn strains, Gowe (1983) was able to maintain high levels of fertility and hatchability, two components of fitness, in strains selected for high egg production by culling only against very low performance while not selecting positively for these traits amongst the upper 80 to 90% of the families. It was hypothesized that this approach selected against low frequency, segregating deleterious recessive genes affecting fertility and hatchability. This procedure made it possible to use more selection pressure and therefore make significant progress in the other key and secondary traits, particularly egg production (Gowe and Fairfull, 1982, 1984, 1985, 1986, 1990; Fairfull and Gowe, 1990). To test Gowe's hypothesis (Gowe, 1983), Frankham et al. (1988) selected for increased inebriation time in replicate Drosophila lines. They culled the bottom 20% of individuals for fitness in three replicates and in three other replicates they did not cull for fitness. There was no significant difference in inebriation time between treatment groups. However, in the strains selected for fitness, fitness did not decrease whereas it decreased significantly in the lines not culled for fitness. In a review of selection response for fitness traits in several species, Frankham (1990) has shown that responses to selection for reproductive fitness traits are generally asymmetrical and higher in the low fitness direction. In a simulation study, Li and James (1992:515) concluded, "... that culling on low fitness can lead to less fitness loss without substantial reduction in response ...".

The present paper documents a study on long-term selection for multiple traits in White Leghorn strains in which selection for fertility and hatchability was based on culling males and females from the breeding population only if their parents' performance was very much below the population mean. In Gowe (1983: 28-29), the rationale for the selection procedure for fertility and hatchability used in this long-term multiple trait selection was described as follows: Fertility is a trait that has low heritability. Experience has shown that high selection pressure to improve it or maintain it, if it is already satisfactory, will be generally wasteful of the selection pressure available. Yet the selection of dams and especially sires from full- or half-sib families with very low fertility (2 or 3 standard deviations below the mean) will lead to a drop in fertility in their offspring. This lower level of fertility will be refractory to improvement. Therefore we are careful to eliminate progeny from very poor families but pay no attention to minor variations in fertility We believe that fertility may be an example of a trait where the underlying genetic values may not be linear or continuous.

It is well-known that inbreeding depression in relatively small breeding populations reduces fertility and hatchability. With the exception of the paper by Ameli et al. (1991) that reported on commercial selected strains, and earlier brief reports on this study (Gowe and Fairfull, 1980, 1985), detailed information has not been available on inbreeding in populations under multiple trait selection for many generations such as is characteristic of commercial egg stocks. The purposes of this paper were to examine 1) the fertility and hatchability in selected and control strains of the Ottawa long-term selection study; 2) the inbreeding levels in selected and control strains along with the regression of inbreeding and fertility and hatchability over time; and 3) the selection differentials and the genetic changes in the two fitness traits. MATERIALS AND METHODS Experimental Strains Selected Strains 1 and 3 and Control Strain 5 (Base 5). Strains 5 and 3 originated

SELECTION FOR FERTILITY AND HATCHABILITY

from a common base population in 1950. Strain 3 was under selection from 1951 to 1980 except for 1970 when it was completely unselected and randomly bred, and 1971 when there was reduced selection. Control Strain 5 was unselected and randomly bred from 1950 to 1980. In 1971, all females in Strain 3 that were alive at breeding time were randomly assigned within full- and half-sib families to two populations to continue Strain 3 and start Strain 1. Pairs of full-sib males to reproduce the two populations were selected on the limited full- and half-sib female performance data available, and one of each full-sib pair was assigned to each of the two strains. Selected Strains 2 and 4 (Base 4). Strain 4 originated in 1950 from seven Canadian "Record of Performance" stocks selected to be as unrelated as possible and with good home farm performance. A 7 x 7 diallel cross including the diagonal was set up in 1951, and the progeny resulting from these 49 groups were the base population for Strain 4. The new composite was put under selection starting in 1952 with no attention paid to origin. In 1969, Strain 4 was divided into two populations to continue Strain 4 and start Strain 2 as described above for the formation of Strain 1. Because twice the usual number of males and females were selected in 1969, there was some reduction in selection pressure that year. Selected Strains 8 and 9 and Control Strain 7 (Base 7). Strain 7 originated from four widely used Leghorn commercial stocks being sold in North America (H&N Nick Chick, Hy-Line® 934A, Kimber K137, and Shaver 288). These stocks were obtained in 1958 as hatching eggs and over 2 yr pooled in a balanced crossing system so that by 1960 each individual had an average 25% of the genes of each commercial strain. The strain was then randomly bred until 1968, when from a larger man normal hatch, two populations (in addition to Strain 7) were created by within family assignment of males and females. These two populations were designated Strains 8 and 9. The randomly bred control Strain 7 was also continued without selection. Control Strain 10. This base population was originated from four widely used Leghorn commercial stocks by obtaining

