Exploring the genetic and dietary mechanisms of urban/rural divergence in a potentially self-domesticating animal

Overview

Human activity is drastically altering the habitat use of natural populations and is known to drive of phenotypic divergence in a number of wild animal populations. We have recently shown that urban and rural populations of red foxes (Vulpes vulpes) from London and surrounding boroughs are divergent in skull traits (Parsons et al. 2020). This divergence was related to jaw size, muscle attachment sites, and braincase size, suggesting that changes are likely driven by differing biomechanical demands of feeding or cognition between habitats. Notably, these patterns of skull divergence between urban and rural habitats matched the description of morphological changes that can occur during domestication. Specifically, urban populations of foxes show variation consistent with ‘domestication syndrome (Wilkins et al. 2014).

Therefore, phenotypic divergence in relation to human activity could potentially inform us of the conditions and mechanisms that initiate a ‘self’ domestication process. This project will aim to address whether additional phenotypic traits match this pattern in urban foxes, as well as determining the genetic changes that potentially underlie them. Specifically, candidate genes for domestication have been identified from comparisons of dogs with wolves (Axelsson et al. 2013), as well as from red foxes derived from the well-known Belyaev domestication experiments in Russia (Kukekova et al. 2018). This knowledge will inform genome-level examinations of variation between populations of urban and rural red foxes. A number of these genes relate to neurological function, as well as dietary variation, as found in other urban-dwelling animals (Pollock et al. 2017, Salmon et al. 2020). This would enable the student to develop projects aimed at related phenotypes including behaviours, further skull or other anatomical features, and the possibility to investigate dietary differences through a metagenomic approach. A key prediction is that as fox individuals more closely match domestication in one trait, they should in turn match domestication in other traits.

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Image Captions

An urban fox (photo credit Sean Page).

Methodology

Samples of foxes will be procured from London , Newcastle, as well as Glasgow and the surrounding countryside, which may require some field work. Tissue from these samples will be used to provide DNA for investigation of genome-wide variation to determine regions of allelic differentiation between urban and rural populations. This will take advantage of an existing red fox genome and the latest cutting-edge sequencing approaches.

Other phenotypic features would ideally be sampled from the same individuals used for genomic investigation to enable relationships to be established and test the key prediction that multiple traits correspondingly change. Skull morphology would be investigated through 3D morphometric approaches using geometric morphometrics. This would enable tests for urban/rural divergence and determine whether the same type of divergence is occurring between London, Newcastle and Glasgow study areas (i.e. tests of parallel divergence).

Additional anatomical features should correspondingly change with skull morphology that are developmentally linked and related to ‘domestication syndrome’ (Wilkins et al. 2014). To address this the student would dissect and identify the size of the adrenal gland. The size of the adrenal gland is important for determining the degree of fear response in animals. Therefore, depending on student interest it is also possible they could perform behavioural investigations including flight initiation distance assays in sets of urban and rural foxes.

Dietary analysis will include general investigations of stomach contents as well as metagenomic sequencing of scats. This approach involves sequencing prey material from scats and then using bioinformatics to compare sequences to available reference databases, allowing precise identification of dietary differences between urban and rural populations (Deiner et al. 2017).

Project Timeline

Year 1

– Collection of samples from study areas for genomic approaches, and other phenotypic traits (skull, diet)
– Extraction of DNA and preparation of libraries for sequencing
– Begin acquiring morphometric data from samples

Year 2

– Analysis of genomic data
– Conduct analysis of skull shape variation and diet
– Begin writing first manuscript
– Initiate behavioural investigations of flight initiation distance
– Presentation at a national or international conference

Year 3

– Analysis of data and writing of manuscripts
– Analysis of flight initiation distance data
– Presentation at a national or international conference

Year 3.5

– Finalize analyses
– Writing of the thesis and completion

Training
& Skills

The training provided by this project will cover a broad suite of skills from quantitative to molecular approaches and their analysis. This, combined with extensive sampling of wild fox populations, will provide the student with an extremely strong basis for pursuing further research in their areas of interest or for transitioning to roles in growth areas such as conservation science.
The scholar will be based within IBAHCM under the supervision of Dr Kevin Parsons. Dr Davide Dominoni, an expert in urban ecology and also at IBAHCM, will co-supervise the student and will provide support for the quantification of urbanisation at every sampling location. At IBAHCM the student will be exposed to a lively research environment that is also highly social. Several special interest groups are present in the institute that will help the student develop theoretical and practical skills, including the Evolutionary Analysis group, the Spatial Ecology group and the Statistics group.
In year 1, the student will receive training in lab protocols for genomic analysis and morphometrics, and for statistical protocols to quantify urbanisation gradients, through the support of the local supervisors. They will also receive training from co-supervisor Dr. Andreanna Welch at Durham in diet metagenomics. In year 2, the student will develop skills in bioinformatics through a dedicated course on genomic analyses and through support from supervisors. This will focus on integrating different datasets from phenotypic traits, dietary variation, and allelic differences between habitats. The student will be provided opportunities to attend a conference and to join retreat sessions on scientific writing for their first manuscript. In year 3, through participation in Institute seminars and national and international conferences, she/he will also develop presentation and communication skills.

References & further reading

Axelsson, E., Ratnakumar, A., Arendt, M. et al. 2013. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495: 360-364.

Deiner, K, Bik, HM, Mächler, E, et al. 2017. Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Mol Ecol. 26: 5872-5895.

Kukekova A et al. 2018. Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours. Nat. Ecol. Evol. 2: 1479-1491.

Parsons KJ, Rigg A, Conith AJ, et al. 2020. Skull morphology diverges between urban and rural populations of red foxes mirroring patterns of domestication and macroevolution. Proc R Soc. B Biol. Sci. 287: 20200763.

Pollock, C.J., Capilla-Lasheras, P., McGill, R.A.R. et al. Integrated behavioural and stable isotope data reveal altered diet linked to low breeding success in urban-dwelling blue tits (Cyanistes caeruleus). Sci Rep 7, 5014 (2017).

Salmón P, Jacobs A, Ahrén D, Biard C, Dingemanse NJ, Dominoni D, et al. 2020. Repeated genomic signatures of adaptation to urbanisation in a songbird across Europe
bioRxiv 2020.05.05.078568; doi: https://doi.org/10.1101/2020.05.05.078568

Wilkins AS, Wrangham RW, Tecumseh Fitch W. 2014The ‘domestication syndrome’ in mammals: a unified explaination based on neural crest cell behaviour and genetics. Genetics 197: 795-808.

Further Information

Application procedure: For IAPETUS2 applications to the University of Glasgow please use the dedicated application portal: www.gla.ac.uk/ScholarshipApp (you will still need to submit your administrative details to the IAPETUS2 website as well).

This project is in competition with others for funding, and success will depend on the quality of applicants. Funding includes tuition fee waiver for Glasgow University, a competitive stipend, and research support. Please contact Dr. Kevin Parsons for further information (Kevin.Parsons@glasgow.ac.uk) by early January 2021. Kevin.Parsons@glasgow.ac.uk

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