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Uncovering how behavioral variation underlying mutualist partner quality is partitioned within a species complex of keystone seed-dispersing ants

Abstract

Generalized mutualisms, such as seed dispersal by ants (myrmecochory), involve guilds of mutualistic partners that exchange services. Partners within guilds vary in traits that affect the quality of mutualistic services. Research aimed at uncovering within-guild variation in partner quality primarily considers the identity of partner species. However, mutualism-related traits vary within species, especially for populations in states of incomplete speciation where the distinction between intra- and interspecific variation is not well defined. Ants in the genus Aphaenogaster are mutualists and the major disperser of seeds of understory plants adapted to dispersal by ants (myrmecochores) in eastern North American forests. A. rudis and A. picea are polyphyletic with overlapping morphological features. We ask if functional variation partitions discretely between named species or along a continuum in this species complex. We collected replicate colonies of three populations, each of the named species. We performed 2D morphometrics on the thorax to quantify complex morphological variation among colonies. We performed lab behavioral trials, measuring behaviors that influence seed dispersal quality such as foraging, seed dispersal rate and preference, and intra- and interspecific aggression. Morphometrics revealed differences between species but also continuous variation in diagnostic features. We found behavioral differences between species, with A. rudis being a better disperser and having higher intraspecific aggression and A. picea being a more active forager and dominant over A. rudis. Behavior also varied along a continuum between species corresponding with colony morphometrics, with intermediate phenotypes having intermediate behavior. This work shows that it is important to consider partner identity in species complexes of mutualistic partners at multiple levels of biological organization.

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Data availability

Data and code are available on FigShare (link will be made public upon publication).

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Acknowledgements

We would like to thank Carly Gerth and Elisa Buono who helped with field collections. Lena Eder, Dylan Jones, Jesse Lofaso, and John Santare helped with the ant box assembly. Alycia Lackey provided invaluable advice on our morphometric analysis. This research was funded by Binghamton University, including the Summer Scholars Program (WRS, AJL), Provost Fellowships (CMB, GIQ), and the Presidential Diversity Grant (KMP). This project was also funded by a grant from the Torrey Botanical Society (CMB) and a grant from the Theodore Roosevelt Memorial Fund of the American Museum of Natural History (GIQ). We thank several land managers for access to their property: Cornell Botanical Garden, The Nature Conservancy, New York City Department of Parks & Recreation, Rutgers University Ecological Preserve, Rutgers University Hutcheson Memorial Forest Center, and Binghamton University. This work was conducted on Haudenosaunee, Susquehannock, Lenni-Lenape, and Munsee Lenape ancestral lands; land that Indigenous communities were forcibly removed from. We acknowledge Indigenous peoples as the original stewards of this land and honor the lasting relationship between these nations and the land. We offer this land acknowledgement to affirm Indigenous sovereignty, history, and experiences connected with these regions and we hope to advocate for increased Indigenous recognition within the scientific and research community.

Funding

Funding was provided by Binghamton University (K. Prior, T. Powell), including through the Summer Scholars Program (W. Smisko, A. Lupinski), Presidential Diversity Grant (K. Prior), Provost Fellowships (C. Buono, G. Quartuccia), and Graduate School Rosa Colecchio Travel Award (C. Buono), along with the Torrey Botanical Society (C. Buono), and the Theodore Roosevelt Memorial Fund of the American Museum of Natural History (G. Quartuccia).

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KP, TP, CB, GQ developed the idea. CB, WS, AL, GQ, AR designed and performed the research. KP, CB, AL, GQ analyzed the data with input from TP. KP, TP, CB, GQ wrote the introduction/discussion. CB, WS, AR, AL, GQ wrote the methods with input from KP and TP.

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Correspondence to K. M. Prior.

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Buono, C.M., Quartuccia, G.I., Smisko, W.R. et al. Uncovering how behavioral variation underlying mutualist partner quality is partitioned within a species complex of keystone seed-dispersing ants. Insect. Soc. 69, 247–260 (2022). https://doi.org/10.1007/s00040-022-00865-5

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Keywords

  • Myrmecochory
  • Aphaenogaster
  • Seed dispersal
  • Mutualism
  • Species complex
  • Intraspecific variation
  • Morphometrics