1435

hatching eggs in 1972 (Babcock B300, H&N Nick Chick, Hy-Line® 934, and Shaver 288). It was kept as a random breeding population after preliminary systematic crossing to ensure the genes of the parent stocks were equally represented in the base population individuals. Detailed information on the selected and control strains can be found in Gowe and Fairfull (1990) and Fairfull and Gowe (1990) and the references in these papers. Selection and Mating Procedures Selected Strains. A consistent multivariate culling levels scheme that involved the use of full-sib and half-sib family means as well as individual records of females was used in the selection of all selected strains. The egg production trait was selected as shown in Table 1. All other traits were selected with approximately the same emphasis for all six selected strains. It is not the purpose of this paper to present the results for the traits other than fertility and hatchability, but it is important to appreciate that most of the selection pressure was directed at these other traits (McAllister, 1977). The year selection was started for the array of traits is shown in Table 1. The selected strains from the genetic bases started in 1950 and 1951 were selected for fertility and hatchability from 1953 on, whereas other selected strains were selected for these two reproductive traits as soon as they were formed. The objective with respect to fertility and hatchability was to maintain the generally high levels of the base populations with little expectation of increasing performance. Selection for fertility and hatchability was based mainly on pedigree information, that is, breeding males and females were selected based on the records of their dams and sires. Individual selection was based mainly on natural selection in that individual chicks that failed to hatch were, of course, never selected, and selected males and females that had very low reproductive records did not contribute to the next generation. In addition, all selected males were pretested for fertility. For this test, selected females were assigned to singlemale mating groups, then artificially inseminated twice. A small sample of fresh

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GOWE ET AL.

TABLE 1. Traits under selection in the six selected strains from three genetic bases and the year selection for different traits was introduced to the selection program Experimental strains Base 5 Traits under selection Hen-housed egg production to 273 days, no. Hen-day egg production from A.F.E.1 to 273 days, % Viability: brooding and rearing period, % Viability: laying house to 273 days, % Egg size at 240 days, g Specific gravity at 240 days Haugh units at 240 days Blood spot percentage at 240 days Body weight at 265 days, kg Fertility, % Hatchability, % Egg shape and shell defects J

Strain 3

Base 7

Base 4

Strain 1

Strain 4

Strain 2

1952

1951 1971

Strain 8

Strain 9

1969 1969

1969

1951

1951

1951

1951

1969

1969

1951

1951

1951

1951

1969

1969

1953 1969 1969 1969

1953 1969 1969 1969

1953 1969 1969 1969

1953 1969 1969 1969

1969 1969 1969 1969

1969 1969 1969 1969

1975 1953 1953 1969

1975 1953 1953 1969

1975 1953 1953 1969

1975 1953 1953 1969

1975 1969 1969 1969

1975 1969 1969 1969

Age at first egg.

hatching eggs from each group was collected and broken out, and fertility was determined by examining the unincubated blastoderm (Gowe, 1950). Until 1963 the two selected strains were reproduced by individual sire pedigree pens with each of about 28 selected sires per strain mated to 8 to 12 females. The pretest was then done by putting the selected males in the breeding pens several days before hatching eggs were required. After several days, a sample of eggs was broken out to determine fertility. Only males that were sterile or very low in fertility were replaced, preferably by a full brother, before hatching eggs were saved. Only a few males were eliminated by this procedure, but it prevented the loss of potential progeny from the selected females assigned to these males. From 1964 on, all strains were reproduced by artificial insemination (AI). Control Strains. Up to 1953, Strain 5 was reproduced by natural multiple male pen matings using 40 to 60 sires each year. From 1954 to 1958, Strain 5 was randomly reproduced by AI using 40 to 50 sires (Gowe

et al, 1959a). From 1959 on, Strain 5 was reproduced by AI using pedigreed random mating (Gowe et al, 1959b) with 80 sires and 240 dams each year. Test Procedures From 1950 to 1963, several farms of Agriculture Canada's Research Branch cooperated in testing the stocks in this longterm selection experiment. Several hatches were obtained each breeding season (year) to provide test stock of all strains for all locations. Up to the 1955 hatch year, the strains were randomly distributed within family to each farm at each hatch. From 1956 to 1963 each hatch was sent to a separate farm (except in 1956 when all of Hatch 1 and part of Hatch 2 went to Ottawa). The fertility and hatchability records presented in this study cover the complete breeding season. When there were four hatches distributed to the test farms the records reported here were based on the eggs set in all four hatches. Eggs were saved for 2 wk for each hatch. From 1964 to 1980,

