The genetics of migration in the Asian houbara bustard Chlamydotis macqueenii

Abstract

Migration allows birds to adapt to environmental conditions by moving to lower latitudes in winter and therefore overcoming low resource availability at their breeding grounds. This movement is optimized by population-specific strategies regarding timing, direction and duration of migration. Variation in migratory behaviour can be a consequence of adaptations to the environment driven by endogenous genetic mechanisms, but much uncertainty exists around the potential influence of these mechanisms on the migration process. In Asian houbara, both resident and migrant individuals occur across the distribution range. This partial migrant species can give precious insights on the genetic mechanisms underlying migration. To address these evolutionary questions on Asian houbara, it is crucial to have a solid genomic foundation with a high-quality genome assembly and a robust annotation.

To explore the influence of genetic mechanisms on the migration of Asian houbara, we evaluated and compared the genomic resource already available for the species, we provided an improved annotation of its genome, and finally investigated genomic regions potentially involved in the evolution of migratory behaviour (using a candidate gene approach) using samples distributed across the whole distribution range and representing individuals with contrasted migratory behaviour.

We first evaluated the quality of the recent assembly and showed that it is 10-fold more contiguous (N50=2.88Mb) than the previous one and provides a completeness exceeding 96% based on the BUSCO protocol. Combining this genome assembly with four transcriptomic datasets (blood and embryos), we achieved a more complete annotation for Asian houbara reaching 17,992 genes, which is close to the 20,000 genes found in chicken. From the literature, we identified 14 candidate genes that have been linked to migration in birds, including the well-studied CLOCK and ADCYAP1 genes. Mining the new genome assembly, we found 13 of these candidate gene regions. We used hierarchical groupings (AMOVA), to evaluate the effect of migratory behaviour (migrant/resident) and geographic locations on the genetic variance. Sampling locations played a significant role on the genetic variation at seven candidate genes, and migratory behaviour had a significant effect on the variance of at least one gene (DIO2), highlighting its potential role in the migration of Asian houbara. The DIO2 gene has been shown to play a significant role in the metabolism of long-distance migrants in Swainson's thrush. Creating haplotype networks and haplotype heatmaps with the coding sequences of 13 genes confirm the role of geography, and reveal the possible role of migratory behaviour in other genes. Further investigation of amino acid changes in the coding sequences also supports these findings. The improved genomic resource for Asian houbara provides us with the potential to further investigate genomic variation in this species. It also provides a reference that can be used in the genome assembly and annotation of closely related species. The candidate gene approach in the present study gives further insights into genes that are potentially linked to migration which opens perspectives for future investigations and the conservation of Asian houbara.