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Available from: https:\/\/CRAN.R-project.org\/package=movMF."},{"issue":"1\/2","key":"pcbi.1012029.ref046","doi-asserted-by":"crossref","first-page":"256","DOI":"10.2307\/2334214","article-title":"A distribution-free two-sample test on a circle","volume":"51","author":"S Wheeler","year":"1964","journal-title":"Biometrika"},{"issue":"1","key":"pcbi.1012029.ref047","doi-asserted-by":"crossref","first-page":"20337","DOI":"10.1038\/s41598-021-99299-5","article-title":"Advice on comparing two independent samples of circular data in biology","volume":"11","author":"L Landler","year":"2021","journal-title":"Scientific reports"},{"key":"pcbi.1012029.ref048","unstructured":"Agostinelli C, Lund U. R package circular: Circular Statistics (version 0.4-93); 2017. Available from: https:\/\/r-forge.r-project.org\/projects\/circular\/."},{"issue":"10","key":"pcbi.1012029.ref049","doi-asserted-by":"crossref","DOI":"10.18637\/jss.v031.i10","article-title":"CircStat: A MATLAB Toolbox for Circular Statistics","volume":"31","author":"P Berens","year":"2009","journal-title":"Journal of Statistical Software"},{"key":"pcbi.1012029.ref050","unstructured":"Zar JH. Biostatistical Analysis. Prentice-Hall international editions. Prentice Hall; 1999. Available from: https:\/\/books.google.com\/books?id=edxqAAAAMAAJ."},{"issue":"1","key":"pcbi.1012029.ref051","doi-asserted-by":"crossref","first-page":"1927","DOI":"10.1038\/s41467-020-15617-x","article-title":"Circadian regulation of mitochondrial uncoupling and lifespan","volume":"11","author":"M Ulgherait","year":"2020","journal-title":"Nature Communications"},{"issue":"7880","key":"pcbi.1012029.ref052","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1038\/s41586-021-03934-0","article-title":"Circadian autophagy drives iTRF-mediated longevity","volume":"598","author":"M Ulgherait","year":"2021","journal-title":"Nature"},{"issue":"1","key":"pcbi.1012029.ref053","doi-asserted-by":"crossref","first-page":"2054","DOI":"10.1038\/srep02054","article-title":"Cold-induced RNA-binding proteins regulate circadian gene expression by controlling alternative polyadenylation","volume":"3","author":"Y Liu","year":"2013","journal-title":"Scientific 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