SELECTION FOR FERTILITY AND HATCHABILITY

there was only one test farm, and the fertility and hatchability records were based on one hatch for which hatching eggs were saved for 21 days. Hatching eggs from the control strains were saved over the same period as for the selected strains so that the effect of holding hatching eggs was the same for all strains, because it is well known that hatchability decreases as the holding time for hatching eggs increases [see Fairfull and Gowe (1987) and Proudfoot (1969) for references]. From 1968 on, the hatching eggs for all strains for the oldest 2 wk of the 3-wk collection were stored in Cryovac®4 bags and flushed with nitrogen, as this had been shown to increase hatchability of eggs stored longer than 7 days (Proudfoot, 1969). For the last 10 yr (1970 on), the hatching eggs for the 2 oldest wk of the 3-wk collection were stored small end up without daily turning, as Proudfoot (1969) had shown that the hatchability of eggs stored this way was either just as good, or better, than when stored in the conventional way. For all the data presented in this paper, the fertility estimate was based on classifying eggs as infertile that were clear when candled at 18 days of incubation. Because such clear eggs could include some very early embryonic deaths, the trait fertility as used in this paper should be understood as "apparent fertility". The hatchability percentage for this study is based on the number of "apparently fertile" eggs at 18 days that hatched. Hatched chicks did not include the pipped eggs that failed to hatch, but it did include crippled chicks that hatched on their own. From 1965 on, all females were housed at 17 to 20 wk of age in individual cages. From 1968 on, all females were brooded and reared in cages. Statistical Analysis Inbreeding. Inbreeding was calculated three ways for all the selected and control strains. Using the pedigree records, inbreeding (Fx) was calculated according to Malecot (1948) and Henderson (1976). This

4

W. R. Grace Chemicals Ltd., Cryovac Division, Montreal, PQ, Canada, H4T 1P3.

1437

took into account the effect of artificial and natural selection in the selected strains and natural selection in the control strains. Inbreeding for each generation was also estimated on the basis of random or panmictic mating (FR) using the conventional formula,

u - -L + -L R

" 8S 8D where S and D, respectively, are the number of sires and dams contributing to the next generation. For the control strains (5,7, and 10), inbreeding was also estimated on the basis of random pedigree matings in which each sire contributed a sire and each dam contributed a dam to the next generation, as described by Gowe et ol. (1959b),

Fp - J - + J " 32S

32D

to compare the expected inbreeding using this formula with that estimated assuming panmictic mating and the actual inbreeding calculated from the pedigrees. To estimate changes in fertility and hatchability over generations, the deviations between the selected and control strain means for each trait were regressed over generations. To estimate the change in inbreeding over generations, strain mean percentage inbreeding was regressed over generations. Selection Differentials. Selection differentials were estimated as the deviation between pedigree values of selected and population means where the selected strain means were weighted by the number of matings in which an individual participated. The male and female contributions were summed and divided by two. These estimates were calculated from the year (1964) when all selected and control strains were artificially inseminated and unbiased comparisons could be made. RESULTS Fertility and Hatchability Figures la and 2a show the absolute fertility and hatchability, respectively, of all strains over all years, and the genetic trend

1438

GOWE ET Ah.

1950

1952

1954

1956

1958

1960

1962

1964

1966

1968

1970

1972

1974

1976

1978

19

YEAR OF HATCH 10

B FERTILITY

flMft/

•10-

SfLtCTEO • • 3 O O I

1950

1952

1954

1956

1958

1960

1962

1964

1966

19

1970

1972

1974

1976

COMTROt Q O I $ ^Hl

1978

19

YEAR OF HATCH

FIGURE 1. A) Fertility of six selected and three control strains from their origin to 1980. B) Six selected and two control strains plotted as deviations from control Strain 5 to show genetic trends for fertility.

1439

SELECTION FOR FERTILITY AND HATCHABILITY

100

HATCHABILITY

90

80

70 -

SELECTED

1950

1952

CONTROL

•

»3

e

o * A

o l * 4 & 2

a V

1954

1956

1958

•es B7 V'O

I960

1962

1964

1966

1968

1970

1972

1974

1976

1978

1980

YEAR OF HATCH 10

B HATCHABILITY

SELECTED • • 3 O O 1

1950

A

A 2

D

o 9

1952

1954

CONTROL H U7 $ ^10

1956

1958

1960

1962

1964

1966

1968

1970

1972

1974

1976

1978

1980

YEAR O F H A T C H

FIGURE 2. A) Hatchability of six selected and three control strains from their origin to 1980. B) Six selected ap two control strains plotted as deviations from control Strain 5 to show genetic trends for hatchabi)'

1440

GOWE ET AL.

