Genetic Control of Neonatal Growth and Intestinal Maturation in Turkeys

Genetic Control of Neonatal Growth and Intestinal Maturation in Turkeys1 V. L. Christensen,*2 D. T. Ort,* K. E. Nestor,† S. G. Velleman,† and G. B. Havenstein* *Department of Poultry Science, College of Agriculture and Life Sciences, North Carolina State University, Raleigh 27695-7608; and †Department of Animal Sciences, The Ohio State University, Ohio Agriculture and Development Center, Wooster 44691 ABSTRACT Turkey experimental lines E (selected 44 yr for increased egg production) and F (selected 38 yr for increased 16-wk BW) were mated reciprocally with the randombred control lines from which they were derived (RBC1 and RBC2, respectively), and the pure line and reciprocal cross poults were compared according to their hatch, 3- and 7-d BW, jejunum weight, jejunum length, and jejunal maltase and alkaline phosphatase activities. Orthogonal contrasts of the data from the pure line and reciprocal cross-poult data were used to estimate additive genetic effects, reciprocal effects (confounded maternal and sex-linked effects), and heterosis for each of the traits measured. Body weights at hatch and at 3 and 7 d of age

were increased in the F line relative to the RBC2 line and were decreased in the E line relative to the RBC1 line. The genetic changes from long-term selection in the E and F lines have had concomitant effects on jejunum growth and function that parallel the changes in growth rate. The increased BW of the F line poults and the decreased BW of the E line poults relative to their randombred controls may be due to increases in the absorption of nutrients because of greater intestinal mass rather than to differences in glucose digestion. Concomitant changes in egg weight in the 2 selected lines appear to have resulted in maternal effects that have significantly affected neonatal BW and digestive system maturation.

Key words: turkey, body weight, feed conversion, carbohydrate metabolism, inheritance 2007 Poultry Science 86:476–487

We hypothesized that genetic selection of modern turkey sire and dam lines for economically important traits may have had effects on embryo growth or on the development of the intestinal tract during the initial 7 d of life that may have influenced early poult performance. The objective of the current study was to examine the genetic changes that have been brought about in poult growth, neonatal feed conversion, and several aspects of neonatal carbohydrate metabolism from long-term selection for increased egg production or increased 16-wk BW from hatching until 1 wk of age.

INTRODUCTION Poult mortality and embryonic and neonatal growth are known to be influenced by many factors (Phelps et al., 1987a,b,c; Donaldson et al., 1995). These factors include stressors such as temperature and hatchery servicing procedures, prolonged holding without feed or water after hatching, incubation temperature, time of removal from the incubator, age of the breeder flock, genetics, hypercapnia, and poult sex. Each of these risk factors can be traced back to some aspect of carbohydrate metabolism (Donaldson and Christensen, 1994). Data suggest that the best solution to the poult mortality problem may be by stimulating the neonate to eat readily available carbohydrates as soon as possible after hatching. That solution requires an appetite as well as a functional digestive system. Little is known of the influence that genetic selection of turkeys for economically important traits has had on neonatal poult growth and intestinal maturation in the initial week of life.

MATERIALS AND METHODS The lines of turkeys used in the current study were obtained from The Ohio State University and are described by Velleman and Nestor (2004, 2005). In brief, the RBC1 line was developed in 1960 from crossing 4 commercial strains of turkeys in all possible combinations (McCartney, 1964) and has been maintained by a paired mating system as a randombred control without conscious selection (Nestor, 1977a). A subline (E) of the RBC1 line was developed in 1960 and has been selected for the past 44 yr only for increased egg production for various periods of time (Velleman and Nestor, 2005). The E line has been maintained with the same paired mating system. The pure line and reciprocal cross embryos and neonates

©2007 Poultry Science Association Inc. Received October 13, 2006. Accepted November 19, 2006. 1 The mention of trade names in this publication implies neither endorsement of the products mentioned nor criticism of similar products not mentioned. 2 Corresponding author: [email protected]

476

477

EMBRYONIC GROWTH IN TURKEYS

Table 1. Comparison of the BW (g) at hatch and at 3 and 7 d of age of the pure lines and reciprocal crosses of the E line, which has been selected long-term for increased egg number, and its randombred control (RBC1); and of the F line, which has been selected long-term for increased 16wk BW, and its randombred control (RBC2) BW of pure line and reciprocal crosses of the E and RBC1 lines Variable E line sire RBC1 line sire Dam line average

Age, d

E line dam

RBC1 dam

Sire line average

0 3 7 0 3 7 0 3 7

44.8 47.2 61.0 44.5 52.2 73.8 44.65 49.70 67.40

56.7 64.8 88.6 54.9 64.8 94.4 55.80 64.80 91.50

50.75 56.00 74.80 49.70 58.50 84.10 50.22 57.25 79.45

Effect

0

Sire Dam Sire × dam Sire Dam Sire × dam Sire Dam Sire × dam

3 7

Variable

P 0.0797 0.0001 0.2198 0.0004 0.0001 0.0006 0.0001 0.0001 0.0108

Comparison Additive Reciprocal Heterosis Additive Reciprocal Heterosis Additive Reciprocal Heterosis

Age, d

F line dam

RBC2 dam

Sire line average

0 3 7 0 3 7 0 3 7

64.5 79.7 122.7 63.9 77.2 116.7 64.20 78.45 119.70

55.9 72.1 110.4 57.9 69.3 99.5 56.90 70.70 104.95

60.20 75.90 116.55 60.90 73.25 108.10 60.55 74.58 112.32

F line sire RBC2 line sire Dam line average

Genetic test1

ANOVA Age

BW of pure line and reciprocal crosses of the F and RBC2 lines

ANOVA P

Age

0.0001 0.0001 0.2202 0.0001 0.0001 0.0009 0.0001 0.0001 0.1434

0 3 7

Effect Sire Dam Sire × dam Sire Dam Sire × dam Sire Dam Sire × dam

Genetic test P 0.2873 0.0001 0.0347 0.0006 0.0001 0.7854 0.0001 0.0001 0.1858


P 0.0001 0.0001 0.3178 0.0001 0.0001 0.8614 0.0001 0.008 0.1924

1

Orthogonal contrasts: The contrasts for reciprocal effects include confounded maternal and sex-linked effects.

