Developmental Instability in Japanese Quail Genetically Selected for Contrasting Adrenocortical Responsiveness 1
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1 Developmental Instability in Japanese Quail Genetically Selected for Contrasting Adrenocortical Responsiveness 1 D. G. Satterlee,*,2 G. G. Cadd,* and R. B. Jones *Applied Animal Biotechnology Laboratories, Department of Poultry Science, Louisiana Agricultural Experiment Station, Louisiana State University Agricultural Center, Louisiana State University, Baton Rouge, Louisana 70803; and Welfare Biology Group, Roslin Institute (Edinburgh), Roslin, Midlothian EH25 9PS, Scotland ABSTRACT Differences in developmental instability of the HS and LS lines. These findings suggest that developmental were assessed with Japanese quail of two lines that had been genetically selected over several generations for reduced (low stress, LS) or exaggerated (high stress, HS) plasma corticosterone response to brief mechanical restraint. At 32 wk of age, three bilateral traits were selected for study in each quail line. The characteristics chosen were length of the metatarsus (shank length, SHL), diameter of the shank (SHD) perpendicular to the spur, and distance between the auditory canal and the nares (face length, FL). Significantly greater bilateral trait size variances were associated with the measurement of SHL (P < ) and FL (P < ) in the HS line than in the LS line. SHD variances did not differ (P = 0.22) in quail instability (i.e., fluctuating asymmetry, FA) is more pronounced in HS quail than in LS quail. Previous studies have shown that not only do quail of the HS line show greater adrenocortical responsiveness to a wide range of stressors but that they are also more easily frightened than LS birds. Therefore, the line differences in FA found here may reflect the birds differential responsiveness to chronic social and physical environmental stressors. The present findings also support previous suggestions that measuring asymmetries in bilateral traits could be an additional and valid method of assessing stress and of comparing phenotypic stability in selected populations. (Key words: quail, fluctuating asymmetry, corticosterone, stress) 2000 Poultry Science 79: INTRODUCTION Developmental instability is attracting growing interest because it is thought to reflect the inability of individual organisms to produce a stable phenotype under given environmental conditions (Parsons, 1990; Moller and Swaddle, 1997; Moller et al., 1999). Unlike genetic preprogramming that can lead to antisymmetry or directional asymmetry, developmental instability produces fluctuating asymmetry (FA) or small, random deviations from symmetry in otherwise bilaterally symmetrical characteristics (Parsons, 1990; Moller and Swaddle, 1997; Thomson, 1999). In other words, differences between the size of left and right bilateral characters are normally distributed with a mean of zero and a variance governed by the amount of developmental instability (Van Valen, 1962; Thomson, 1999). It has been proposed that FA is caused by genetic and environmental stress, and its occurrence has been noted in a variety of mammalian and avian species (Palmer and Strobeck, 1986; Jones, 1987; Parsons, 1990; Moller and Swaddle, 1997; Thomson, 1999). Inbreeding, the introduction of novel mutants into the genome, and hybridization are among the genetic factors that increase FA, whereas the environmental causes include parasitic infestation, pathologies, feed deprivation, forced exposure to novelty, loud sounds, and social stress (Parsons, 1990; Moller and Swaddle, 1997). More specifically, FA was more pronounced in chickens with tibial dyschondroplasia and in those reared under high stocking densities or under permanent light (Moller et al., 1995, 1999). Strong directional selection, such as that imposed by animal breeders, may also be particularly influential in increasing developmental instability. For example, asymmetry was greater in White Leghorn lines that had been selected for contrasting antibody response to sheep red blood cells (Siegel and Gross, 1980) than in their reciprocal crosses (Yang et al., 1997; Yang and Siegel, 1998). Received for publication October 29, Accepted for publication August 17, Approved for publication by the Director of the Louisiana Agricultural Experiment Station as manuscript Number To whom correspondence should be addressed: dsatterlee@agctr. lsu.edu. Abbreviation Key: FA = fluctuating asymmetry; FL = face length; G = generation; HS = high stress; LS = low stress; RA = relative asymmetry; SHL = shank length; SHD = shank diameter. 1710