in the selected strains was calculated from made, but only the final year (1980) is deviations from control Strain 5 as shown in shown to contrast with inbreeding calcuFigure lb and 2b. An outbreak of coryza lated from the pedigrees. For the selected seriously affected the health of both Strains strains, FR grossly underestimated the in5 and 3 in 1950 and resulted in lower than breeding as was expected, because FR did normal fertility and hatchability. In 1953, not take into account the effects of selection. selection for fertility and hatchability was For the control strains, FP estimated more introduced for the selected strains, because closely than FR the actual F*, as the FP Strain 3 was decreasing in reproductive estimate took into consideration the restricperformance relative to the control. tions in the matings. There was good As can be seen in Figure la and b, after all agreement between the actual (Fx) and strains were reproduced by AI (from 1964), expected (FP) inbreeding. the fertility of the selected strains exceeded The differences each year between those the control most years and varied around females and males selected and the total 95%. Because the two selected Strains 3 and female and male populations, respectively, 4 were reproduced by single male matings were not large, suggesting that inbreeding from 1950 to 1963, and the control strain depression did not substantially affect any was flock mated, then artificially inseminated in this period, comparisons between of the performance traits under selection the control and selected strains in absolute (Table 4). Inbreeding in the six selected and two level of fertility would be biased by the preferential mating that occurs in single control strains was regressed over generamale matings. There was no significant tions for different periods in the selection genetic trend for either strain in this period study, after selection for fertility and hatch(Table 2). Hatchability, averaging about ability started (Table 5). For the first 10 yr, 88%, for the selected strains has generally inbreeding changed at a rate of about .50% been high, particularly considering the egg per generation and, for the last 10 yr, about .90% per generation for the selected strains. save period of 3 wk from 1964 on. This increase in inbreeding was due mostly to the reduction in population sizes of the Inbreeding selected strains after 1969, when four strains were added to the program. There was a The inbreeding coefficients (Fx) by year for all selected and control strains (both significant positive regression of inbreedsexes) from their origin to 1980 are shown in ing for all selected strains in all periods, Table 3. Results up to 1978 were previously indicating a steady increase in the inbreedreported by Gowe and Fairfull (1980). The ing coefficient. This can be contrasted with yearly calculations for FR and FP were the much smaller increase in inbreeding of

TABLE 2. Regression coefficients and standard errors for fertility (F) and hatchability (H) percentage of six selected strains as deviations from control strains over various periods 1954 to 19631 Strain 14 3 2 4 8 9 x

F

H

1964 to 1980W F

H

.06 ± .04

-.03 ± .03

.13 ± .13

-.00 ± .10

.02 ± .04

.02 ± .03

-.02 ± .12

-.17 ± .20

-.02 ± .03

-.01 ± .02

.08 ± .09

-.09 ± .09

1969 to 19803 ]F

.16 .31 .27 -.09 .06 .24 .18

H .13 .20 .26 .23 .09 .12 .08"

deviation from control Strain 5. For years where strains were not selected, data were not included (Strain 3, 1970). 3 Deviation from mean of control Strains 5 and 7. 4 From origin of the strain in 1971 to 1980. **P < .01. 2

.27 ± -.09 ± .18 ± .22 ± -.07 ± -.06 ± -.07 ±

.31 .18 .20 .19 .14 .15 .07

SELECTION FOR FERTILITY AND HATCHABILITY

the control strains of a little more than .1% per generation after these populations were reproduced with restrictions (Tables 3 and 5). Genetic Changes in Fertility and Hatchability If inbreeding of .5 to .9% per generation was causing a significant depression in fertility and hatchability of the selected strains not compensated by selection, it would produce a negative regression over

1441

generations for the deviations of selected from control strains for the different periods. For the two long-term selected strains (30 and 29 generations), for the periods 1954 to 1963 and 1964 to 1980, there were no significant genetic trends in fertility or hatchability (Table 2), which suggests that there was no change after selection for these traits was initiated. For the last period 1969 to 1980, there were no significant genetic trends in hatchability, with three of the strain estimates for hatchability being negative and three being positive. However,

TABLE 3. Percentage inbreeding (Fx) from pedigree records for six selected (S) and three control (C) strains Strains Year 1950 1 2 3 4 5 6 7 8 9 1960 1 2 3 4 5 6 7 8 9 1970 1 2 3 4 5 6 7 8 9 1980 19802 19803 A/yr» !

1 S

3 S

5 C .8 1.1 1.4

14.6 15.2 15.5 16.0 16.6 17.8 18.6 19.6 20.6 21.4 22.8 14.8

.8 1.0 1.4 2.6 3.6 4.5 5.3 5.9 5.2 6.3 7.4 7.1 7.7 8.6 11.2 11.9 12.0 13.0 13.3 14.0 14.6 15.2 15.4 15.6 16.4 17.3 18.1 18.7 19.5 20.2 21.3 14.8

.73

.68

1

2S

1.8

2.1 2.5 2.8 3.1 3.4 3.5 3.7 3.8 4.0 4.1 4.2 4.4 4.2 4.4 4.5 4.8 4.8 5.1 5.2 5.4 5.5 5.6 5.9 6.0 6.1 6.3 6.3 8.2 6.3 .18

. . ,,

15.3 15.8 17.0 17.6 19.0 19.7 20.6 22.0 23.0 23.7 24.8 25.4 26.2 14.2 .89

4 S .5 .5 2.1 2.3 3.8 4.7 5.5 4.7 6.5 6.6 6.6 7.5 7.1 11.7 12.7 12.9 14.9 15.4 15.7 16.8 17.2 18.1 18.7 19.4 20.3 21.1 22.2 22.8 23.8 24.4 14.3 .82