used in the current study were from the 43rd and 44th generations of selection for the E line. Another randombred control line (RBC2), the base population of the F line, was started in 1966 from reciprocal crosses of 2 commercial strains that were representative of commercial turkeys at that time (Velleman and Nestor, 2004), and has been maintained without intentional selection using the same paired mating system. The F line was started in 1966 as a subsample of the RBC2 line and was selected only for increased 16-wk BW over the past 38 yr, and has been maintained using procedures reported previously (Nestor, 1977b). The pure line and reciprocal cross embryos and neonates examined in the current study were from the 37th and 38th generations of selection for the F line. In each of 2 yr, approximately 400 day-old poults from The Ohio State University were delivered to the North Carolina State University Turkey Educational Unit. The poults were brooded and grown using standard procedures in each year. At 37 wk of age, the hens were moved to a curtain-sided house and hens from each of the 4 lines (E, RBC1, F, and RBC2) were distributed randomly by line to each of 12 pens of 6 birds each. The hens were exposed to long days of 15.5 h of light per day to stimulate egg production. Approximately 15 toms from each line were moved to a totally enclosed environmental house located near the hen house and were distributed to 3 pens with 5 birds each. The toms were exposed to 14 h of light per day to stimulate semen production. When the first eggs were produced, half of the hens for the E and F lines were artificially inseminated with semen that was pooled from 9 hatch mate sires of the

same line to reproduce the pure lines. The remaining hens in each of the 2 selected lines were inseminated with semen from the randombred control line from which the selected line had been derived. The same pool of semen was used to inseminate the pure line and reciprocal crosses. Weekly inseminations were performed for a 20wk experimental period. Embryo survival data were recorded at weekly intervals by examining eggs set in the cabinets using standard incubation conditions (Christensen et al., 2005). At wk 16, 17, and 18 of production, embryo survival data were not collected, but embryos were sampled for reciprocal crossing effects on growth and intestinal physiology. In each of 3 trials within each year, 3 embryos (27 d of development) or hatched poults (28 d of development or 3 d posthatching) were sampled as described previously (Christensen et al., 2003b). Intestinal tissue was dissected, weighed (to the nearest microgram), and then quickly frozen (−22°C) in saline for subsequent analysis (Suvarna et al., 2004). Each jejunum was analyzed for maltase and alkaline phosphatase (ALP) activities. Total maltase activity was measured as micromoles of glucose produced per minute for the entire jejunum, and specific maltase activity was measured as micromoles of glucose activity per minute per milligram of protein (Suvarna et al., 2004). Likewise, total ALP activity was measured as micromoles of phosphorus produced per minute for the entire jejunum, and specific ALP was measured as micromoles of ALP activity per minute per gram of protein (Moog, 1950; Suvarna et al., 2004). Within each trial, 240 poults from each of the pure lines and reciprocal crosses were taken to a total confinement

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Table 2. Comparison of feed eaten (g/bird per d) from 0 to 3, 4 to 7, and 0 to 7 d following hatching of pure lines, and reciprocal crosses of the E line, which has been selected long-term for increased egg number, and its randombred control (RBC1); and of the F line, which has been selected long-term for increased 16-wk BW, and its randombred control (RBC2) Amount of feed eaten by pure line and reciprocal crosses of the E and RBC1 lines1 Variable E line sire RBC1 line sire Dam line average

Age, d

E line dam

RBC1 dam

Sire line average

0–3 4–7 0–7 0–3 4–7 0–7 0–3 4–7 0–7

3.1 9.1 6.2 5.1 13.5 9.5 4.3 10.1 7.3

5.5 11.1 8.4 5.5 12.7 9.2 5.3 12.1 9.3

4.1 11.3 7.8 5.5 11.9 7.8 3.1 9.1 6.2

Effect

0–3


4–7 0–7

Variable

Age, d

F line dam

RBC2 dam

Sire line average

0–3 4–7 0–7 0–3 4–7 0–7 0–3 4–7 0–7

6.7 15.4 11.2 6.3 13.8 10.2 6.4 14.8 10.7

6.3 13.8 10.2 5.5 11.8 8.8 5.9 12.8 9.4

6.5 14.6 10.7 5.8 12.9 9.5 6.7 15.4 11.2


Genetic test2

ANOVA Age, d

Amount of feed eaten by pure line and reciprocal crosses of the F and RBC2 lines1

P 0.2371 0.0199 0.1259 0.6859 0.0464 0.3274 0.0093 0.0684 0.0464


Genetic test2

ANOVA P

Age, d

0.0037 0.5699 0.0820 0.0961 0.2514 0.3381 0.0132 0.3879 0.1222

0–3 4–7 0–7


P 0.0019 0.0641 0.9263 0.0012 0.0001 0.4272 0.0002 –0.0002 0.4446


P 0.8868 0.3994 0.1236 0.0215 0.4051 0.0970 0.0049 0.1957 0.0089

1

Feed eaten per day (g/bird per d). Orthogonal contrasts: The contrasts for reciprocal effects include confounded maternal and sex-linked effects.

