Gene expression in the brain of a migratory songbird during breeding and migration.

John Boss,Sara Naurin,Dennis Hasselquist,Max Lundberg,Nils Reischke,Peter Olsson,Mats Grahn,Miriam Liedvogel,Susanne Åkesson,Staffan Bensch,Anthony Wright

doi:10.1186/s40462-016-0069-6

Abstract

BackgroundWe still have limited knowledge about the underlying genetic mechanisms that enable migrating species of birds to navigate the globe. Here we make an attempt to get insight into the genetic architecture controlling this complex innate behaviour. We contrast the gene expression profiles of two closely related songbird subspecies with divergent migratory phenotypes. In addition to comparing differences in migratory strategy we include a temporal component and contrast patterns between breeding adults and autumn migrating juvenile birds of both subspecies. The two willow warbler subspecies, Phylloscopus trochilus trochilus and P. t. acredula, are remarkably similar both in phenotype and genotype and have a narrow contact zone in central Scandinavia. Here we used a microarray gene chip representing 23,136 expressed sequence tags (ESTs) from the zebra finch Taeniopygia guttata to identify mRNA level differences in willow warbler brain tissue in relation to subspecies and season.ResultsOut of the 22,109 EST probe sets that remained after filtering poorly binding probes, we found 11,898 (51.8 %) probe sets that could be reliably and uniquely matched to a total of 6,758 orthologous zebra finch genes. The two subspecies showed very similar levels of gene expression with less than 0.1 % of the probe sets being significantly differentially expressed. In contrast, 3,045 (13.8 %) probe sets were found to be differently regulated between samples collected from breeding adults and autumn migrating juvenile birds. The genes found to be differentially expressed between seasons appeared to be enriched for functional roles in neuronal firing and neuronal synapse formation.ConclusionsOur results show that only few genes are differentially expressed between the subspecies. This suggests that the different migration strategies of the subspecies might be governed by few genes, or that the expression patterns of those genes are time-structured or tissue-specific in ways, which our approach fails to uncover. Our findings will be useful in the planning of new experiments designed to unravel the genes involved in the migratory program of birds.Electronic supplementary materialThe online version of this article (doi:10.1186/s40462-016-0069-6) contains supplementary material, which is available to authorized users.

Highlights

We still have limited knowledge about the underlying genetic mechanisms that enable migrating species of birds to navigate the globe
Whereas quantitative genetic studies demonstrate the presence or absence of within-species genetic variation associated with migratory traits, they do not provide data required for testing whether the same or different genes are involved in the migratory phenotypes of different species [14]
Gene expression differences associated with seasonal sampling time dominated the clustering result and allowed to perfectly separate the birds

Summary

Introduction

We still have limited knowledge about the underlying genetic mechanisms that enable migrating species of birds to navigate the globe. In addition to comparing differences in migratory strategy we include a temporal component and contrast patterns between breeding adults and autumn migrating juvenile birds of both subspecies. We used a microarray gene chip representing 23,136 expressed sequence tags (ESTs) from the zebra finch Taeniopygia guttata to identify mRNA level differences in willow warbler brain tissue in relation to subspecies and season. We may expect differentially migrating bird populations to differ in genes encoding for several adaptations directly or indirectly linked to modulation of the migratory phenotype. Whereas quantitative genetic studies demonstrate the presence or absence of within-species genetic variation associated with migratory traits, they do not provide data required for testing whether the same or different genes are involved in the migratory phenotypes of different species [14]. A microsatellite polymorphism in the 3′-UTR of the gene encoding Adenylate Cyclase Activating Polypeptide 1 (ADCYAP1) was found to explain a small but significant proportion of migratory restlessness within populations, as well as variation in migratory distance across populations [17]

Methods

Results

Discussion

Conclusion