9 S

1.0 1.0 1.5 3.8 4.8 5.3 6.3 7.5 8.7 9.8 10.5 11.6 7.4 .96

8 S

i.6 1.0 1.5 2.2 3.4 4.4 5.5 6.3 7.2 8.0 9.0 9.9 7.4 .81

7 C

.0 .0 .0 .1 .3 .4 .5 .9 .8 .7 .9 1.0 1.2 1.4 1.6 1.6 1.7 2.1 2.0 2.1 2.4 2.4 4.0 2.5 .11

10 C

.6.6 .5 .7 .7 .8 .9 1.1 1.4 .9 .14

Up to 1959, control Strain 5 was maintained as a random flock mated population so that expectations based on pedigreed random matings with restrictions apply only after 1959. 2 Expected based on panmictic mating. F R = 1/8S + 1/8D, each generation. 3 Expected based on restricted random mating. Fp = 3/32S + 1/32D, each generation. 4 A/yr = Mean increase in inbreeding (Fx) per year.

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GOWE ET AL.

TABLE 4. Mean percentage inbreeding (Fx) values for all males and females before selection and for breeder males and females from 1964 or the origin of the strain to 1980, each year given equal weight Total population

Breeder population

Strain

Males

Females

Males

Females

Selected strains 1 3 2 4 8 9 5c

17.5 14.9 18.9 17.2 4.3 5.2 13.0

17.8 15.3 20.7 17.5 4.4 5.4 13.5

17.8 15.2 20.7 17.6 4.4 5.3 13.5

17.9 15.3 20.8 17.7 4.5 5.5 13.6

Control strains 5 7 10 X

5.1 1.4 .6 2.4

5.1 1.4 .6 2.4

5.21 1.51 .71 2.5

5.21 1.41 .61 2.4

JRandomly chosen.

note that for fertility over the last period, there was only one negative nonsignificant estimate, and the pooled estimate for the six strains was small, but positive (.18%) and significant.

selected strains for fertility was .40% per generation. For the three controls, natural selection gave a differential of .07% or less than one quarter that of the selected strains. Thus, overall selection for fertility was low, in the order of about .33% per generation. For hatchability, the selection differential estimated for the control strains was .32%, Selection Differentials indicating that natural selection was higher Selection differentials were calculated for hatchability. The uncorrected selection for the years 1964 to 1979 for fertility and differential was 1.14% for the selected hatchability, and these are shown in Table 6. strains, and thus selection for hatchability The overall selection differential for the six was also low, about .8% per generation.

TABLE 5. Regression coefficients with standard errors for the calculated inbreeding (Fx) of the six selected strains and three control strains over different periods Strain 11 3 2 4 8 9 5 7 102 5c

1954 to 1963

1964 to 1980

49 ± .05"

60 ± .04**

.51 ± .07"*

78 ± .01**

.50 ± .05** .21 ± .02**

69 ± .04** 15 ± .01** 13 ± .01**

.21 ± .02**

14 ± .07*

iFrom origin of the strain in 1971 to 1980. From origin of the strain in 1972 to 1980. +P < .10. **P < .01.

2

1969 to 1980 .82 .66 .96 .79 .87 1.03 .90 .15 .14 .12 .14

± ± ± ± ± ± ± ± ± ± ±

.04" .03" .02" .01" .03" .04" .24" .01" .01' .02" .12

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SELECTION FOR FERTILITY AND HATCHABILITY

TABLE 6. Selection differentials for fertility and hatchability from 1964 to 1979 for the six selected (S) strains ani I three control (C) strains Percentage hatchability

Percentage Strain

Years

1 S 3 S 2 S 4 S 8 S 9 S X 5 C 7 C 10 C x"

1971 1964 1969 1964 1969 1969 1964 1964 1966 1973 1964

to to to to to to to to to to to

1979 19791 1979 1979 1979 1979 19791 1979 1979 1979 1979


9

(6* + 9)/2


9

(6* + 9)/2

-.19 .71 .93 .88 .63 .32 .55 .13 .15 .09 .12

.12 .12 .37 .28 .36 .26 .25 .15 -.05 -.06 .01

-.04 .42 .65 .58 .50 .29 .40 .14 .05 .02 .07

1.60 2.07 1.60 1.22 1.85 2.19 1.75 .56 .92 .13 .54

.62 .63 .56 .46 .38 .51 .53 .17 .11 .01 .10

1.11 1.35 1.08 .84 1.12 1.35 1.14 .37 .52 .07 .32

x

Year 1970 excluded for Strain 3.

Perhaps a more useful way to illustrate the selection practiced is by contrasting the frequency distribution of the fertility or hatchability of all the full-sib families of a strain with the frequency distributions of those full-sib families that contributed dams and the full-sib families that contributed sires to the next breeding population. The histograms for these populations pooled over all six selected strains in 1978 and 1979 are shown in Figure 3 to illustrate that the selection practiced was mainly culling of potential breeding males and females from parental families with very low levels of fertility and hatchability. It is also instructive to contrast the frequency distributions of fertility and hatchability of the three control strain fullsib families pooled over 1978 and 1979 (Figure 4). There is a higher frequency of completely infertile dams and dams, whose eggs failed to hatch in these strains than in the selected strains. DISCUSSION Selection for fertility and hatchability was based on a hypothesis of selecting against segregating deleterious recessive genes probably at low frequencies with a presumption that the heritabilities are low. Also, mean fertility and hatchability were high and close to maximum values. Both considerations suggest that conventional selection would be relatively ineffective.