2

facility that contained 2 Petersime battery brooders (Petersime, Gettysburg, OH) with 12 pens each. Ten poults per treatment combination were placed randomly into each of 3 replicate pens. The poults were brooded using standard conditions for 7 d. The poults were weighed (to the nearest 0.1 g) at hatch and at 3 and 7 d of age. Feed consumption was measured (to the nearest gram) at 3 and 7 d to estimate feed conversion from 0 to 3 d, 4 to 7 d, and 0 to 7 d for each of the pure lines and their reciprocal crosses. The entire experiment was replicated in 3 trials during 2 consecutive generations. Statistical analyses were performed using the GLM procedure of SAS (SAS Institute, 1998) with both year and trial considered to be fixed factors. Two primary data sets were produced that included each selected line and its randombred control line (i.e., E and RBC1, and F and RBC2) mated as pure lines and in both reciprocal cross combinations to determine the genetic changes that had taken place because of the history of selection of the E and F strains for increased egg production or increased 16-wk BW, respectively. Thus, each data set contains information on poults from the 2 pure lines and their reciprocal crosses from the selected line and the respective randombred control from which it had been derived. No significant effects attributable to trial or year could be detected; therefore, trial and year were pooled across other factors. For the physiological traits measured, BW was used as a covariate in the ANOVA to determine whether effects seen in the absolute data were simply due to changes in BW. Orthogonal contrasts (Emmerson et al., 2002) were used to test for addi-

tive, reciprocal (confounded sex-linked, maternal, or both), and heterotic gene effects. The comparison of the 2 pure lines (i.e., E vs. RBC1 and F vs. RBC2) was used as a measure of additive variation. Heterosis was measured as the deviation of the mean of the reciprocal crosses from the mean of the 2 parental lines. The difference between the 2 reciprocal crosses was used to measure maternal or sex-linked effects, which are confounded in these data.

RESULTS BW Table 1 summarizes the BW data from the 2 sets of pure lines and their reciprocal crosses. For the E and RBC1 lines, the RBC1 sires and dams produced heavier poults at hatching than did the E sires and dams, and the pure line E poults were approximately 18% lighter than the pure line RBC1 poults. The reciprocal crosses were intermediate in weight between the 2 pure lines, but the crosses from the RBC1 line dams mated with the E sires were about 27% heavier at hatch than crosses from the E dams mated with the RBC1 sires. These general relationships held throughout the 7-d experimental period, except that by 7 d of age, the pure line E poults were about 54% lighter than the pure line RBC1 poults. A sire × dam interaction was present at 3 d of age, where the difference between the offspring of the E and RBC1 dams was significantly larger than the difference between the E and RBC1 sires.

479


Table 3. Comparison of the feed conversions (g of feed/g of BW) at 0 to 3, 4 to 7, and 0 to 7 d of age of the pure lines and reciprocal crosses of the E line, which has been selected long-term for increased egg number, and its randombred control (RBC1); and of the F line, which has been selected long-term for increased 16-wk BW, and its randombred control (RBC2) Feed conversions of pure lines and reciprocal crosses of the E and RBC1 lines Variable E line sire RBC1 line sire Dam line average

Age, d

E line dam

RBC1 dam

Sire line average

0–3 4–7 0–7 0–3 4–7 0–7 0–3 4–7 0–7

0.20 0.76 0.77 0.32 0.76 0.73 0.260 0.760 0.750

0.23 0.73 0.72 0.25 0.65 0.63 0.240 0.690 0.675

0.215 0.745 0.745 0.285 0.705 0.680 0.250 0.725 0.712

Effect

0–3


4–7 0–7

Variable

Age, d

F line dam

RBC2 dam

Sire line average

0–3 4–7 0–7 0–3 4–7 0–7 0–3 4–7 0–7

0.25 0.62 0.58 0.26 0.61 0.60 0.25 0.61 0.59

0.24 0.60 0.57 0.24 0.58 0.57 0.24 0.59 0.57

0.26 0.62 0.59 0.23 0.59 0.57 0.24 0.57 0.57


Genetic test1

ANOVA Age, d

Feed conversions of pure lines and reciprocal crosses of the F and RBC2 lines

P 0.0093 0.0133 0.0515 0.6785 0.4138 0.6920 0.4958 0.4335 0.8199


Genetic test1

ANOVA P

Age, d

0.0694 0.0400 0.1653 0.4102 0.7861 0.7078 0.3454 0.9469 0.8354

0–3 4–7 0–7


P 0.0304 0.3749 0.5781 0.0284 0.2913 0.8421 0.0715 0.4808 0.5723


P 0.5432 0.1599 0.7198 0.4693 0.7939 0.9509 0.7211 0.4231 0.8006

1


For BW data from the F and RBC2 lines, the poults from the F line sires were heavier than those from the RBC2 line sires at 3 and 7 d, but not at hatch (Table 1). Poults from the F line dams were consistently heavier than those from the RBC2 dams at all 3 ages measured. The pure line F poults were about 11% heavier than the pure line RBC2 poults at hatch, and this difference had increased to 23% by 7 d of age. As with the reciprocal crosses between the E and RBC1 lines, the reciprocal crosses between the F and RBC2 lines were intermediate in weight between the 2 pure lines, and the crosses from the F line dams mated with the RBC2 sires were about 14% heavier than crosses from the RBC2 dams mated with the F sires. This difference in the reciprocal crosses had decreased to about 6% by 7 d of age. A sire × dam interaction was present at hatch, indicating that the difference in the BW between the F and RBC2 dams was significantly larger than the hatch weights between the offspring from the F and RBC2 sires. This interaction was not present in the 3- and 7-d data. Highly significant additive and sex-linked or maternal effects (reciprocal) were present for BW at all 3 ages studied for both sets of BW data (Table 1). With the exception of significant heterosis (−7.7%) for BW at 3 d of age for the E × RBC1 crosses, none of the tests for heterosis was significant for either BW data set.

Appetite Feed consumption data are summarized in Table 2. Pure line E poults consistently ate less feed than did their control counterparts. Reciprocal crosses between the E

and RBC1 lines resulted in significant dam effects at both 0 to 3 d and 4 to 7 d of age and a significant sire × dam interaction when feed consumed was viewed from 0 to 7 d of age. The F sires and dams showed increased feed consumption at all 3 ages in comparison with the sires and dams from the RBC2 line, with no sire × dam interaction for feed consumption or appetite. Except for 4 to 7 d of age, highly significant additive effects for feed consumption were present for feed consumption at all 3 ages studied for the E and RBC1 data (Table 2). None of the tests for reciprocal or heterosis effects was significant for either BW data set. In the comparison of F and RBC2 lines, a significant additive effect was seen at 4 to 7 d of age, and at 0 to 7 d of age, significant heterosis effects were noted.

