Introduction

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Chickens are thought to have been domesticated from the red jungle fowl (Gallus gallus) and specifically two subspecies, G. g. gallus and G. g. spadiceus. 1 Not only are there genomic differences with domestication 2,3 but also evidence of unidirectional introgression from the green jungle fowl (G. sonnerati). 4 The processes of domestication and the subsequent changes in an animal’s biology are attracting increasing attention based principally on the genomic studies. 2,3,5,6 The present communication examines the shifts in hematological parameters during domestication and recent intensive selection of poultry. This is based on a meta-analysis of published studies of the hematological parameters comparing chickens with the ancestral red jungle fowl and with other wild birds. In addition, indigenous chickens were employed as a proxy to allow comparison of effects of domestication versus intensive selection. It is hypothesized that there would be shifts in hematological parameters between modern domesticated chickens compared to unselected chickens, to jungle fowl and to other wild birds.

A database of multiple hematological parameters in wild birds was previously developed. 7 It is recognized that the terms hematocrit (hct) and packed cell volume (pcv) are distinct but the term are frequently used interchangeably.‡ For the vast majority of studies in the database, pcv was determined by centrifugation but called hct in the publications contributing to the database. In the present communication, pcv and hct are pooled and referred to as hct/pcv. On causal inspection of the database, there appeared to be lower hct/pcv in wild birds of the order Galliformes and even lower pcv in chickens. One hematological parameter was also determined in the course of studies of the effects of fasting on metabolism and hormonal responses in young fed and fasted modern meat type chickens. 8,9 These modern meat type chickens had a hct that was estimated as <22% 12 as determined using an ABL 77 blood gas analyzer (Radiometer America, Inc., Westlake, OH 44145). The hematocrit values are similar to those reported in broiler chickens (22%). 1014

The database was queried systematically to determine whether hematological parameters are different in domesticated chickens compared to either descendants of the ancestral species (jungle fowl) or to the taxonomic order (Galliformes) which the domesticated chicken belongs. This analysisis not only relevant to the understanding of domestication and subsequent selection programs, but in addition to the physiology of the animal. Marked changes in hct/pcv would be predicted to impact gaseous exchange.

‡ahdc.vet.cornell.edu/sects/clinpath/modules/hemogram/hct.htm

Materials and Methods

ls and MethodsDatabase:

There is a large but diffuse body of literature containing data on hematological parameters of domesticated and wild birds, the latter most commonly determined in blood samples obtained at capture. A database of multiple hematological parameters in birds is available as a supplementary series of tables.

Statistical analysis:

Multiple comparisons were made using one way ANOVA with means separated from Tukey’s range test.

Results

Table. 01 summarizes hematological parameters (hct/pcv, hemoglobin concentration and erythrocyte number) in a series of studies in commercial chickens while Table. 02 summarizes these parameters in studies of indigenous and random-bred chickens together with jungle fowl. Differential leukocyte percentages in studies of indigenous/native chickens are summarized in Table. 03. The data in Tables 01-03 were employed in the meta-analysis with this presented in Tables. 04 and 05.

Table. 04 summarizes a series of comparisons of hematological parameters between I. chickens (indigenous and non-selected chickens) and the ancestral species, the jungle fowl (Gallus gallus); II. Commercial chickens and indigenous and other non-selected chickens; III. jungle fowl and other Gallinaceous birds; IV. Wild birds within the order Galliformes and throughout the Class Aves Subclass Neognathae (for detailed data see supplementary table B). The hct/pcv was 16.9% lower (p<0.01) in indigenous and other non-selected chickens than in jungle fowl (Table. 02, Figure. 01). Moreover, hct/pcv was further reduced (p<0.01) in commercial chickens compared to either indigenous/non-selected chickens or jungle fowl, respectively, by 11.3% and 26.4% (Table. 02, Figure. 01). The hct/pcv of jungle fowl was essentially identical to other gallinaceous species of birds (Table. 01). Moreover, hct/pcv in gallinaceous species are 10.7% lower (p<0.001) than wild birds overall (Table. 02, Figure. 01).

