Genetic and phenotypic correlation between fluctuating asymmetry and two measurements of fear and stress in chickens

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Abstract

The purpose of the present study was to estimate the genetic and phenotypic correlation between fluctuating asymmetry and two measurements of fear and stress in chickens which had not deliberately stressed in any way, using the restricted maximum likelihood procedure. A total of 1073 36-week-old birds from two generations with complete pedigree of the Quail Castellana breed was used. Fluctuating asymmetry of several traits (leg, wing, and feather lengths, and ear-lobe and wattle areas), tonic immobility duration (indicator of fear), and heterophil to lymphocyte ratio (indicator of stress) were measured. The estimated genetic relationship between relative fluctuating asymmetry for the different traits and tonic immobility tended to be positive, that between the combined relative asymmetry of all traits and tonic immobility being near to +1; no significant phenotypic relationship was found between relative fluctuating asymmetry and tonic immobility. The genetic relationship between relative fluctuating asymmetry and heterophil to lymphocyte ratio was not consistent across the traits, ranging from +1 to −1, although the genetic correlation between the combined relative asymmetry and the heterophil to lymphocyte ratio was near to +1 too; no significant phenotypic relationship was found between relative fluctuating asymmetry and heterophil to lymphocyte ratio either. Relative fluctuating asymmetry and body weight were genetically negatively correlated for leg length and ear-lobe area but positively for feather length; the genetic correlation between the combined relative asymmetry and the body weight being near to −1; phenotypic relationships were not significantly different from zero. A significant negative genetic correlation between tonic immobility and heterophil to lymphocyte ratio was found, although the phenotypic association between these two measurements was zero. Phenotypic correlations always near to zero suggest that fluctuating asymmetry was not associated with duration of tonic immobility and heterophil to lymphocyte ratio in birds that have not been deliberately stressed.

Introduction

Fluctuating asymmetry (FA) is the most recommended index of developmental instability (Palmer and Strobeck, 1992). It is considered to be a valid indicator of genetic and environmental stress during development (Clarke et al., 1986, Leary and Allendorf, 1989, Parsons, 1990, Parsons, 1992), especially if the analysis is based on the composite FA of multiple traits (Leung et al., 2000). Fluctuating asymmetry is characterised by a normal distribution of left minus right side differences with a mean of zero (van Valen, 1962, Palmer and Strobeck, 1986, Palmer and Strobeck, 1992, Palmer, 1994, Polak and Trivers, 1994, Swaddle et al., 1994). In contrast to FA, directional asymmetry (DA) and antisymmetry (AS) have not been generally associated with stress, and are characterised by normal distribution with a mean of not zero, and non-normal distribution with a mean of zero, respectively. Any two or all three types of asymmetry can occur together in the same trait, particularly the DA–FA combination (van Valen, 1962).

Fluctuating asymmetry is used as a measurement of welfare and fitness at the individual level following development (Jones, 1987, Clarke, 1995, Moller, 1999a, Tuyttens, 2003). In his review of available information from the literature on the relationship between fluctuating asymmetry and various fitness components, Moller (1997) suggested that symmetrical individuals do generally have faster growth, higher fecundity, and better survival. This review included only one study of the relationship between fluctuating asymmetry and growth rate in chickens (Moller et al., 1995), the correlation coefficient being −0.07. Clarke (1998) criticised Moller's review indicating that a significant proportion of the data supposed to be supporting a positive relationship between developmental stability and fitness components failed to do so. Based again on a literature survey, Moller (1999b) concluded that correlation coefficients between fluctuating asymmetry and growth, fecundity, and survival are negative and highly significant (−0.15, −0.35, and −0.25, respectively; see also Moller and Manning, 2003).

The relationship between FA and indicators of fear and stress has been less studied. Moller et al., 1995, Moller et al., 1999 reported that fluctuating asymmetry was positively correlated with the duration of tonic immobility (TI) in chickens that were experiencing population density or lighting stress. Mignon-Grasteau et al. (2003) did not find significant relationship between asymmetry of tibia length and duration of tonic immobility in Japanese quail that were non-stressed. Yalcin et al. (2003) reported that fluctuating asymmetry was not closely correlated with duration of tonic immobility and heterophil to lymphocyte ratio in broilers that were both non-stressed and experiencing food or heat stress. Campo et al., 2000, Campo et al., 2002 found a significant relationship between asymmetry and tonic immobility only in one sex and one breed of chickens that were non-stressed, and no significant relationship between asymmetry and heterophil to lymphocyte ratio (H:L).