The results of the present study demonstrate the effectiveness of selecting only against such presumed deleterious genes, and coupled with other published findings, suggest that this method makes efficient use of limited selection pressure. Genetic Effects Fertility is generally considered a trait of the two parents (Bernier et al, 1951; Crittenden et al, 1957). It is perhaps more correctly defined as the interaction of a male and a female gamete to produce a viable zygote. Zygote development and, thus, hatchability, are traits of the embryo with large maternal effects. Fertility and hatchability are therefore all-or-none traits. However, they are usually considered as traits of the selected breeding population of sires and dams. The percentage of eggs set per dam that are fertile and that hatch are used to estimate genetic variance. In only a few studies were fertility and hatchability estimated for each female in the population being tested for other traits such as egg production, egg size, etc. (Crittenden et al, 1957; Hunton, 1969). There are few estimates of heritability for fertility and, in general, they are low when measured conventionally, but higher when the number of fertile eggs produced after two inseminations is the measure of fertility (Table 7). Heritability estimates for the hatchability of fertile eggs are variable, but

1444

GOWE ET AL.

15 20

25

30 35 40 45 50 55 60 Percentage Fertility

65

70

75 80

1 85 90

•• — •

95

a

•

10

15 20

25 30 35 40 45 50 55 60 65 Percentage Hatchability

10

15 20

25 30

70

llll Mill 75 80 85

90

95

w250

E 300

15 20 25

30

35 40 45 50 55 60 Percentage Fertility

65

S

70 75 •

Tuft

35 40 45 50 55 60 65 Percentage Hatchability

70

75

H

^ 15 20 25

30

35 40 45 50 55 60 Percentage Fertility

65 70 75 80 85 90 95

10

15 20 25

30

35 40 45 50 55 60 65 Percentage Hatchability

1

70 75

80 85

90

95

FIGURE 3. A) Frequency distribution of percentage fertility for all full-sib families in the breeding population of six selected strains pooled over 1978 and 1979. B) Frequency distribution of percentage fertility of those full-sib families from which female breeders were selected of six selected strains pooled over 1978 and 1979. C) Frequency distribution of percentage fertility of those full-sib families from which male breeders were selected of six selected strains pooled over 1978 and 1979. D) Frequency distribution of percentage hatchability for all full-sib families in the breeding population of six selected strains pooled over 1978 and 1979. E) Frequency distribution of percentage hatchability of those full-sib families from which female breeders were selected of sue selected strains pooled over 1978 and 1979. F) Frequency distribution of percentage hatchability of those full-sib families from which male breeders were selected of six selected strains pooled over 1978 and 1979.

generally higher than those for fertility (Table 8). Major genes affecting both fertility and hatchability have been reported (Crawford, 1965; Landauer, 1967; Hurt, 1969; Merat, 1990; Froman et al, 1992). There is no doubt that both fertility and hatchability have a genetic basis and that there are major genes that affect each trait and other genes with smaller effects. Even though the heritabili-

ties are generally low, the effects are profound when these alleles are present. In the current study, the frequency distributions of fertility and hatchability were consistent with an hypothesis of low frequency, segregating deleterious recessive genes with major effects (Figures 4a and 4b). Also, it is obvious that improvement was achieved by reducing the frequency of deleterious genes as shown by

1445

SELECTION FOR FERTILITY AND HATCHABILITY

the diminishment of the long lower tail of the frequency distribution over generations (Figures 3a and 3d). Inbreeding There are numerous reports on the effect of rapid inbreeding, such as results from the development of inbred lines, on traits of laying strains. In general, there is a substantial reduction in overall fitness of inbred lines (Abplanalp, 1990), as would be expected with the presence of segregating undesirable recessives at some loci. Also, there is evidence that selection may not alleviate the detrimental effects of rapid inbreeding (Nordskog and Hardiman, 1980; Ibe et al, 1983), possibly because the deleterious alleles could not be eliminated before fixation. Hatchability is generally more seriously affected than fertility, which is not reduced in some inbred lines (Abplanalp, 1990), but is in others (Bernier et al, 1951). Selection Studies. Only a few reports exist of multiple trait selection experiments in which fertility and hatchability were included in the program or reported. In the Cornell long-term selection study, three strains were selected principally for disease resistance or susceptibility, egg production, and egg size. Fertility was about 88,91, and 95% for the C, K, and S strains, respectively, after 32 yr of selection (Hutt, 1969). After 35 yr, the inbreeding in the S strain was 39%, indicating that high levels of fertility are possible in long-term selected populations with high inbreeding coefficients provided

r

•a

1

15 20 25 30 35 40 45 50 55 60 65 70 75 Percentage Fertility

450400
h

f• I I I

Z 150-•

0

5

JX • I I I I

10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 Percentage Hatchability

FIGURE 4. A) Frequency distribution of percentage fertility for all full-sib families in the breeding population of three control strains pooled over 1978 and 1979. B) Frequency distribution of percentage hatchability for all full-sib families in the breeding population of three control strains pooled over 1978 and 1979.

these are achieved gradually (Gavora et ah, 1979). Also, the C strain rapidly declined in fertility but recovered with a culling program. The infertility in this strain was shown to have a genetic basis (Gowe and Hutt, 1949; Hutt, 1969).