Feed Conversion Feed conversion data are summarized in Table 3. Pure line E poults had consistently poorer (higher) 0- to 7-d feed conversion than did RBC1 poults. Reciprocal crosses between the E and RBC1 lines were intermediate between the 2 pure lines in their feed conversion. The only significant effects present for the E and RBC1 data set were a lower 0- to 3-d feed conversion in the poults from the E line sires than those from the RBC1 line sires, and a sire × dam interaction, in which the difference in the feed conversion of poults from the E and RBC1 sires was significantly larger than the difference in the feed conversion of poults from the E and RBC1 dams. Comparison of the F and RBC2 lines showed that progeny from the F line sires had higher feed conversions that

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Table 4. Comparison of jejunal weights (mg) at pipping (P), hatching (H), and 3 d of age of the pure lines and reciprocal crosses of the E line, which has been selected long-term for increased egg number, and its randombred control (RBC1); and of the F line, which has been selected longterm for increased 16-wk BW, and its randombred control (RBC2) Jejunal weights of pure line and reciprocal crosses of the E and RBC1 lines Variable

Age

E line dam

RBC1 dam

Sire line average

E line sire

P H 3d P H 3d P H 3d

200 301 933 263 392 1,174 231.5 346.5 1,053.5

209 351 992 271 428 1,171 240.0 389.5 1,081.5

205.5 326.0 962.5 267.0 410.0 1,172.5 235.8 368.0 1.067.5

RBC1 line sire Dam line average

Effect

P


H 3d

Variable

Age

F line dam

RBC2 dam

Sire line average

F line sire


321 538 1,915 304 494 1,839 312.5 516.0 1,877.0

298 448 1,733 255 412 1,535 282.0 430.0 1,634.0

309.5 493.0 1,824.0 285.0 453.0 1,687.0 297.2 473.0 1,755.5


Genetic test1

ANOVA Age

Jejunal weights of pure line and reciprocal crosses of the F and RBC2 lines

P 0.4340 0.0001 0.9374 0.0090 0.0001 0.6311 0.7272 0.0105 0.6957


Genetic test1

ANOVA P 0.0001 0.0013 0.9409 0.0001 0.1770 0.7295 0.0394 0.1100 0.6986

Age

Effect

P


H 3d

P 0.1361 0.0471 0.6270 0.1468 0.0027 0.8893 0.1839 0.0213 0.5492


P 0.0340 0.8225 0.9048 0.0069 0.3042 0.9048 0.0069 0.4842 0.5665

1


those from the RBC2 line sires at 0 to 3 d and at 4 to 7 d (Table 3). No significant sire × dam interactions were found in this comparison.

Weight of the Jejunum The absolute weight of the jejunum was significantly lower at pipping and at 3 and 7 d of age in poults produced by E line sires and dams than in poults from RBC1 sires and dams (Table 4). The absolute weight of the jejunum from the reciprocal crosses was intermediate that of the pure lines except at 7 d, when the jejunal weights of the poults from RBC1 sires mated with the E dams were equal to those of the poults from the RBC1 pure line matings. Dam line effects were significant at all 3 ages tested, but sire line effects were significant only at hatch. No significant sire × dam interactions were present for the jejunal weights of the E and RBC1 pure lines and their reciprocal crosses. The absolute jejunal weights were consistently higher in the pure line F poults than in the pure line RBC1 poults (Table 4). Jejunal weights of the reciprocal crosses of these 2 lines were intermediate between the 2 pure lines. As with the BW data, the jejunal weights of poults from the RBC2 sires mated with the F line dams were consistently heavier than those for poults from the F line sires mated with the RBC2 dams. As with the BW data, the genetic analyses of jejunal weights indicated that the changes seen were controlled by additive gene effects (Table 4). However, none of the reciprocal cross-genetic comparisons showed evidence of

maternal or sex-linked effects or of the presence of heterosis. The absolute weights of the jejunum were also analyzed using BW as a covariate (data not shown) to test the relative jejunal weights when the effects of BW had been removed. None of the sire, dam, or sire × dam interaction effects was significant for the BW-adjusted jejunal weights from either data set.

Length of the Jejunum Data for the length of the intestinal jejunum are presented in Table 5. The differences in the lengths of the jejunum between the poults from the E and RBC1 dams were significant at all 3 ages studied. Poults from the RBC1 dams had consistently longer jejuna than did poults from the E line dams. Poults from the RBC1 sires also had consistently longer jejuna than did poults from the E sires, but none of the sire line differences was significant. None of the sire × dam interactions for jejunal length between the E and RBC1 lines was significant. Likewise, the differences in jejunal length for poults produced by the F and RBC2 line dams were highly significant at the 3 ages measured (Table 5). As with the first data set summarized above, the differences in jejunal length from the F and RBC2 sires were not significant at any age measured with the exception of at 3 d of age. Again, as with the first data set, none of the sire × dam interactions for jejunal length was significant. Genetic analyses for jejunal length were inconsistent (Table 5). Three of the 6 analyses performed showed the

481


Table 5. Comparison of jejunal lengths (cm) at pipping (P), hatching (H), and 3 d of age of the pure and reciprocal crosses of the E line, which has been selected long-term for increased egg number, and its randombred control (RBC1); and of the F line, which has been selected long-term for increased 16-wk BW, and its randombred control (RBC2) Jejunal lengths (cm) of pure line and reciprocal crosses of the E and RBC1 lines Variable

Age

E line dam

RBC1 dam

Sire line average

E line sire


9.2 10.5 16.0 9.2 11.2 17.3 9.20 10.80 16.65

10.3 12.0 18.7 9.8 11.2 17.3 10.05 11.60 18.00

9.75 11.25 17.37 10.05 11.60 18.00 9.62 11.42 17.68


Effect

P


H 3d

Variable

Age

F line dam

RBC2 dam

Sire line average

F line sire


11.6 13.7 23.0 11.8 13.7 21.6 11.70 13.70 22.30

10.7 13.0 20.4 10.9 12.2 18.3 10.80 12.60 19.35

11.15 13.35 21.70 11.35 12.95 19.95 11.25 13.15 20.82


Genetic test1

ANOVA Age

Jejunal lengths (cm) of pure line and reciprocal crosses of the F and RBC2 lines

P 0.3684 0.0012 0.2390 0.8672 0.0156 0.0750 0.5345 0.0073 0.1228


Genetic test1

ANOVA P 0.1391 0.0135 0.3270 0.1204 0.1733 0.1323 0.0500 0.1634 0.1851

Age

Effect

P


H 3d

P 0.3612 0.0033 0.2929 0.5100 0.0031 0.8472 0.0065 0.0001 0.5107


P 0.1488 0.0269 0.8665 0.0082 0.1392 0.3083 0.0001 0.2051 0.5433

1


presence of significant additive genetic effects for jejunal length, and 2 showed significant reciprocal (maternal or sex-linked) effects.

