Testosterone pulses paired with a location induce a place preference to the nest of a monogamous mouse under field conditions

  1. Radmila Petric  Is a corresponding author
  2. Matina C Kalcounis-Rueppell
  3. Catherine A Marler
  1. University of North Carolina at Chapel Hill, United States
  2. University of Alberta, Canada
  3. University of Wisconsin-Madison, United States

Abstract

Changing social environments such as the birth of young or aggressive encounters present a need to adjust behavior. Previous research examined how long-term changes in steroid hormones mediate these adjustments. We tested the novel concept that the rewarding effects of transient testosterone pulses (T-pulses) in males after social encounters alters their spatial distribution on a territory. In free-living monogamous California mice (Peromyscus californicus), males administered three T-injections at the nest spent more time at the nest than males treated with placebo injections. This mimics T-induced place preferences in the laboratory. Female mates of T-treated males spent less time at the nest but the pair produced more vocalizations and call types than controls. Traditionally, transient T-changes were thought to have transient behavioral effects. Our work demonstrates that in the wild, when T-pulses occur in a salient context such as a territory, the behavioral effects last days after T-levels return to baseline.

Data availability

All data analysed for this study are included in the manuscript and supporting files. Source data files have been provided for all figures.Petric, Radmila. 2021. "T-Pulses at the Nest." OSF. osf.io/qknze.doi.org/10.17605/OSF.IO/QKNZE

Article and author information

Author details

  1. Radmila Petric

    Institute for the Environment, University of North Carolina at Chapel Hill, Chapel Hill, United States
    For correspondence
    r_petric@uncg.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2651-3328
  2. Matina C Kalcounis-Rueppell

    Biological Sciences, University of Alberta, Edmonton, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Catherine A Marler

    Psychology, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (1355163)

  • Matina C Kalcounis-Rueppell
  • Catherine A Marler

Sigma Xi (Spring 2018)

  • Radmila Petric

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal care and use guidelines were followed and research protocols for this study were approved by the University of North Carolina at Greensboro and University of Wisconsin-Madison Institutional Animal Care and Use Committees (IACUC; UNCG 12-004 and UWM L005047-A01) and by California Department of Fish and Wildlife under Scientific Collection Permits (SC-9663 and SC-13190).

Reviewing Editor

  1. Kristin Tessmar-Raible, University of Vienna, Austria

Publication history

  1. Received: December 16, 2020
  2. Preprint posted: January 4, 2021 (view preprint)
  3. Accepted: March 29, 2022
  4. Accepted Manuscript published: March 30, 2022 (version 1)
  5. Version of Record published: April 21, 2022 (version 2)

Copyright

© 2022, Petric et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 563
    Page views
  • 60
    Downloads
  • 1
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Radmila Petric
  2. Matina C Kalcounis-Rueppell
  3. Catherine A Marler
(2022)
Testosterone pulses paired with a location induce a place preference to the nest of a monogamous mouse under field conditions
eLife 11:e65820.
https://doi.org/10.7554/eLife.65820

Further reading

    1. Ecology
    2. Epidemiology and Global Health
    Carolina Oliveira de Santana, Pieter Spealman, Gabriel G Perron
    Insight

    The global spread of antibiotic resistance could be due to a number of factors, and not just the overuse of antibiotics in agriculture and medicine as previously thought.

    1. Ecology
    2. Evolutionary Biology
    Naïma Madi, Daisy Chen ... Nandita R Garud
    Research Advance Updated

    How the ecological process of community assembly interacts with intra-species diversity and evolutionary change is a longstanding question. Two contrasting hypotheses have been proposed: Diversity Begets Diversity (DBD), in which taxa tend to become more diverse in already diverse communities, and Ecological Controls (EC), in which higher community diversity impedes diversification. Previously, using 16S rRNA gene amplicon data across a range of microbiomes, we showed a generally positive relationship between taxa diversity and community diversity at higher taxonomic levels, consistent with the predictions of DBD (Madi et al., 2020). However, this positive 'diversity slope' plateaus at high levels of community diversity. Here we show that this general pattern holds at much finer genetic resolution, by analyzing intra-species strain and nucleotide variation in static and temporally sampled metagenomes from the human gut microbiome. Consistent with DBD, both intra-species polymorphism and strain number were positively correlated with community Shannon diversity. Shannon diversity is also predictive of increases in polymorphism over time scales up to ~4-6 months, after which the diversity slope flattens and becomes negative – consistent with DBD eventually giving way to EC. Finally, we show that higher community diversity predicts gene loss at a future time point. This observation is broadly consistent with the Black Queen Hypothesis, which posits that genes with functions provided by the community are less likely to be retained in a focal species' genome. Together, our results show that a mixture of DBD, EC, and Black Queen may operate simultaneously in the human gut microbiome, adding to a growing body of evidence that these eco-evolutionary processes are key drivers of biodiversity and ecosystem function.