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Relatedness within colonies of three North American species of carpenter ants (Subgenus: Camponotus) and a comparison with relatedness estimates across Formicinae

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Abstract

Understanding a haplodiploid species’ social structure and quantifying relatedness among individuals are both important when designing sampling schemes or identifying potential biases in population genetics studies. However, it is not always possible to accurately identify social structure of study species in the field, or to collect large numbers of individuals from a single colony to estimate relatedness with methods that rely on accurate estimation of allele frequencies. Here, we assessed the utility of allele-frequency-free inference of relationships in haplodiploid ant colonies, while using limited sample sizes. Using genome-wide single-nucleotide polymorphism data, we measured intracolony relatedness and kinship estimates consistent with full-sister relationships among workers in three Nearctic species: Camponotus herculeanus, C. laevissimus, and C. modoc. Notably, the allele-frequency-free inference of relationships clearly demonstrated these full-sister relationships without ambiguity; this result suggests the utility of these methods for identifying closely related individuals in population genetics studies of haplodiploid organisms. We additionally performed a literature review of relatedness estimates in the subfamily Formicinae both as a compiled resource and to place our results in context within this larger clade of ants. Our results suggestive of Camponotus colonies founded by a lone singly mated queen are consistent with previously published relatedness estimates in the genus Camponotus that have generally shown high intracolony relatedness.

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Data availability

All raw sequencing data is at NCBI’s SRA repository with an accession under BioProject # PRJNA874018. Mitochondrial DNA sequences are uploaded to NCBI GenBank (OQ325048-OQ325100). Code used for analyses in this project is available on GithHub: github.com/jdmanthey/camponotus_relatedness_revised.

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Acknowledgements

This work was supported by Texas Tech University startup funds to JDM (sequencing) and National Science Foundation award #1953688 to JDM (support of undergraduate research students). Mohamed Fokar at the TTU Center for Biotechnology & Genomics provided sequencing support. The TTU Center for Biotechnology & Genomics acquisition of the NovaSeq6000 was supported by NIH grant 1S10OD025115-01. The High-Performance Computing Center at TTU supported computational analyses. The Invertebrate Zoology Collection of the Museum of Texas tech University houses voucher specimens of the colonies used in this study.

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  1. Department of Biological Sciences, Texas Tech University, Lubbock, TX, USA

    B. A. Meadows, M. Emad, J. P. Hruska, J. Silva, G. J. Behrends & J. D. Manthey

  2. Natural Science Research Laboratory, Museum of Texas Tech University, Lubbock, TX, USA

    J. C. Girón & J. D. Manthey

Authors
  1. B. A. Meadows
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  2. M. Emad
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  3. J. P. Hruska
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  4. J. Silva
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  5. G. J. Behrends
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  6. J. C. Girón
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  7. J. D. Manthey
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Contributions

All authors contributed to data analysis and writing and revision of the manuscript. JDM and JPH performed fieldwork. JDM performed DNA extractions. JCG and JDM took ant specimen photographs.

Corresponding author

Correspondence to J. D. Manthey.

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The authors declare no conflict of interest.

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Appendix 1

Appendix 1

See Table 3

Table 3 Summary of the scientific literature review for studies using genetic markers to estimate within-colony worker-worker relatedness in the Formicinae
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Meadows, B.A., Emad, M., Hruska, J.P. et al. Relatedness within colonies of three North American species of carpenter ants (Subgenus: Camponotus) and a comparison with relatedness estimates across Formicinae. Insect. Soc. 70, 191–202 (2023). https://doi.org/10.1007/s00040-023-00906-7

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