Jejunal Maltase Activity Total and specific maltase activity in the jejunum of the pure lines and their reciprocal crosses for the 2 data sets at the time of pipping (∼27 d of incubation), hatch, and 3 d of age are provided in Tables 6 and 7, respectively. The total jejunal maltase data from the E and RBC1 lines (Table 6) indicated that significant dam effects were present at hatch and 3 d of age, with the RBC1 poults having higher total maltase levels that the poults from the E line dams. None of the sire effects between these 2 lines was significant for total maltase activity. A significant sire × dam interaction was present for total maltase activity from the E and RBC1 lines at 3 d of age, where the difference between the E and RBC1 dams was much larger than and in the opposite direction from the difference between the E and RBC1 sires. Total maltase activity for the F and RBC2 lines (Table 6) showed no significant differences in sire line or dam line effects. The only significant difference was in the sire × dam interaction at pipping, where the difference in total maltase activity of the poults from F line and RBC2 line sires was significantly larger than the difference in total maltase activity of the poults from F and RBC2 line dams. Genetic analyses of total maltase activity from the 2 sets of data provided very little evidence for specific modes of genetic control, with only 1 of 6 analyses being significant for additive effects and another 1 of 6 being significant

for maternal or sex-linked effects (Table 6). The data on specific jejunal maltase activity showed no evidence of significant sire line, dam line, or sire × dam effects for either of the 2 data sets at these ages (Table 7). None of the genetic tests from the 2 total maltase data sets was significant.

Jejunal ALP Activity Total and specific ALP activities in the jejuna of the pure lines and their reciprocal crosses for the 2 data sets at the time of pipping (∼27 d of incubation), hatch, and 3 d of age are provided in Tables 8 and 9, respectively. For total ALP activity (Table 8), significant sire and dam line effects were present in neonatal poults from the E and RBC1 lines at all of the ages tested, except for sire effects at hatch. A significant sire × dam line interaction was also present for data from these 2 lines at pipping, in which the difference between the levels of ALP was significantly larger in poults from the sires of the 2 lines than in poults from the dams of the 2 lines. This interaction was not present at the time of hatch or at 3 d of age. The genetic analyses of the E and RBC1 line total ALP data indicated that significant additive effects were present at all times measured (Table 8). None of the other genetic analyses showed significant effects as being present. Total ALP data from the F and RBC2 lines were not as clear as those from the E and RBC1 lines (Table 8). Significant sire line effects were present at pipping for the F and RBC2 data, but not at hatch or 3 d of age. None of the dam line effects was significant for these lines. A

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Table 6. Comparison of total jejunal maltase activity at pipping (P), hatching (H), and 3 d of age of the pure lines and reciprocal crosses of the E line, which has been selected long-term for increased egg number, and its randombred control (RBC1); and of the F line, which has been selected long-term for increased 16-wk BW, and its randombred control (RBC2) Total maltase activity1 of pure line and reciprocal crosses of the E and RBC1 lines Variable

Age

E line dam

RBC1 dam

Sire line average

E line sire


84 229 668 82 266 715 83.0 247.5 691.5

82 321 1,234 113 370 824 97.5 345.5 1,029.0

83.0 275.0 951.0 97.5 318.0 769.5 90.2 296.5 860.2

RCB1 line sire Dam line average

Age

Effect

P

Comparison

P


0.2685 0.2878 0.2070 0.3080 0.0228 0.8846 0.1876 0.0229 0.0486

Additive Reciprocal Heterosis Additive Reciprocal Heterosis Additive Reciprocal Heterosis

3d

Variable

Age

F line dam

RMC2 dam

Sire line average

F line sire


110 404 865 128 338 733 119.0 371.0 799.0

130 353 832 91 412 843 110.5 382.5 837.5

120.0 378.5 848.5 109.5 375.0 788.0 114.8 376.8 818.2


Genetic test2

ANOVA

H

Total maltase activity1 of pure line and reciprocal crosses of the F and RBC2 lines

Genetic test2

ANOVA P 0.1167 0.9741 0.1937 0.0210 0.3523 0.8850 0.5048 0.0256 0.1385

Age

Effect

P


H 3d

P 0.5335 0.5868 0.0432 0.9469 0.8200 0.2108 0.5785 0.7241 0.5088


P 0.4210 0.9561 0.1002 0.9085 0.8338 0.2138 0.9110 0.6174 0.6070

1

Total maltase activity (␮mol of glucose/min per jejunum). Orthogonal contrasts: The contrasts for reciprocal effects include confounded maternal and sex-linked effects.

2

significant sire × dam line interaction was present for total ALP at hatch, but not at pipping or at 3 d of age. This interaction indicated that the difference in the levels of total ALP between poults from the sires of the 2 lines was significantly larger than the difference in the levels between poults from the dams of the 2 lines. As with total maltase, the results from genetic analyses for total ALP were again mixed (Table 8). Three of the 6 analyses indicated the presence of significant additive gene effects, and 3 of the 6 also showed the presence of significant levels of heterosis. Results from the analyses of the levels of specific ALP produced, or the amounts produced per gram of protein, from the 2 data sets are summarized in Table 9. These data mirror results from the analyses of total ALP in that the sire line effects were significant at pipping and at 3 d of age, but not at hatch. None of the dam line effects was significant. The sire × dam line interaction was present only at pipping; similar to the total ALP results, the difference in specific ALP levels at pipping in poults of the 2 sire lines was significantly larger than the difference in poults from the 2 dam lines.

