Functional implications of outlier loci in Bermuda’s feral chickens
Exploring gene function and annotation within sweep loci from feral gene pools offer clues as to which traits are selected in ferals. Unfortunately, the large number of unannotated genes found in the Bermudian sweeps limits our ability to test for enrichments of particular gene functions. Recognizing this limitation, it is still of interest to examine gene functions in those genes that are annotated. In the case of the nine genes within Bermuda sweeps that were annotated, several had previously been identified as affecting anxiety-related behaviours (see below). Additional roles for annotated genes included bone remodelling, eye development or vision, and the immune system, suggesting possible connections to life-histories, sensory ecology, and/or pathogen resistance. In the case of the Hawaiian sweeps, function was highly variable.
Concerning behavioural genetics, five of the nine genes from Bermuda sweeps were strongly associated with anxiety, schizophrenia, depression, and their related behaviours (ADCY1 (Chen, Xu et al. 2023) (Sundararajan, Manzardo et al. 2018, Chen, Ding et al. 2022), DRD3 (Staal 2015) (Liu, Xu et al. 2022, Sofronov, Dobrovolskaya et al. 2022), PTRB (Ishiguro, Gong et al. 2008), TAFA5 (Huang, Zheng et al. 2021) (Li, Li et al. 2020), tSNARE1 (Sleiman, Wang et al. 2013, Gu, Jiang et al. 2015, Fromer, Roussos et al. 2016, Whelan, St Clair et al. 2018, Li, Whelan et al. 2019, Schrode, Ho et al. 2019, Li, Shen et al. 2020, Plooster, Rossi et al. 2021)). Although the studies linking these genes to behaviour come mostly from human literature, we have previously demonstrated a strong cross-species replication for anxiety-related genes in chickens, humans and mice (Johnsson, Williams et al. 2016). Thus, the relationship between anxiety-related traits and adaptive (e.g. anti-predator) behaviour may explain the presence of such behavioural genes in the Bermudian population. In particular, Red Junglefowl display much more anxiety-related/ anti-predator behaviour than their domesticated counterparts (Johnsson, Williams et al. 2016), and hence the feral chickens appear to be reverting to ancestral behaviour in wild habitats where feral cats, humans, and other wild animals present credible mortality risks. It is also possible that these genes are influenced by other sources of behavioural selection in wild settings (such as high-stakes social interactions, and the demands of successful foraging in complex and changing environments).
The remaining known annotated genes affected bone remodelling via osteoblast differentiation (MYST/Esa1)(Hu, Yin et al. 2021), the immune system via the regulation of inflammation (Zc3h12a/ MCPIP1) (Matsushita, Takeuchi et al. 2009, Lin, Chien et al. 2013, Miao, Huang et al. 2013), and cancer metastasis and development (Nasri Nasrabadi, Nayeri et al. 2020). Once again, these raise exciting questions about how pathogens and life history selection might influence feral gene pools that merit targeted future study – particularly since feral G. gallus are known to host zoonotic diseases (Dubey 2010).
Altogether, annotated genes in sweeps conform with our predictions as to how feral birds should adapt to the natural environment, with the return of natural and sexual selection pressures driving adaptive responses within sufficiently diverse gene pools such as those of Kauai and Bermuda chickens. The fact that anxiety-related genes are present in selected regions of the feral gene pools’ genomes provides a tantalizing suggestion of selection on behavior that requires further study. We have found previously that domesticated birds are less anxious than their wild counterparts the Red Junglefowl (Johnsson, Williams et al. 2016, Johnsson, Henriksen et al. 2018, Fogelholm, Inkabi et al. 2019). The observation that the feral sweeps involve anxiety-related genes, and also harbor alleles of domesticated origin, indicates that such polymorphisms are still potentially circulating in domesticated populations but are not fixed or maintained at a low frequency.