2 DEVELOPMENTAL INSTABILITY AND ADRENOCORTICAL RESPONSIVENESS 1711 The potential value of using asymmetries of bilateral traits as tools in the study of evolution and animal breeding is becoming widely recognized (see Yang et al., 1997). This approach also has considerable strategic relevance for farm animals. For example, the magnitude of asymmetries might be used as a valid measure of stress, as a way of comparing developmental instability between populations, and as a means of identifying the optimal rearing conditions for domestic animals (Yang et al., 1997; Moller et al., 1995, 1999). Such information could have important implications for well-being and productivity, both of which can be seriously compromised if the animals are chronically distressed (Jones, 1996, 1997). Intuitively, genetic lines that have been selected over several generations for differences in their physiological and behavioral responsiveness to stressful stimulation would be particularly powerful tools for studying developmental instability. Therefore, in the present study the occurrence and magnitude of asymmetries were studied in divergent lines of Japanese quail that had been selected for low (LS, low stress) or high (HS, high stress) plasma corticosterone responses to brief mechanical restraint (Satterlee and Johnson, 1988). These genetic lines are particularly suitable for exploring the above issues for many reasons. First, the selection program has apparently exerted a nonspecific effect on stress susceptibility because LS quail showed lower adrenocortical responses to a wide variety of stressors, e.g., cold, crating, food and water deprivation, social tension, and manual restraint, than did HS birds (Satterlee and Johnson, 1988; Jones et al., 1994; Jones, 1996). Second, selection has also influenced underlying fearfulness (propensity to be easily frightened by diverse events). Fear responses were consistently less pronounced in LS than HS quail when they were exposed to human beings, exposed areas, unfamiliar objects and places, or mechanical restraint (Jones et al., 1992a,b, 1994, 1999; Satterlee and Jones, 1995; Jones and Satterlee, 1996). Third, not only is the Japanese quail an important agricultural species in many countries (Baumgartner, 1994), but it is also thought to be a useful model for other more commercially important species, such as the domestic fowl (Mills and Faure, 1992; Aggrey and Cheng, 1994). In the first of a series of projected studies, attempts were made to illuminate the potential role of environmental stress in determining developmental instability. More specifically, the hypothesis was tested that quail from genetic lines selected for reduced or exaggerated sensitivity to stressful stimulation would show decreased or elevated levels of FA, respectively. Three bilateral traits were measured in adult male quail from the LS and HS lines that had been housed in same-line breeding groups for 26 wk. It was reasoned that they would likely have been exposed to a variety of environmental stressors (e.g., human traffic, extraneous noises, 3 Petersime Incubator Co., Gettysburg, OH and interbird aggression) during this time. Fluctuating asymmetries were then compared between the two lines by calculating intra-individual variances in trait size (Thomson, 1999). MATERIALS AND METHODS Genetic Stocks and Husbandry Adult male offspring of Japanese quail (Coturnix japonica) were studied from two genetic lines that were selected over several generations for low (LS) or high (HS) plasma corticosterone response to brief mechanical immobilization (Satterlee and Johnson, 1988). After pedigree selection for 12 generations, average plasma corticosterone levels postimmobilization were 156 and 54% of the values measured in nonselected controls in the HS and LS lines, respectively (Satterlee and Johnson, 1988). Selection pressure was continued for two additional