DISCUSSION Selection of turkeys and chickens for economically valued traits may have increased metabolic disorders such as round heart in turkeys (Hunsaker, 1971) or ascites in broilers (Balog, 2003). Commercial turkeys are the result of a cross between a sire line, or a sire line cross, that has been selected primarily for increased growth and

improved feed efficiency and 1 or 2 dam lines that have been selected for increased growth, improved feed efficiency, and increased egg production. The sire line is usually selected exclusively for increased growth rate and feed efficiency, whereas the dam lines are selected for reproductive and growth traits (Velleman and Nestor, 2005). Little is known about sire line or dam line effects on the performance status of hatchling turkey poults. However, when infectious diseases are discounted, the major mortalities during brooding and rearing are weak poults and “starve-outs” (Christensen et al., 2003a). As many as 10% of the poults may suffer some sort of problem caused by management during the initial stages of life. Management-related problems during brooding and growing have been estimated as accounting for greater than 6% of mortality and for 10 to 30% of growth depressions. Weak poults may also be a function of metabolic disorders related to the transition from the egg to the precoccial poult (Noble et al., 1999; Christensen et al., 2003b). Many factors have been suggested (Donaldson et al., 1995) as affecting poult mortality. Factors such as hatchery holding temperatures, hatchery servicing procedures (Donaldson et al., 1991), prolonged holding without feed or water after hatching, incubation temperature (Christensen et al., 2003b), time of removal from the hatcher (Christensen and Donaldson, 1992), age of the breeder flock (Christensen et al., 2001), genetics (Hunsaker, 1971), hypercapnia (Donaldson et al., 1995), and poult sex can affect poult mortality. Each of these risk factors can be traced to some aspect of carbohydrate metabolism (Don-

483


Table 7. Comparison of specific jejunal maltase activity at pipping (P), hatching (H), and 3 d of age of the pure line and reciprocal crosses of the E line, which has been selected long-term for increased egg number, and its randombred control (RBC1); and of the F line, which has been selected long-term for increased 16-wk BW, and its randombred control (RBC2) Specific maltase activity1 of pure line and reciprocal crosses of the E and RBC1 lines Variable

Age

E line dam

RBC1 dam

Sire line average

E line sire


7.9 9.9 9.1 7.2 10.5 9.0 7.55 10.20 9.05

6.4 11.0 14.4 8.1 11.9 8.4 7.25 11.25 11.40

7.15 10.45 11.75 7.65 11.2 8.70 7.40 10.75 10.22


Effect

P


H 3d

Variable

Age

F line dam

RBC2 dam

Sire line average

F line sire


7.0 11.9 6.5 8.6 10.6 5.8 7.80 11.25 6.15

8.7 12.0 6.7 7.1 13.7 8.0 7.90 12.85 7.35

7.85 11.95 6.60 7.85 12.15 6.90 7.85 376.8 6.75


Genetic test2

ANOVA Age

Specific maltase activity1 of pure line and reciprocal crosses of the F and RBC2 lines

P 0.5428 0.7274 0.1531 0.5620 0.3408 0.8723 0.1977 0.3131 0.2148


Genetic test2

ANOVA P 0.8642 0.5307 0.1843 0.2847 0.7921 0.8736 0.8437 0.1033 0.2070

Age

Effect

P


H 3d

P 0.9825 0.9089 0.1403 0.8934 0.2567 0.3012 0.7986 0.2663 0.3377


P 0.9535 0.9315 0.1875 0.3714 0.4793 0.3038 0.3914 0.5890 0.3954

1

Total maltase activity (␮mol of glucose/min per jejunum). Orthogonal contrasts: The contrasts for reciprocal effects include confounded maternal and sex-linked effects.

2

aldson et al., 1995; Christensen et al., 2003b; Suvarna et al., 2005). Little carbohydrate remains in turkey eggs (Romanoff, 1967), and because of the limited supply of carbohydrate, severe or prolonged stress can be life-threatening in poults before feeding or intestinal maturation (Donaldson and Christensen, 1994). In unfed, newly hatched turkeys, depletion of yolk sac and body proteins is required for carbohydrate production via gluconeogenesis. The current study examined the influence of genetic line on some aspects of carbohydrate metabolism using 2 randombred pure lines and 2 other lines that had originated from the randombred controls, and that had in 1 case been selected only for increased 16-wk BW and in the other case been selected only for increased egg production, when mated in pure and reciprocal combinations with their associated randombred and selected line combinations. Several economically important traits, as well as several aspects of carbohydrate metabolism, were studied in pure line and cross-line neonatal poults to determine whether the traits were controlled by additive, maternal, or sex-linked effects and whether heterosis was evident in the performance of the crosses.

BW The genetic analyses of BW from both sets of pure line and reciprocal crosses indicated that the genetic changes that have taken place in hatch and neonate BW, either indirectly from selection for increased egg production in the E line or directly from selection for increased 16-wk BW in the F line, have come about from additive genetic

changes or sex-linked or maternal effects. No evidence of heterosis for BW was found at any of the 3 ages studied. This is different from what Emmerson et al. (2002) observed for BW measured at 8, 16, and 20 wk of age and at 50% production. In their study, a highly significant level of heterosis was present at all ages studied. Long-term selection for increased egg production and long-term selection for 16-wk BW have both affected embryonic and neonatal growth rates. In agreement with data from later ages (Nestor et al., 1996; Emmerson et al., 2002), selection for increased egg production has reduced the growth rate of the E line poults compared with the growth rate of the RBC1 controls from which the E line was derived. This result was probably not expected at the beginning of the selection process because, of the few published estimates of the genetic correlation between BW and egg production in turkeys, the average was close to zero (Arthur and Abplanalp, 1975). Nevertheless, as was pointed out by Nestor et al. (1996) and by Emmerson et al. (2002), the genetic correlation between egg production and BW has changed several times during the 38 generations of selection in the E line, and has resulted in a dramatic decrease in BW and egg size as concomitant effects of selecting for increased egg number. On the other hand, the BW of the F pure line poults has dramatically increased from the BW of their RBC2 line (Nestor et al., 1996). Egg weight has also increased substantially (0.32 g/generation of selection; Nestor et al., 1996) in the F line. These changes are in good agreement with changes that have taken place in the growth rate of commercial turkeys, where it has recently been shown that commercial

484

CHRISTENSEN ET AL.