The purpose of the present study was to estimate the genetic and phenotypic correlation between fluctuating asymmetry and two indices of fear and stress (tonic immobility duration and heterophil to lymphocyte ratio, respectively; Gallup, 1979, Gross and Siegel, 1983) in chickens, using the restricted maximum likelihood (REML) procedure (Patterson and Thompson, 1971) under a multivariate mixed model. With respect to the existing literature the current study analyses for the first time the genetic correlation between FA and these two measurements of fear and stress, and complements the scarce previous experiments to analyse the phenotypic correlation between FA and tonic immobility (three experiments with broiler chickens, and one experiment with quails), and between FA and heterophil to lymphocyte ratio (one experiment with broilers). The relationship between FA and body weight (a fitness component) is included in the study.

Section snippets

Materials and methods

Birds were housed at 20 weeks of age in pens with a raised slatted floor covering a dropping pit and straw litter on the rest of the floor; the slatted area occupied one third of the floor. Bird density was 4 birds/m2. Birds were fed standard diet, containing 16% CP, 2700 kcal ME/kg, 3.5% Ca, and 0.5% available P. Feed and water were supplied for ad libitum consumption. The lighting regime was 14 h light:10 h darkness (light from 7.00 to 21.00) and room temperature was 16–20 °C. Feeders, drinkers,

Results

A significant positive genetic relationship was found between relative asymmetry for ear-lobe and wattle areas, and tonic immobility duration (Table 1), whereas phenotypic relationships were near zero for all five traits. Although a significant positive genetic relationship was found between relative asymmetry for ear-lobe area and heterophil to lymphocyte ratio, those for feather length and wattle area were significant but negative. The same was true for heterophil number, whereas the opposite

Discussion

The current study fulfilled the criteria to estimate the genetic correlations between FA and other traits confidently (Palmer, 1994) without the effect of confounding factors. The type of asymmetry was determined, an assessment was made of measurement error, the relationship between the amount of asymmetry and trait size was controlled, the genetic correlation was estimated using the REML procedure under a general multivariate mixed model, and finally, a large sample size was used. The genetic

References (48)

  • A.P. Moller et al.

    Developmental instability and light regime in chickens (Gallus gallus)

    Appl. Anim. Behav. Sci.

    (1999)
  • K.E. Nestor et al.

    Effects of selection for increased body weight, egg production, and shank width on developmental stability in turkeys

    Poult. Sci.

    (2000)
  • K.E. Nestor et al.

    Effect of selection for increased body weight and increased plasma yolk precursor on developmental stability in Japanese quail

    Poult. Sci.

    (2002)
  • M. Polak et al.

    The science of symmetry in biology

    Trends Ecol. Evol.

    (1994)
  • J.P. Swaddle et al.

    The analysis of fluctuating asymmetry

    Anim. Behav.

    (1994)
  • S. Yalcin et al.

    Criteria for evaluating husbandry practices to alleviate heat stress in broilers

    J. Appl. Poult. Res.

    (2003)
  • G. Beuving et al.

    Adrenocortical and heterophil/lymphocyte responses to challenge in hens showing short or long tonic immobility reactions

    Br. Poult. Sci.

    (1989)
  • J.L. Campo et al.

    Genetic basis of the Melanotic Prat phenotype

    Br. Poult. Sci.

    (1986)
  • J.L. Campo et al.

    Negative association between heterophil to lymphocyte ratio and tonic immobility reaction in hens

  • J.L. Campo et al.

    Fluctuating asymmetry in male secondary sexual traits: association with indicators of stress in chickens

    Arch. Geflügelk.

    (2002)
  • G.M. Clarke

    Relationships between developmental stability and fitness. Application for conservation biology

    Conserv. Biol.

    (1995)
  • G.M. Clarke

    Developmental stability and fitness: the evidence is not quite so clear

    Am. Nat.

    (1998)
  • G.M. Clarke et al.

    Fluctuating asymmetry: a technique for measuring developmental stress caused by inbreeding

    Aust. J. Biol. Sci.

    (1986)
  • H.U. Graser et al.

    A derivative-free approach for estimating variance components in animal models by restricted maximum likelihood

    J. Anim. Sci.

    (1987)
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