Table. 01

Hematocrit (hct)/pcv together concentrations of erythrocytes and hemoglobin in commercial chickens.

Hct/pcv(%) Hemoglobing dL-1 Erythrocytes[# x 106μl-1] Reference or calculated from
Chickens (broiler) (6 weeks) [Cobb] 22.3 7.75 [10]
Chickens (broiler) 2-8 weeks [Ross 708] 22.65 7.25 [11-14]
Chickens (broiler) 5 weeks [Cobb] 30.7 9.4 1.7 [15]
Chickens (broiler) (2-7 weeks)[Hendrix sire line] 33.8 [16]
Chickens∆(broiler) [mixed] 31.0 9.56 2.36 [17]
Chickens (broiler)[Ross 308] 35.5 12.71 2.5 [18]
Selected for high/low growth 31.1 [19]
Chicken (Leghorn) male (4-8 weeks) 32.45 11.58 4.05 [20]
Chicken adult female (laying hen) 27.2 11.75 2.3 [21]
Mean + (n=) SEM 29.6+(9) 1.5 10.0+(9)08 2.6 +(5) 0.4

Δmeta-analysis of 98 studies comprising 37,000 birds

Circulating concentrations of hemoglobin were 13.3 % lower (p<0.05) in jungle fowl than birds in the order Galliformes (excluding chickens) (Table 2). Moreover, there was a greater reduction in circulating concentrations of hemoglobin, respectively, by 21.0% in non-selected and 30.1% in commercial chickens compared with birds in the order Galliformes (excluding chickens) and by 25.2 % in non-selected and 33.8 % in commercial chickens compared with wild birds (Class Aves Infra-class Neognathae) (Table. 04). There were no consistent differences with erythrocyte numbers. There was little difference between hematological parameters in commercial and wild turkeys (Table. 04).

There were few differences in either total leukocyte numbers (Table. 04) or differential leukocyte counts (Table. 05) in domesticated birds and wild birds. Circulating concentrations of leukocytes were higher (p<0.01) in adult commercial than either indigenous/non-selected chickens or compared with wild gallinaceous birds (Table. 04). There was no differences in the differential leukocyte count (Table. 05) or heterophil:lymphocyte ratio (data not shown) between jungle fowl, indigenous/non-selected chickens, commercial chickens or wild gallinaceous birds.

Table. 02

Hematocrit together concentrations of erythrocytes and hemoglobin indigenous/native chickens, random-bred chickens and jungle fowl.

Hematocrit[%] Hemoglobin[g dL1] Erythrocytes[# x 106 μl-1] Reference
Indigenous/native chickens
Assil (breed originating from Indian sub-continent) mean 4 weeks and adult 29.5 8.93 2.3 [22]
Bangladesh indigenous chickens – region 1 32.1 8.88 2.92 [23]
Bangladesh indigenous chickens region 2 34.6 3.0 [22]
Botswana indigenous chickens 34.0 2.15 [24]
Fayoumi (breed originating from Egypt) mean 4 weeks and adult 27.85 7.70 2.95 [22]
Iran indigenous chickens 40.8 [25]
Iran (Shiraz) indigenous chickens 31.0 9.6 2.7 [26]
Kashmir indigenous chickens 35.05 12.6 2.98 [27]
Nigerian indigenous chickens (aged 60-150 days 23.8 2.5 [28]
Nigerian indigenous chickens 35.6 12.0 3.92 [29]
Saudi Arabia indigenous chickens 32.05 9.8 2.86 [30]
Sudan indigenous chickens 43.4 17.8 2.42 [31]
Thailand native chickens 32.2 8.89 2.26 [32]
Tibetan chickens (young) 30.3 1.8 [33]
Mean – Indigenous/native and non-selected chickens 33.0+(14) 1.32 10.7+(9)1.03 2.67+(13) 0.15
Random-bred lines
Athens Canadian random-bred 5-9 weeks old 31.3 [34,35]
Cornell random-bred 5-9 weeks old 33.3 [34,35]
Mean Random-bred lines 32.3
Jungle fowl (Gallus gallus)
Jungle fowl (Gallusgallus bankiva) 36.1 12.2 2.63 [38]
Red jungle fowl (Gallusgallus gallus) 41.3 11.4 2.7 [39]
Malaysian jungle fowl (Gallus gallusspadiceus) 43.3 13.6 4.4 [40]
Mean – Jungle fowl(Gallus gallus) 40.2+(3) 2.14 12.4+(3) 0.64 3.24+(3) 0.58