Table 8. Comparison of total jejunal alkaline phosphatase activity at pipping (P), hatching (H), and 3 d of age of the pure lines and reciprocal crosses of the E line, which has been selected long-term for increased egg number, and its randombred control (RBC1); and of the F line, which has been selected long-term for increased 16-wk BW, and its randombred control (RBC2) Total alkaline phosphatase activity1 of pure line and reciprocal crosses of the E and RBC1 lines Variable

Age

E line dam

RBC1 dam

Sire line average

E line sire


720 5,005 33,463 972 8,104 49,832 846.0 6,554.5 41,647.5

847 9,841 46,568 1,735 11,082 56,778 1,291.0 10,461.5 51,673.0

783.5 7,423.0 40,015.5 1,353.5 9,593.0 53,305.0 1,068.5 8,508.0 46,660.2


Effect

P


H 3d

Variable

Age

F line dam

RBC2 dam

Sire line average

F line sire


2,553 17,502 79,333 2,425 10,033 73,671 2,489.0 13,767.5 76,502.0

3,095 11,410 67,429 1,483 16,513 63,172 2,289.0 13,961.5 65,300.5

2,824.0 14,456.0 73,381.0 1,954.0 13,273.0 68,421.5 2,389.0 13,864.5 70,901.2


Genetic test2

ANOVA Age

Total alkaline phosphatase activity1 of pure line and reciprocal crosses of the F and RBC2 lines

P 0.0044 0.0238 0.0506 0.2776 0.0541 0.6399 0.0192 0.0457 0.6488


Genetic test2

ANOVA P 0.0005 0.6457 0.1021 0.0392 0.5466 0.6480 0.0076 0.6379 0.6632

Age

Effect

P


H 3d

P 0.0274 0.6546 0.1032 0.6149 0.9341 0.0100 0.4851 0.1193 0.9210


P 0.1037 0.3085 0.0966 0.7638 0.6756 0.0093 0.1064 0.5277 0.9198

1

Total alkaline phosphatase activity (␮mol of phosphorus/min per jejunum). Orthogonal contrasts: The contrasts for reciprocal effects include confounded maternal and sex-linked effects.

2

turkeys in 2003 were approximately twice as large at a given age as the RBC2 turkeys (Havenstein et al., 2004a,b). Based on the above discussion, we suspect that the presence of positive reciprocal effects (i.e., confounded maternal and sex-linked effects) in both the E and F line data sets are at least partially due to the changes that have taken place in egg size for the 2 selected lines. The E line currently has a much smaller egg size than the RBC1 (19 g/egg in the 44th generation; Nestor, unpublished data), and the change in egg size has been documented in several published studies (Nestor et al., 1982, 1996; Christensen and Nestor, 1994; Nestor and Noble, 1995; Emmerson et al., 2002). The reduced egg size (Emmerson et al., 2002) is an expected genetically correlated response to selection for increased egg number (Arthur and Abplanalp, 1975). Long-term selection for 16-wk BW has had a dramatic effect by increasing the egg weight (Nestor et al., 1982, 1996; Nestor and Noble, 1995) and poult weight of the F line. Again, this is expected because BW and egg weight have a strong positive genetic correlation in avian species (Kinney, 1969); therefore, selection for increased BW should increase concomitantly with egg weight. Residual yolk was measured at all developmental stages, and the levels of yolk were consistently reduced at all times in the poults from E line dams in comparison with those from RBC1 dams (data not shown). This is consistent with the findings of Nestor and Noble (1995), who found that the reduction of egg weight in the E line

was due to a proportional reduction in all component parts of the egg.

Appetite and Feed Conversion Poults from the E line have been reported to be weak (Noble et al., 1999; Christensen et al., 2003a); therefore, observations with this line may be associated with increased poult mortality. Selection for increased egg production has resulted in poults of the pure E line sires and dams showing reduced appetite and embryo BW. This reduction in embryo weight appears to be affected by both maternal or sex-linked effects and additive gene effects, whereas appetite appears to be affected by both dam and sire as additive effects. The pure line E poults not only grew more slowly, but they also had poorer (higher) feed conversion ratios from 0 to 7 d and from 3 to 7 d of age. Feed conversion was affected by both maternal or sex-linked and additive gene effects. In an orthogonal comparison, the line cross poults provided evidence that heterosis was present in the feed conversion ratios at 0 to 3 d, but not at 4 to 7 d or 0 to 7 d. Christensen and Nestor (1994) speculated that the dam effects may be mediated through physical and functional qualities of eggs from the E line. Increased appetite and BW of the F line, compared with RBC2 poults, was readily apparent and was due to both additive and heterosis effects. Poults from F line sires had improved (lower) feed conversion ratios in comparison

485


Table 9. Comparison of specific jejunal alkaline phosphatase activity at pipping (P), hatching (H), and 3 d of age of the pure lines and reciprocal crosses of the E line, which has been selected long-term for increased egg number and its randombred control (RBC1), and of the F line, which has been selected long-term for increased 16-wk BW, and its randombred control (RBC2) Specific alkaline phosphatase activity1 of pure line and reciprocal crosses of the E and RBC1 lines Variable

Age

E line dam

RBC1 dam

Sire line average

E line sire


0.07 0.22 0.43 0.08 0.31 0.58 0.075 0.370 0.505

0.06 0.32 0.51 0.13 0.35 0.63 0.095 0.335 0.570

0.065 0.270 0.475 0.110 0.330 0.605 0.850 0.300 0.540


Effect

P


H 3d

Variable

Age

F line dam

RBC2 dam

Sire line average

F line sire


0.17 0.51 0.60 0.15 0.32 0.60 0.160 0.420 0.600

0.20 0.38 0.56 0.12 0.53 0.58 0.160 0.455 0.570

0.185 0.395 0.580 0.135 0.425 0.590 0.160 0.438 0.585


Genetic test2

ANOVA Age

Specific alkaline phosphatase activity1 of pure line and reciprocal crosses of the F and RBC2 lines

