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Population genomics of Sociable Weavers Philetairus socius reveals considerable admixture among colonies

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Abstract

The evolution of sociality often leads to genetic structuring among groups and alters the evolutionary forces that the groups experience. Describing the genetic structuring of social species is, therefore, necessary to understand the selective forces that act on a species. While recent work has used genomic methods to investigate population structure in eusocial insects, relatively little genomic work has examined population structure in the largest non-human mammal and avian clades. We delimited population genetic structuring in Sociable Weavers (Philetairus socius), a passerine that lives in large, stable, perennial colonies, using the genotyping-by-sequencing approach to generate a dataset of several thousand SNPs. We used the SNPs to estimate genetic structuring within and among eight nests. While we document relatively low levels of genetic structuring among nests, the structuring was not explained by distance between nests. We also found significantly higher structuring among male Sociable Weavers compared to female weavers, suggesting that female Sociable Weavers are more prone to dispersal in this species. Not all nests represent distinct genetic groups according to Bayesian clustering analysis, which is unsurprising given the low differentiation among nests, especially compared to other social species. In almost all colonies there was less heterozygosity than expected, possibly due to reproductive skew within each colony.

Zusammenfassung

Populationsgenomik von Siedelwebern ( Philetairus socius ) zeigt beträchtliche Vermischung zwischen Kolonien Die Evolution von Sozialität führt oftmals zu einer genetischen Strukturierung zwischen Gruppen und verändert die evolutiven Kräfte, welche die Gruppen erfahren. Eine Beschreibung der genetischen Strukturierung sozialer Arten ist daher notwendig, um zu verstehen, welche Selektionskräfte auf eine Art wirken. Während neuere Arbeiten genomische Methoden verwendet haben, um die Populationsstruktur eusozialer Insekten zu untersuchen, gibt es bislang nur relativ wenige genomische Arbeiten zur Populationsstruktur in den größten nicht-humanen Säuger- und Vogelkladen. Wir haben die genetische Populationsstruktur beim Siedelweber (Philetairus socius) abgesteckt, einem Sperlingsvogel, der in großen, stabilen, mehrjährigen Kolonien lebt. Wir haben den Genotypisierung-durch-Sequenzierung-Ansatz verwendet, um einen aus mehreren Tausend SNPs bestehenden Datensatz zu generieren. Wir haben die SNPs verwendet, um die genetische Strukturierung innerhalb und zwischen acht Nestern abzuschätzen. Wir dokumentieren ein relativ niedriges Ausmaß genetischer Strukturierung zwischen Nestern, was nicht durch die Entfernung zwischen den Nestern erklärt werden kann. Wir fanden signifikant stärkere Strukturierung zwischen männlichen Siedelwebern als zwischen weiblichen Siedelwebern, was darauf hindeutet, dass weibliche Siedelweber eher zur Abwanderung neigen. Gemäß einer Bayesschen Clusteranalyse stellen nicht alle Nester distinkte genetische Gruppen dar, was angesichts der besonders im Vergleich zu anderen sozialen Arten geringen Differenzierung zwischen Nestern nicht überraschend ist. In fast allen Kolonien war die Heterozygosität geringer als erwartet, möglicherweise aufgrund von reproduktiver Asymmetrie innerhalb jeder Kolonie.

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Acknowledgments

We thank William Searcy and other members of the Department of Biology for the constructive suggestions that improved this paper. We thank Elizabeth Cooper for providing guidance on the bioinformatics software and we thank Cornell’s Institute for Genomic Diversity for assistance with NGS. We thank Dirk Heinrich and Holger Kolberg for support carrying out the field work. This work was funded via a National Science Foundation Doctoral Dissertation Improvement Grant (#121500), funding from the University of Miami College of Arts and Sciences, and funding from the William Maytag Endowment. The University of Miami IACUC (permit number: 12-098) and the Ministry of Environment and Tourism (permit number: 1866) provided permits that allowed for this work. The work was performed on private land in central Namibia. We followed the ethics of IACUC and the Animal Behavior Society in performing this work. We thank two anonymous reviewers for suggestions that improved the manuscript.

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All raw data will be deposited in NCBI’s short read sequence archive.

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Correspondence to Gavin M. Leighton.

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Communicated by M. Wink.

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Leighton, G.M., Echeverri, S. Population genomics of Sociable Weavers Philetairus socius reveals considerable admixture among colonies. J Ornithol 157, 483–492 (2016). https://doi.org/10.1007/s10336-015-1307-1

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