Note. Unless otherwise stated – adults

Table. 03

Differential leukocyte percentages in indigenous/native chickens.

Heterophil% Lymphocyte % Monocyte% Eosinophil% Basophil% Reference
Assil 22.6 69.7 2.8 4.7 0.6 [22]
Bangladesh – region 1 21.1 66.35 2.2 2.475 0.92 [23]
Bangladesh – Region 2 20.0 71.0 4.5 3.5 1.0 [22]
Botwana 17 75 4.3 4 0 [24]
Fayoumi 30.5 61.7 6.25 1.25 0.25 [22]
Indian – NicobariIslands 20.05 55.75 10.6 1.3 4.22 [43]
Indian -Vanaraja 27.85 48.6 10.1 1.35 3.95 [43]
Iran 33.45 58.65 3.65 3.05 1.25 [26]
Kashmir 29.4 49.4 10.87 7.18 2.62 [28]
Saudi Arabia 44 45.9 4.3 4 1.7 [31]
Thailand 23.7 63.7 4.2 5.83 2.65 [33]
26.3 + (11) 2.38 60.5 + (11) 2.9 5.8 + (11) 0.97 3.5 + (11) 0.58 1.7 + (11) 0.43

Discussion

The present analyses provide strong evidence that hct/pcv is markedly reduced in domestic chickens. There was a similar hct/pcv across wild birds (Figure. 01). In contrast, the hct/pcv was lower in wild birds of the order Galliformes including the red jungle fowl (Gallus gallus) (Table. 03, Figure. 01) from which chickens were domesticated. 1 Hct/pcv was further reduced in non-selected indigenous chickens (Tables. 02 and 04, Figure. 01). There were very similar hct/pcv in adult indigenous non-selected chickens (Table. 02) to early reports on young chickens from non-selected lines (Athens Canadian random-bred and Cornell random-bred with pcvs of 31.3 and 33.3% respectively) 34,35 and with studies with commercial lines prior to 1986 [mean male and female adults 34.7± (7 studies) 1.5%. 36,37 The hct/pcv was lower in more recent reports of chickens from commercial breeds (Tables. 01 and 04, Figure. 01).

The basis for the shifts in hct/pcv are not known. Hct/pcv is tightly controlled physiologically. This is supported by the following. Hypoxia elevates hct/pcv in chickens. 41 Moreover, chronic infusion of adrenocorticotropic hormone (ACTH) is followed by increases in the hct/pcv and blood concentrations of hemoglobin in broiler chickens. 11 In addition, there are genetic and developmental effects. In chickens selected for low growth, there is reduced hct/pcv. 19 There are also changes in erythrocytes during development and growth (embryonic development; 42 post-hatch growth. 14

Table. 04

Comparison of hematological parameters in adult commercial or indigenous and non-selected chickens with jungle fowl, other gallinaceous birds and wild birds[mean + (nα=) SEM].

