The genomic basis of evolutionary differentiation among honey bees
- Bertrand Fouks1,2,
- Philipp Brand3,4,
- Hung N. Nguyen5,
- Jacob Herman1,
- Francisco Camara6,
- Daniel Ence7,8,
- Darren E. Hagen9,
- Katharina J. Hoff10,11,
- Stefanie Nachweide10,
- Lars Romoth10,
- Kimberly K.O. Walden12,
- Roderic Guigo6,13,
- Mario Stanke10,11,
- Giuseppe Narzisi14,
- Mark Yandell8,15,
- Hugh M. Robertson12,
- Nikolaus Koeniger16,
- Panuwan Chantawannakul17,
- Michael C. Schatz18,
- Kim C. Worley19,
- Gene E. Robinson12,20,21,
- Christine G. Elsik5,22,23 and
- Olav Rueppell1,24
- 1Department of Biology, University of North Carolina at Greensboro, Greensboro, North Carolina 27403, USA;
- 2Institute for Evolution and Biodiversity, Molecular Evolution and Bioinformatics, Westfälische Wilhelms-Universität, 48149 Münster, Germany;
- 3Department of Evolution and Ecology, Center for Population Biology, University of California, Davis, Davis, California 95161, USA;
- 4Laboratory of Neurophysiology and Behavior, The Rockefeller University, New York, New York 10065, USA;
- 5MU Institute for Data Science and Informatics, University of Missouri, Columbia, Missouri 65211, USA;
- 6Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, 08036 Barcelona, Spain;
- 7School of Forest Resources and Conservation, University of Florida, Gainesville, Florida 32611, USA;
- 8Department of Human Genetics, University of Utah, Salt Lake City, Utah 84112, USA;
- 9Department of Animal and Food Sciences, Oklahoma State University, Stillwater, Oklahoma 74078, USA;
- 10University of Greifswald, Institute for Mathematics and Computer Science, Bioinformatics Group, 17489 Greifswald, Germany;
- 11University of Greifswald, Center for Functional Genomics of Microbes, 17489 Greifswald, Germany;
- 12Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- 13Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain;
- 14New York Genome Center, New York, New York 10013, USA;
- 15Utah Center for Genetic Discovery, University of Utah, Salt Lake City, Utah 84112, USA;
- 16Department of Behavioral Physiology and Sociobiology (Zoology II), University of Würzburg, 97074 Würzburg, Germany;
- 17Environmental Science Research Center (ESRC) and Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand;
- 18Departments of Computer Science and Biology, Johns Hopkins University, Baltimore, Maryland 21218, USA;
- 19Department of Molecular and Human Genetics, Human Genome Sequencing Center, Baylor College of Medicine, Houston, Texas 77030, USA;
- 20Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- 21Neuroscience Program, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- 22Division of Animal Sciences, University of Missouri, Columbia, Missouri 65211, USA;
- 23Division of Plant Sciences, University of Missouri, Columbia, Missouri 65211, USA;
- 24Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
Abstract
In contrast to the western honey bee, Apis mellifera, other honey bee species have been largely neglected despite their importance and diversity. The genetic basis of the evolutionary diversification of honey bees remains largely unknown. Here, we provide a genome-wide comparison of three honey bee species, each representing one of the three subgenera of honey bees, namely the dwarf (Apis florea), giant (A. dorsata), and cavity-nesting (A. mellifera) honey bees with bumblebees as an outgroup. Our analyses resolve the phylogeny of honey bees with the dwarf honey bees diverging first. We find that evolution of increased eusocial complexity in Apis proceeds via increases in the complexity of gene regulation, which is in agreement with previous studies. However, this process seems to be related to pathways other than transcriptional control. Positive selection patterns across Apis reveal a trade-off between maintaining genome stability and generating genetic diversity, with a rapidly evolving piRNA pathway leading to genomes depleted of transposable elements, and a rapidly evolving DNA repair pathway associated with high recombination rates in all Apis species. Diversification within Apis is accompanied by positive selection in several genes whose putative functions present candidate mechanisms for lineage-specific adaptations, such as migration, immunity, and nesting behavior.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.272310.120.
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Freely available online through the Genome Research Open Access option.
- Received September 30, 2020.
- Accepted April 22, 2021.
This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