generations, after which the lines were maintained for six generations without selection. Nonselection was accomplished by colony breeding of family crosses within a line, avoiding only full-sib matings. Despite relaxation of the selection pressure during generation 15 (G 15 )to G 19, examination of the lines at G 20 showed that divergence had been maintained; means ± SEM of the circulating corticosterone concentrations in HS and LS quail exposed to the immobilization stressor were 19.4 ± 0.7 and 10.0 ± 0.5 ng/ml, respectively. Selection pressure was reimposed to produce G 21 wherein immobilization resulted in corticosterone concentrations of 29.0 ± 5.4 and 13.7 ± 4.1 ng/ml in the HS and LS quail, respectively (Jones and Satterlee, 1996). The lines reproduced for an additional three generations without selection before their use in the present study (G 24 ). The quail studied were taken from a larger population of an 800-bird hatch. Egg incubation and chick brooding, feeding, and lighting procedures were similar to those described elsewhere (Jones and Satterlee, 1996) with the exception that chicks were brooded from Day 1 in mixedsex, mixed-line groups of 50 within each of 16 compartments of two Model 2SD-12 Petersime brooder batteries 3 modified for quail. To maintain the line identity of each bird, leg bands (placed on chicks at hatching) were replaced with permanent wing bands at 14 d of age. At 6 wk of age, quail were sexed, and same-line groups of 10 females and 5 males were placed into 24 colony cages for breeding (i.e., 12 cages of LS quail and 12 cages of HS quail). Throughout a laying cycle of 26 wk, and when extra birds were available, breeders that had naturally succumbed, escaped, or were removed for mechanical reasons were replaced by same-line, same-sex, fullsibling quail from the original hatch. This practice insured that a high number of experimental units would be available in each line at the end of the experiment as the intent was to take measurements on aged quail (32 wk). We reasoned that if exposure to stressful stimulation is positively related to age, then environmentally
3 1712 SATTERLEE ET AL. TABLE 1. Bilateral trait means ± SEM for sides (left, L; right, R) and side differences (L minus R) at 32 wk of age by quail line 1 LS HS Trait L R L R L R L R Shank, mm Length ± ± ± ± ± ± 0.06 Diameter 2.71 ± ± ± ± ± ± 0.01 Face length, 2 mm ± ± ± ± ± ± LS = low stress; HS = high stress. 2 Distance between nares and auditory canal. induced line differences of developmental instability should be more pronounced in older quail. Breeders received a laying diet (21% CP and 2,750 kcal ME/kg) and water ad libitum. A 16 h light:8 h darkness photoperiod was provided with lights-on occurring at 0500 h. Daily maintenance and feeding chores were done at the same time each day (0800 h). Traits Measured At 32 wk of age, 53 LS and 60 HS quail were killed by cervical dislocation. Data were obtained for the following bilateral traits: length of the metatarsus (shank) (SHL), diameter of the shank (SHD) perpendicular to the spur, and distance between the auditory canal and the nares (face length, FL). The same person (blinded to the experimental protocol) made all quail measurements to the nearest 0.1 mm. Statistical Analyses Having calculated absolute FA as the unsigned leftright character sizes, many researchers (e.g., Yang et al., 1997; Moller et al., 1999) have then divided this value by character size to give a measure of relative asymmetry (RA) for each bilateral trait. Once summed, these measures were averaged to produce an overall RA score for each animal. However, the use of unsigned asymmetries is thought to be contentious (Swaddle et al., 1994; Gangestad and Thornhill, 1998; Thomson, 1999) because it violates the assumptions of normally distributed errors as well as that of homogeneous variance inherent in techniques like ANOVA, t-tests, and multiple linear regressions. Therefore, in line with Thomson (1999), these problems were avoided when comparing FA in the two lines by focusing on intra-individual variance for SHL, SHD, and FL. For each trait, the intra-individual, interlateral variance in trait size, V ind, was calculated from V ind = (L 2 + R 2 ) ([L + R] 2 /2). After calculating V ind for each individual (quail) within a given trait and line, trait variance data were fitted to a general linearized model with gamma errors and a log link function using PROC GENMOD (SAS Institute, 1985). The dependent variable in each model was quail line, and the independent variable was V ind of a given trait. Within a line, and using the criteria that approximately 68, 95, and 99.7% of the values in a normal population are within one, two, or three standard deviations of the population mean, respectively (SAS Institute, 1985), the signed asymmetries of each trait were found to be normally distributed within the population mean for the respective trait (plots not shown). These findings verified that each trait showed characteristics of FA and not those of directional asymmetry or antisymmetry. This justified the use of Thomson s (1999) procedures for the assessment of intra-individual variance in trait size and subsequent analysis for line differences in developmental instability. RESULTS Table 1 gives bilateral trait line means by side and mean trait differences (left side minus right side) by line. Table 2 shows the influence of quail line on intraindividual, interlateral variances in bilateral trait sizes (V LS vs. V HS ) and the likelihood-ratio test statistic (X 2 1) associated with each line comparison. Significantly greater bilateral trait size variances were associated with the measurement of SHL (P < ) and FL (P < ) in the HS line than in the LS line; however, quail of the HS line did not show a significant tendency toward greater (P = 0.22) SHD variance when compared with quail of the LS line. DISCUSSION Fluctuating asymmetry was significantly greater in HS than LS quail in two (SHL and FL) of the three bilateral TABLE 2. Influence of quail line (low stress, LS; high stress, HS) on intra-individual, interlateral variances in bilateral trait sizes (V LS vs. V HS ) 1 and the likelihood-ratio test statistic (X 2 1) associated with each line comparison Trait V LS V HS X 2 1 Probability > X Shank length Shank diameter Face length After measuring traits on each side of the body (L = left; R = right), the intraindividual, interlateral variance in trait size, V ind, was calculated from V ind = (L 2 + R 2 ) ([L + R] 2 /2) (see Thomson, 1999).
4 DEVELOPMENTAL INSTABILITY AND ADRENOCORTICAL RESPONSIVENESS 1713 traits measured in the present study. The interlateral variance for SHD was also numerically larger in HS than LS birds, but this difference was not significant. These findings suggest that developmental instability is more pronounced in quail from a genetic line selected for high plasma corticosterone responses rather than low responses to brief immobilization (Satterlee and Johnson, 1988). Not only do quail of the HS line show greater adrenocortical responsiveness to a wide range of stressors, but also they are also more easily frightened than LS birds (Satterlee and Johnson, 1988; Jones et al., 1992a, 1999; Satterlee and Jones, 1994, 1995; Jones and Satterlee, 1996). Given such contrasting levels of stress susceptibility and underlying fearfulness, we might tentatively suggest that the line differences in FA found here reflected the birds differential responsiveness to social and physical environmental stressors, such as those associated with mating behavior, interbird aggression, human traffic, cage cleaning, and extraneous noises. However, although both lines have been subjected to a similar amount of inbreeding, it cannot be guaranteed that the resultant effects of such genetic stress (Parsons, 1990; Moller and Swaddle, 1997) on FA would have been identical in the LS and HS birds. The inclusion of truly randombred, nonselected lines or reciprocal crosses in future comparisons will allow meaningful assessment of the role of genetic (directional selection) stress. Quail of the nonselected Louisiana State University line were not included in this study because they have been subjected to inbreeding (genetic stress) over 24 generations. The possible exploitation of individual variation in fearfulness and in susceptibility to stress has important implications for poultry breeding, welfare, and performance. For example, in addition to the reduced stressresponsiveness and fearfulness accompanying selection of the LS line, these