TABLE 7. Heritabiliry (h2) of the fertility of eggs set as reported in the literature Heritabiliry estimates1 h|

Breed 2

Various Leghorn' Leghorn' Leghorn' Leghorn' Egg type3

.02 !06 .14 .11

*D

.21 .08 .06 .28 .27

h

l+D

hop

Reference

.08

.04 .02

Kinney (1969) Dickerson (1964) Liljedahl et al. (1979) Chaudhaury et al. (1984) Chaudhaury et al. (1984) Beaumont (1990)

!()6 !06 .04 .30<

Subscripts refer to method of calculation: S = sire variance component, D = dam variance component, S+D = sire plus dam components, OP = offspring-parent regression. 2 Means of literature reports for several breeds to 1968. 'Data from selected strains. 4 Number of fertile eggs after two artificial inseminations.

1446

GOWE ET AL.

TABLE 8. Heritability (h2) of the hatchability of fertile eggs as reported in the literature Heritability estimates1 Breed 2

Various Leghorn3 Leghorn4 Light Sussex3-5 Rhode Island Red3-5 Leghorn3 Leghorn6 Leghorn3 Leghorn3

h|

h

D

^D

^P

Reference

.14

.22 -.04 .21 .22 .14 .19 .07 .14 .25

06

16 06

Kinney (1969) Dickerson (1964) Liljedahl et al. (1979) Hunton (1969) Hunton (1969) Prasad et al. (1977) Prasad et al. (1977) Chaudhaury et al. (1984) Chaudhaury et al. (1984)

.05 .37 .13 .12 .12

13 31 13 12 26

Subscripts refer to method of calculation: S = sire variance component, D = dam variance component, S+D = sire plus dam components, OP = offspring-parent regression. 2 Means of literature reports for several breeds to 1968. 3 Data from selected strains. 4 Data from control strains. 5 Hatchability of all eggs set. 6 Data from strain crosses.

Commercial poultry breeders rarely report on the inbreeding in their strains or on the levels of fertility and hatchability. However, successful commercial strains require high fertility and hatchability both in parent and grandparent stocks. Recently, Lohmann Tierzucht GmbH published the inbreeding levels for two of their White Leghorn commercial lines (Ameli et al, 1991), although they did not go back to the origin of the strains. From 1974 to 1986, inbreeding increased about .6% per generation, which was slightly lower than the selected strain average of .9% for the last 11 yr of the current study. The selection program at Kimber Poultry Farm included fertility and hatchability in an index of 18 traits (Kashyap et al, 1981). In the 13 yr reported, there were no significant genetic trends in fertility or hatchability. The index apparently prevented any decline in these two fitness traits. However, the genetic response for rate of egg production was only one quarter that reported by Gowe (1977) for the present study. The results of the present study clearly show that two important components of fitness, fertility and hatchability, can be maintained at high levels in an effective selection program for several characters, including egg production, that results in significant increases in inbreeding. A virtu-

ally identical result with regard to fertility and hatchability was obtained in six selected lines from three genetic base populations. Also, the selection for fertility and hatchability practiced in this study had little effect on the selection pressure available for other traits, indicating that it may be more efficient to maintain the high genetic levels of these characters outside of a formal linear selection index. ACKNOWLEDGMENTS

The authors appreciate the support and input of the many poultry farm staff and technicians who have contributed to the long-term selection study, in particular, the technical input of Leon Asselstine. The authors also appreciate the helpful suggestions of J. S. Gavora and A. J. Lee. REFERENCES Abplanalp, H., 1990. Chapter 39. Inbreeding. Pages 955-984 in: Poultry Breeding and Genetics. R. D. Crawford, ed. Elsevier Science Publishers, Amsterdam, The Netherlands. Ameli, H., D. K. Flock, and P. Glodek, 1991. Cumulative inbreeding in commercial White Leghorn lines under long-term reciprocal recurrent selection. Br. Poult. Sci. 32:439-449. Beaumont, C, 1990. Selection for hen's duration of fertility. Pages 44-47 in: Proceedings of the 4th World Congress on Genetics Applied to Live-