Pcv/hematocrit[%] Hemoglobin[g dL-1] Erythrocytes[# x 106 μl-1] Leukocytes[# x 103 μl1]
Comparison of Indigenous and non-selected chickens and jungle fowl
Indigenous and non-selected chickens 33.4 + (12) 1.6x 11.3 + (11) 0.9 2.7 + (11) 0.15 19.4 + (9) 1.8
Jungle fowl 40.2+(3) 2.1y 12.4+(3) 0.6 3.2 +(3) 0.58 9.1β
Comparison of Indigenous and non-selected chickens with commercial chickens
Commercialchickensγ 29.6 + (10) 1.5x 10.0 + (9) 0.8 2.6 + (5) 0.39 28.0 + (6) 1.4y
Indigenous and non-selected chickens 33.4 + (12) 1.6y 11.3 + (11) 0.9 2.7 + (11) 0.1 19.4 + (9) 1.8x
Comparison of jungle fowl with other Gallinaceous birds
Jungle fowl 40.2+(3) 2.1 12.4+(3) 0.6x 3.2 +(3) 0.58 9.1
Birds in the orderGalliformes(excluding chickens) 39.9 + (18) 1.3 14.3 + (16) 0.7y 2.8 + (16) 0.18 13.4 + (9) 2.6
Comparison of Gallinaceous birds with wild birds
Birds in the orderGalliformes(excluding chickens) 39.9 + (18) 1.3x 14.3 + (16) 0.7 2.8 + (16) 0.18 13.4 + (9) 2.6
Wild birds (ClassAves Infra-classNeognathae)δ 44.7 + (318) 0.3y 15.1 + (227) 0.2 2.9 + (250) 0.05 13.7 + (200) 0.7
Comparison of commercial and wild turkeys
Commercial turkeys (adult) 36.5 17.4 7.8ε
Wild turkeys (adult and juvenile) 38.6 13.8 28.4ζ
Birds in the orderGalliformes 39.9 + (18) 1.3 14.3 + (16) 0.7 13.4 + (9) 2.6

Note:

x, y = Different superscript letter indicate difference p<0.05

α = For commercial chickens n is numbers of studies (Table. 01), for indigenous and non-selected chickens n is number of lines/populations (Table. 02), for jungle fowl n is number of sub-species (Table. 02) and for wild birds in the order Galliformes and Class Aves n is number of species and data on each species are from supplementary tables in reference.7

β = 15

γ = Calculated from 5 studies in 16 and meta-analysis of 37,000 birds.17

δ = Excluding ratites-emus, ostriches, rheas and other birds of the Infra-class Paleognathae

ε = 22

ζ = Mean52,53

Comparison of pcv in domesticated versus wild species. Comparisons include chickens (columns 4 and 5)(green columns) with jungle fowl (Gallus gallus) (column 3)(light blue), with wild birds of the order Galliformes (column 2)(dark blue) and with other wild birds (Class Aves Infra-class Neognathae) (column 1)[red column]

Fig. 1: Figure. 01

Comparison of pcv in domesticated versus wild species. Comparisons include chickens (columns 4 and 5)(green columns) with jungle fowl (Gallus gallus) (column 3)(light blue), with wild birds of the order Galliformes (column 2)(dark blue) and with other wild birds (Class Aves Infra-class Neognathae) (column 1)[red column]

Note:

1. Wild birds (Class Aves Infra-class Neognathae)

2. Wild birds of the order Galliformes

3. Adult jungle fowl (Gallus gallus)

4. Adult indigenous/non-selected chickens

5. Adult commercial chickens

Horizontal bars indicate S.E.M. (Original data shown in Tables. 01 and 02);

abcd-Different superscript letter indicate difference p<0.05

There are also effects of environment and health status on hematological parameters. For instance, both hematocrit and blood hemoglobin concentrations are lower in young broiler chickens at elevated temperatures (27oC) compared to moderate environmental temperatures (16oC). 13 As would be expected, chickens on diets deficient in iron and copper have greatly reduced pcv. 34,35 Similarly, hct/pcv is depressed by protein deficiency 44 and following challenge with mycotoxins. 17 Ascites influences hct/pcv with hct/pcv being higher in broiler chickens with ascites. 16 Moreover, selection for hct/pcv is accompanied with higher incidence of ascites. It is suggested that a propensity for ascites provides a basis for the reduction in hct/pcv in birds of the order Galliformes and, particularly, in chickens. The present studies supports selection pressure for lowered hct/pcv in gallinaceous birds.

In view of the relationship between hematological parameters with diet and health status, it might be predicted that indigenous and other non-selected chickens are not receiving nutritionally complete diets. Commercial chickens would be expected to have replete diet. However, hct/pcv was lower in commercial chickens that indigenous chickens (Table. 04).

