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.