SELECTION FOR FERTILITY AND HATCHABILITY

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stock Production. Vol. XVI. Edinburgh, Scotstrains and three control strains, and a strain land. cross evaluation of the selected strains. Pages Bernier, P. E., L. W. Taylor, and C. A. Gunns, 1951. 141-162 in: Proceedings of the South Pacific The relative effects of inbreeding and outbreedPoultry Science Convention. Auckland, New ing on reproduction in the domestic fowl. Parts Zealand. I-V. Hilgardia 20:529-628. Gowe, R. S., and R. W. Fairfull, 1982. Some lessons Chaudhaury, M. L., J. S. Sandu, and G. S. Brah, 1984. from selection studies in poultry. Pages 261-281 Variance component analysis of fertility and in: Proceedings of the World Congress on Sheep hatchability in White Leghorns. Z. Tierz. and Beef Cattle Breeding, Vol. 1. Palmerston Zuechtungsbiol. 101:359-366. North, New Zealand. Crawford, R. D., 1965. Comb dimorphism in Wyan- Gowe, R S., and R W. Fairfull, 1984. Effect of dotte domestic fowl. I. Sperm competition in selection for part-record number of eggs from relation to rose and single comb alleles. Can. J. housing vs selection for hen-day rate of producGenet. Cytol. 7:500-504. tion from age at first egg. Ann. Agric. Fenn. 23: Crittenden, L. B., B. B. Bohren, and V. L. Anderson, 196-203. 1957. Genetic variance and covariance of the Gowe, R S., and R W. Fairfull, 1985. The direct components of hatchability in New Hampshires. response to long-term selection for multiple Poultry Sci. 36:90-103. traits in egg stocks and changes in genetic Dickerson, G. E., 1964. Experimental evaluation of parameters with selection. Pages 125-146 in: selection theory in poultry. Pages 747-761 in: Poultry Genetics and Breeding. W. G. Hill, J. H. Genetics Today. Proceedings of the XI InternaManson, and D. Hewitt, ed. Longman, British tional Congress on Genetics. The Hague, The Poultry Science. Edinburgh, Scotland. Netherlands. Gowe, R S., and R W. Fairfull, 1986. 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A simple method for homozygosity of the rose comb allele (R) on computing the inverse of a numerator relationduration of fertility of roosters (Gallus domestiship matrix used in prediction of breeding cus). Poultry Sci. 71:1939-1942. values. Biometrics 32:69-83. Gavora, J. S., A. Emsley, and R K. Cole, 1979. Hunton, P., 1969. Variance and covariance of hatchaInbreeding in 35 generations of development of bility and some of its components in the Cornell S strain of Leghorns. Poultry Sci. 58: chicken. Br. Poult. Sci. 10:261-272. 1133-1136. Hutt, F. B., 1969. Genetic aspects of fertility and hatchability in the fowl. Pages 49-56 in: The Gowe, R. S., 1950. Techniques for identifying fertile Fertility and Hatchability of the Hen's Egg. T. C. hens' eggs. Poultry Sci. 29:409-413. Carter and B. M. Freeman, ed. Oliver and Boyd, Gowe, R. S., 1977. Multiple-trait selection in egg Edinburgh, Scotland. stocks. 1. Performance of six selected lines derived from three base populations. 2. 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Agric. Handbook No. 363. Agricultural Research Service, USDA, Washington, DC. Landauer, W., 1967. The hatchability of chicken eggs as influenced by environment and heredity. Storrs Agricultural Experimental Station Monograph 1 (Revised). Storrs, CT. Li, Y., and J. W. James, 1992. Selection for a quantitative trait with and without culling on low fitness when separate loci affect the trait and fitness. Pages 513-515 in: Proceedings of the Australian Association of Animal Breeding and Genetics. Vol. 10. Rockhampton, Queensland, Australia. Liljedahl, L.-E., N. Kolstad, P. Sorensen, and K. Maijala, 1979. Scandinavian selection and crossbreeding experiment with laying hens. 1. Background and genetic outline. Acta Agric. Scand. 29:273-286. Malecot, G., 1948. Les Mathematiques de I'Heredite. Masson et Cie, Paris, France. McAllister, A. J., 1977. Multiple trait selection in egg stocks, in. Retrospective evaluation of individual and family selection. Pages 92-107 in:

Proceedings of the 26th Annual National Poultry Breeders Roundtable. Kansas City, MO. Merat, P., 1990. Chapter 20. Pleiotropic and Associated Effects of Major Genes. Pages 429-467 in: Poultry Breeding and Genetics. R. D. Crawford, ed. Elsevier Science Publishers, Amsterdam, The Netherlands. Nordskog, A. W., and J. Hardiman, 1980. Inbreeding depression and natural selection as factors limiting progress from selection in poultry. Pages 91-99 in: Selection Experiments in Laboratory and Domestic Animals: The Proceedings of a Symposium. A. Robertson, ed. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, England. Prasad, J., A. G. Khan, and M. V. Poulose, 1977. Genetic inferences from interstrain crossing for hatchability and fertility in White Leghorns. Br. Poult. Sri. 18:213-216. Proudfoot, F. C, 1969. The handling and storage of hatching eggs. Pages 127-141 in: The Fertility and Hatchability of the Hen's Egg. T. C. Carter and B. M. Freeman, ed. Oliver and Boyd, Edinburgh, Scotland.