Time trees and clock genes: a systematic review and comparative analysis of contemporary avian migration genetics

Author:

Le Clercq Louis‐Stéphane12ORCID,Bazzi Gaia3ORCID,Cecere Jacopo G.3ORCID,Gianfranceschi Luca4ORCID,Grobler Johannes Paul2ORCID,Kotzé Antoinette12ORCID,Rubolini Diego56ORCID,Liedvogel Miriam78ORCID,Dalton Desiré Lee9ORCID

Affiliation:

1. South African National Biodiversity Institute P.O. Box 754 Pretoria 0001 South Africa

2. Department of Genetics University of the Free State PO Box 339 Bloemfontein 9300 South Africa

3. Area Avifauna Migratrice, Istituto Superiore per la Protezione e la Ricerca Ambientale via Ca' Fornacetta 9 Ozzano Emilia (BO) I‐40064 Italy

4. Dipartimento di Bioscienze Università degli Studi di Milano via Celoria 26 Milan I‐20133 Italy

5. Dipartimento di Scienze e Politiche Ambientali Università degli Studi di Milano via Celoria 26 Milan I‐20133 Italy

6. Istituto di Ricerca sulle Acque, IRSA‐CNR Via del Mulino 19 Brugherio (MB) I‐20861 Italy

7. Max Planck Research Group Behavioral Genomics, Max Planck Institute for Evolutionary Biology Plön 24306 Germany

8. Institute of Avian Research An der Vogelwarte 21 Wilhelmshaven 26386 Germany

9. School of Health and Life Sciences, Teesside University Middlesbrough TS1 3BA UK

Abstract

ABSTRACTTiming is a crucial aspect for survival and reproduction in seasonal environments leading to carefully scheduled annual programs of migration in many species. But what are the exact mechanisms through which birds (class: Aves) can keep track of time, anticipate seasonal changes, and adapt their behaviour? One proposed mechanism regulating annual behaviour is the circadian clock, controlled by a highly conserved set of genes, collectively called ‘clock genes’ which are well established in controlling the daily rhythmicity of physiology and behaviour. Due to diverse migration patterns observed within and among species, in a seemingly endogenously programmed manner, the field of migration genetics has sought and tested several candidate genes within the clock circuitry that may underlie the observed differences in breeding and migration behaviour. Among others, length polymorphisms within genes such as Clock and Adcyap1 have been hypothesised to play a putative role, although association and fitness studies in various species have yielded mixed results. To contextualise the existing body of data, here we conducted a systematic review of all published studies relating polymorphisms in clock genes to seasonality in a phylogenetically and taxonomically informed manner. This was complemented by a standardised comparative re‐analysis of candidate gene polymorphisms of 76 bird species, of which 58 are migrants and 18 are residents, along with population genetics analyses for 40 species with available allele data. We tested genetic diversity estimates, used Mantel tests for spatial genetic analyses, and evaluated relationships between candidate gene allele length and population averages for geographic range (breeding‐ and non‐breeding latitude), migration distance, timing of migration, taxonomic relationships, and divergence times. Our combined analysis provided evidence (i) of a putative association between Clock gene variation and autumn migration as well as a putative association between Adcyap1 gene variation and spring migration in migratory species; (ii) that these candidate genes are not diagnostic markers to distinguish migratory from sedentary birds; and (iii) of correlated variability in both genes with divergence time, potentially reflecting ancestrally inherited genotypes rather than contemporary changes driven by selection. These findings highlight a tentative association between these candidate genes and migration attributes as well as genetic constraints on evolutionary adaptation.

Funder

National Research Foundation

Publisher

Wiley

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology

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