There are likely to be physiological implications of reduced hct/pcv in domesticated poultry. A decrease in circulating concentrations of oxygen would be expected.However, in a study where broiler chickens (43 day old) were assigned to two groups with low and high hct/pcv, there were, surprisingly, no differences in the circulating concentrations of oxygen, carbon dioxide, bicarbonate, sodium or potassium. 45

Along with the reduced hct/pcv there should be a concomitant increase in the percentage of plasma in blood (Tables. 01, 02 and 04, Figure. 01). It is further questioned whether an increase in plasma plays a role in the improved feed to gain efficiency of poultry. Circulating nutrients and hormones are usually expressed per unit volume of plasma while blood flow to a tissue is expressed as volume units of blood per minute per gram tissue (μL min-1 g-1). 4648 Thus, the effective blood concentration of nutrients would be higher in domesticated chickens. This was not a problem in the “classical” study of chicken metabolism using arterial versus venous blood concentrations of multiple metabolites and nutrients. 49 It is recommended that concentrations of metabolites and nutrients be expressed both per unit plasma and blood. It should be note that erythrocytes themselves may be a source of metabolites.

It is questioned whether the present analysis provides evidence for stress being a feature of the domesticated chicken. Hct/pcv was lower in domesticated chicken and, particularly, commercial chickens (Tables. 01, 02 and 04, Figure. 01). Given that activation of the pituitary-adrenal axis by ACTH results in increases in hct/pcv in broiler chickens, 11 the present analyses would militate against stress being a feature of domesticated poultry. There was no evidence of effects of domestication on differential counts (Table. 05). The lack of differences also would again suggest that stress is not a major feature in domesticated chickens. Stresses such as corticosterone administration or fasting influence the ratio of heterophils: lymphocytes in young chickens. 5051

Table. 05

Comparison of differential leukocyte counts (percentages) between jungle fowl(ancestral species for chickens), non-selected chickens, commercial chickens, domesticated and wild turkeys and other birds [mean + (n=) SEM]

Heterophils(%) Lymphocytes(%) Monocytes(%) Eosinophils(%) Basophils(%)
Comparison of Indigenous and non-selected chickens and jungle fowl
Indigenous and non-selected chickensα(n=11) 26.3 + 2.4 60.5 + 2.9 5.8 + 0.97 3.5 + 0.6 1.7 + 0.41.8
Jungle fowlβ (n=1) 21.6 74.6 2.0 3.5 1.7
Comparison of commercial chickens with indigenous/non-selected chickens
Adult commercial chicken (n=8) 25.0 + 2.3 65.8 + 2.6 5.1 + 1.0 2.1 + 0.3 2.2 + 0.2
Indigenous and non-selected chickensα(n=11) 26.3 + 2.4 60.5 + 2.9 5.8 + 0.97 3.5 + 0.6 1.7 + 0.4
Comparison of jungle fowl with other Gallinaceous birds
Jungle fowlβ(n=1) 21.6 74.6 2.0 3.5 1.7
Wild birds in the order Galliformes excluding poultry (n=12) 34.2 + 3.8 54.5 + 3.5 5.4 + 1.0 3.2 + 0.8 3.1 + 0.8
Comparison of commercial turkeys with wild turkeys and other Gallinaceous birds
Wild turkey (juvenile) (Meleagrisgallopavo)ε 41.3 50.1 5.1 0.6 2.9
Commercial turkey(adult)η 36.4 51.1 4.4 1.3 6.7
Wild birds in the order Galliformes excluding poultry (n=12) 34.2 + 3.8 54.5 + 3.5 5.4 + 1.0 3.2 + 0.8 3.1 + 0.8

α Calculated from data in Table. 03. β For comparison, the differential leukocyte counts for the Malaysian jungle fowl (Gallus gallus spadiceus) was reported as the follows: heterophils – 51.3%, lymphocytes – 31.1%, monocytes – 8.6%, eosinophils – 4.3% and basophils – 4.6% (20).38