P 0.0045 0.1686 0.0477 0.2982 0.2171 0.5851 0.0392 0.4072 0.9584


Genetic test2

ANOVA P 0.0047 0.2836 0.0907 0.1266 0.8934 0.6020 0.0753 0.4102 0.9642

Age

Effect

P


H 3d

P 0.0497 0.8905 0.2459 0.7481 0.4640 0.0064 0.8021 0.5708 0.7720


P 0.1647 0.2273 0.2631 0.7660 0.4674 0.0068 0.8298 0.5797 0.7812

Specific alkaline phosphatase activity (␮mol of phosphorus/min per ␮g of protein). Orthogonal contrasts: The contrasts for reciprocal effects include confounded maternal and sex-linked effects.

1 2

with poults produced by the pure line RBC2 control. The pure line F poults had consistently improved feed conversion in comparison with the RBC2 pure line poults. Crossline performance for feed conversion was less predictable, with significant sire line × dam line interactions present for 4- to 7-d and 0- to 7-d feed conversion.

Jejunum Weight and Length The E pure line poults, in comparison with poults from the RBC1 pure line from which the E line was originally derived, had reduced jejunum weights that were in proportion to the reduction in BW, and in addition, the length of their intestines was reduced. The performance of the reciprocal crosses provided evidence that both weight and length of the jejunum is controlled by additive gene effects. During the initial period after hatching, the weight of demand organs of growth-selected animals increases to a greater extent than does BW (Lilja, 1981, 1983; Sell et al., 1991; Obst and Diamond, 1992), but Lilja (1983) also indicated that the growth of supply organs of birds selected for increased BW may be slower than that for demand organs. In birds, energy available for growth is partly limited by the size of the digestive tract (a supply organ) and early investment of growth resources in development of this organ favors a subsequently high growth rate capacity (Mitchell and Smith, 1991). Increases in the weight and length of the small intestine are common mechanistic adaptations for increased growth. In the cur-

rent study, jejunum weight increased from approximately 0.5% of the body mass in all lines at hatching to approximately 2.0% of BW in E poults and 2.5% of BW in F poults at 3 d of age. Thus, jejunum tissue grew more rapidly than the body in F line poults selected for increased BW and more slowly when selected for increased egg production than in their respective control lines. This relationship is in contrast to prior results (Konarzewski et al., 1990) suggesting that bird intestinal and whole body growth parallel one another. When jejunum weights of poults of 2 BW were compared (Suvarna et al., 2004), changes in jejunum weight and BW also did not parallel each other. Changes in jejunum weight and length of both the F and E lines were mediated primarily by the dam, but in the E line, declines in relative jejunum growth also included sire effects. This was obviously advantageous to F line poults, because these birds grew faster and had lower feed conversion ratios than did their counterparts. Because of the dam, the rapid increase in intestinal mass and consequent increase in total maltase and ALP ensures that the bird from the F line is ready to meet the increased demand of nutrients to maintain tissue and promote growth, as well as to accommodate some reserve capacity, in agreement with prior research (Mitchell and Smith, 1991; Ferrais and Diamond, 1997). Conversely, data from E line neonates may infer that the E line poults were not adequately prepared to grow for similar reasons.

Total and Specific Jejunal Maltase Activity Jejunum maltase function was affected only by the growth of the tissue and not by increased specific maltase

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CHRISTENSEN ET AL.

activity. Maltase activity was significantly lower in the E pure line than in the RBC1 pure line hatchlings and 3-dold poults, and this effect was observed to be additive in nature. Lower levels of alkaline phosphatase activity in E pure line poults compared with RBC1 pure line poults indicate a lower metabolic activity for jejunal tissue. The increase in total maltase activity of the F by RBC2 pure line and cross line poults paralleled the increases in jejunum weight and length. Therefore, no effect on specific maltase activity or type of inheritance was evident.

Total and Specific Jejunal ALP Activity Analysis of ALP activity levels showed that embryos from F line sires had increased activity compared with embryos from RBC2 sires, and orthogonal contrasts comparing the reciprocal crosses in relation to the 2 pure lines indicated that heterosis was present at hatching. Progeny of the E line sires had decreased ALP activity, but the only significant orthogonal contrast was for additive gene effects at pipping. Neonatal poults utilize glucose from gluconeogenic amino acids as the preferred substrate immediately posthatching (Donaldson and Christensen, 1994), and previous studies have indicated that low-BW poults have greater gluconeogenic activity (glucose-6-phosphatase activity) than do heavy poults (Christensen et al., 2000). The jejunum must be able to digest and absorb carbohydrates immediately posthatch to enable poults to survive. Total maltase activity was decreased in E and increased in F poults compared with their respective randombred control lines, but at a greater rate in the F than the E line. Thus, maltase activity was changed in each line by increasing or decreasing jejunum mass and length as seen previously (Suvarna et al., 2004), rather than by increasing specific activity. In summary, long-term selection for increased egg production of the E line has reduced the BW at hatching and has led to a slower posthatching growth rate and reduced overall body size at all ages. Conversely, long-term selection for increased 16-wk BW has significantly increased the BW of F line poults. Genetic changes from long-term selection in the E and F lines have had concomitant effects on jejunum growth and function that parallel the changes in growth rates. The increased BW of F line poults and the decreased BW of E line poults may be due to increases in absorption of all nutrients because of greater intestinal mass rather than to differences in glucose digestion (Mitchell and Smith, 1991). Concomitant changes in egg weight in the 2 selected lines appear to have resulted in maternal effects that significantly affect neonatal BW and digestive system maturation. Reduced egg size may be a major factor contributing to reduced poult weight and jejunum development, and is probably involved in the weak poults observed in the E line (Noble et al., 1999). Concomitant changes in length of the developmental periods of both selected lines may also play a role in the level of maturity at hatching (Christensen et al., 2001).

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