Beyond the Chicken: Alternative Avian Models for Developmental Physiological Research

Abstract

Biomedical research focusing on physiological, morphological, behavioral, and other aspects of development has long depended upon the chicken (Gallus gallus domesticus) as a key animal model that is presumed to be typical of birds and generally applicable to mammals. Yet, the modern chicken in its many forms is the result of artificial selection more intense than almost any other domesticated animal. A consequence of great variation in genotype and phenotype is that some breeds have inherent aberrant physiological and morphological traits that may show up relatively early in development (e.g., hypertension, hyperglycemia, and limb defects in the broiler chickens). While such traits can be useful as models of specific diseases, this high degree of specialization can color general experimental results and affect their translational value. Against this background, in this review we first consider the characteristics that make an animal model attractive for developmental research (e.g., accessibility, ease of rearing, size, fecundity, development rates, genetic variation, etc.). We then explore opportunities presented by the embryo to adult continuum of alternative bird models, including quail, ratites, songbirds, birds of prey, and corvids. We conclude by indicating that expanding developmental studies beyond the chicken model to include additional avian groups will both validate the chicken model as well as potentially identify even more suitable avian models for answering questions applicable to both basic biology and the human condition.

Keywords: animal model; bird; chicken; development; domestication; embryo.

Figure 1

Total number of PubMed citations of common animal and plant models derived from the Latin genus and species. Data acquired May, 2021. The two common rodent models (red) are highly dominant in biomedical research. However, while the zebrafish D. rerio and the nematode C. elegans are receiving much attention, both have less than a third of the PubMed citations as the domestic chicken (black). Also shown for comparison are three commonly used plant models (green).

Figure 2

Obesity-associated cardiac disorders in adult broiler chickens. Broiler chickens 49 weeks or older fed ad libitum for 70 days developed significantly more cardiac lesions than calorie restricted birds. (A) Diet-induced alterations in cardiac gross morphology in the form of ascites (fluid accumulation), pericardial effusion, myocardial rupture, and cardiac dilation (B) Internal compensatory responses lead to myocardial dilation or hypertrophy as evident in hens experiencing sudden death. Not shown is the many-fold increase in collagen content in the cardiac tissue in the ad libitum vs. restricted diet population evident in both surviving birds and those experiencing sudden death. Ad libitum birds additionally showed a significantly higher incidence of arrhythmia as well as chronic elevation of systolic blood pressure (from Chen et al., 2017).

Figure 3

A comparison of the onset of elements of cardiovascular control in the developing embryo of the domestic chicken and the emu. Development has been normalized to 100% of development, followed by a hatching period. Note that major developmental landmarks in the emu occur later (e.g., hypoxic bradycardia) or earlier (e.g., onset of tonic vagal tone) than in the domestic chicken. This raises the question “Which species is ‘representative'?" (modified from Crossley et al., ; Dzialowski and Greyner, 2008).

Figure 4

Relationship between body mass and egg incubation length in altricial and precocial birds. Body masses are the average for the species. Second order linear regressions are shown separately for precocial birds (black lines) and altricial birds (red lines).

Figure 5

Manipulation of plasma thyroid hormone (T₃) levels in the Pekin duck (Anas platyrhynchos domestica). T₃ levels were changed by either injection of T3 or by suppression of its synthesis by injection of the thyroid-peroxidase inhibitor MMI. Total plasma [T₃] rises from almost undetectable at embryonic day 25 (d25) to ~2 ng^.μl⁻¹ at external pipping (EP) and 1 day posthatch (1 dph). Injection of T₃, however, elevates total plasma [T₃] at D25 and EP. MMI strongly suppresses [T₃] at all examined stages (from Holmes and Ottinger, 2003). *Statistically significant difference.

Figure 6

Sonograms reflecting song learning and the influence of critical windows (sensitive periods) in the zebra finch, Taeniopygia guttata. By exposing developing birds (the tutee, or “student”) to adult song tutors during different periods of the tutee development, the critical window for song acquisition can be identified. In (A), there was an 86% resemblance to Tutor #1, but only a 57% resemblance to Tutor #2. In (B), using a different pair of tutors and different tutee, there was a 64% resemblance to Tutor #1, but an 84% resemblance to Tutor #2. Collectively these and other data from such studies suggest that auditory memory forms primarily from 25 to 35 days, but that the critical window duration varies upon the interplay of songs from different tutors, particularly in the latter part of the critical window. For most immature zebrafish, the critical window “closes” after 65 days post-hatch (DPH) (modified from Gobes et al., 2019).

Figure 7

Thyroid gland concentrations of T4 from hatchling American kestrels exposed to a range of concentrations of short chain chlorinated paraffins. These compounds, an example of which is shown at the top of the graph, act as endocrine disruptors affecting thyroid function. The widely used short chain chlorinated paraffins and their high environmental prevalence constitute a threat for fauna and humans alike that could be monitored through raptors (modified from Fernie et al., 2020). *Statistically significant different group 1. **Statistically significant different group 2.

Figure 8

Traditional and proposed use of developmental data acquired using the chicken model. (A) In many studies, data acquired from chickens are used to inform both basic biological research as well as biomedical research. These data are assumed to be representative of all birds and are often accepted without question. (B) An alternative approach that incorporates data from both chickens and additional avian species will enable comparative analyses to determine the appropriateness of the animal model employed. Such analyses can either verify the chicken as an animal model or identify limitations of data derived from the chicken that could be overcome by expanding research to include alternative avian models.