quail also show lower stress-induced osteoporosis and greater body weight than HS quail (Satterlee and Roberts, 1990; Jones, 1996). Furthermore, the present findings suggest that such genetic selection would not compromise the ability of the quail to produce stable phenotypes. The present results also support previous suggestions that measuring asymmetries in bilateral traits could be an additional and valid method of assessing stress and the suitability of housing systems (Yang et al., 1997; Moller et al., 1999). Divergent lines, such as the HS and LS quail, represent valuable models for resolving some of these issues. ACKNOWLEDGMENTS The contribution of R. B. Jones was supported by the Roslin Institute and the Biotechnology and Biological Sciences Research Council. The authors are also grateful to R. Stocking and L. Parker of the Department of Poultry Science, Louisiana State University, Baton Rouge, LA 70803, for their technical assistance and to P. B. Siegel and A. Yang of the Department of Poultry Science, Virginia Tech, Blacksburgh, VA 24061, for their helpful comments. REFERENCES Aggrey, S., and K. M. Cheng, Animal model analysis of genetic (Co) variances for growth traits in Japanese quail. Poultry Sci. 73: Baumgartner, J., Japanese quail production, breeding and genetics. World s Poult. Sci. J. 50: Gangestad, S. W., and R. Thornhill, The analysis of fluctuating asymmetry redux: The robustness of parametric statistics. Anim. Behav. 55: Jones, J. S., An asymmetrical view of fitness. Nature 325: Jones, R. B., Fear and adaptability in poultry: Insights, implications and imperatives. World s Poult. Sci. J. 52: Jones, R. B., Fear and distress. Pages in: Animal Welfare. M. C. Appleby and B. O. Hughes, ed. CAB International, Wallingford, UK. Jones, R. B., and D. G. Satterlee, Threat-induced behavioural inhibition in Japanese quail genetically selected for contrasting adrenocortical response to mechanical restraint. Br. Poult. Sci. 37: Jones, R. B., D. G. Satterlee, and G. G. Cadd, Timidity in Japanese quail: Effects of vitamin C and divergent selection for adrenocortical response. Physiol. Behav. 67: Jones, R. B., D. G. Satterlee, and F. H. Ryder, 1992a. Fear and distress in Japanese quail chicks of two lines genetically selected for low or high adrenocortical response to immobilization stress. Horm. Behav. 26: Jones, R. B., D. G. Satterlee, and F. H. Ryder, 1992b. Openfield behavior of Japanese quail genetically selected for low or high plasma corticosterone response to immobilization stress. Poultry Sci. 71: Jones, R. B., D. G. Satterlee, and F. H. 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SAS Institute Inc., Cary, NC. Satterlee, D. G., and W. A. Johnson, Selection of Japanese quail for contrasting blood corticosterone response to immobilization. Poultry Sci. 67: Satterlee, D. G., and R. B. Jones, Fear and adrenocortical responses to human contact in Japanese quail selected for low or high plasma corticosterone response to immobilization stress. Poult. Sci. 73(Suppl. 1):160. (Abstr.). Satterlee, D. G., and R. B. Jones, Timidity in Japanese quail divergently selected for low or high adrenocortical response to immobilization stress. Poultry Sci. 66(Suppl. 1):116. (Abstr.).
5 1714 SATTERLEE ET AL. Satterlee, D. G., and E. D. Roberts, The influence of stress treatment on femur cortical bone porosity and medullary bone status in Japanese quail selected for high and low blood corticosterone response to stress. Comp. Biochem. Physiol. 95A: Siegel, P. B., and W. B. Gross, Production and persistence of antibodies in chickens to sheep erythrocytes. 1. Directional selection. Poultry Sci. 59:1 5. Swaddle, J. P., M. S. Witter, and I. C. Cuthill, The analysis of fluctuating asymmetry. Anim. Behav. 48: Thomson, D. L., Intraindividual variance in trait size and the analysis of developmental instability. Anim. Behav. 57: Van Valen, L., A study of fluctuating asymmetry. Evolution 16: Yang, A., E. A. Dunnington, and P. B. Siegel, Developmental stability in stocks of White Leghorn chickens. Poultry Sci. 76: Yang, A., and P. B. Siegel, Asymmetries and heterosis of bilateral traits in parental lines of chickens and their F 1 crosses. J. Anim. Breed. Genet. 115:
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