Adaptive evolution and loss of a putative magnetoreceptor in passerines

Author:

Langebrake Corinna12ORCID,Manthey Georg13ORCID,Frederiksen Anders3ORCID,Lugo Ramos Juan S.24ORCID,Dutheil Julien Y.5ORCID,Chetverikova Raisa6ORCID,Solov'yov Ilia A.378ORCID,Mouritsen Henrik67ORCID,Liedvogel Miriam126ORCID

Affiliation:

1. Institute of Avian Research ‘Vogelwarte Helgoland’, 26386 Wilhelmshaven, Germany

2. MPRG Behavioural Genomics, MPI Evolutionary Biology, 24306 Plön, Germany

3. Department of Physics, Carl von Ossietzky Universität Oldenburg, 26129 Oldenburg

4. The Francis Crick Institute, London NW1 1AT, UK

5. Research Group Molecular Systems Evolution, MPI Evolutionary Biology, 24306 Plön, Germany

6. Biology and Environmental Sciences Department, Carl von Ossietzky Universität Oldenburg, 26129 Oldenburg

7. Research Centre for Neurosensory Sciences, Carl von Ossietzky Universität Oldenburg, 26129 Oldenburg

8. Center for Nanoscale Dynamics (CENAD), Carl von Ossietzky Universität Oldenburg, 26129 Oldenburg

Abstract

Migratory birds possess remarkable accuracy in orientation and navigation, which involves various compass systems including the magnetic compass. Identifying the primary magnetosensor remains a fundamental open question. Cryptochromes (Cry) have been shown to be magnetically sensitive, and Cry4a from a migratory songbird seems to show enhanced magnetic sensitivity in vitro compared to Cry4a from resident species. We investigate Cry and their potential involvement in magnetoreception in a phylogenetic framework, integrating molecular evolutionary analyses with protein dynamics modelling. Our analysis is based on 363 bird genomes and identifies different selection regimes in passerines. We show that Cry4a is characterized by strong positive selection and high variability, typical characteristics of sensor proteins. We identify key sites that are likely to have facilitated the evolution of an optimized sensory protein for night-time orientation in songbirds. Additionally, we show that Cry4 was lost in hummingbirds, parrots and Tyranni (Suboscines), and thus identified a gene deletion, which might facilitate testing the function of Cry4a in birds. In contrast, the other avian Cry (Cry1 and Cry2) were highly conserved across all species, indicating basal, non-sensory functions. Our results support a specialization or functional differentiation of Cry4 in songbirds which could be magnetosensation.

Funder

Deutsche Forschungsgemeinschaft

European Union HOrizon 2020 research and innovation program

Ministry for Science and Culture of Lower Saxony

Volkswagen Foundation

Max Planck Society

Publisher

The Royal Society

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