Computed tomography shows high fracture prevalence among physically active forager-horticulturalists with high fertility

  1. Jonathan Stieglitz  Is a corresponding author
  2. Benjamin C Trumble
  3. HORUS Study Team
  4. Caleb Finch
  5. Dong Li
  6. Matthew J Budoff
  7. Hillard Kaplan
  8. Michael Gurven
  1. Universite Toulouse 1 Capitole, France
  2. Arizona State University, United States
  3. University of Southern California, United States
  4. Emory University, United States
  5. University of California, Los Angeles, United States
  6. Chapman University, United States
  7. University of California, Santa Barbara, United States

Abstract

Modern humans have more fragile skeletons than other hominins, which may result from physical inactivity. Here we test whether reproductive effort also compromises bone strength, by measuring using computed tomography thoracic vertebral bone mineral density (BMD) and fracture prevalence among physically active Tsimane forager-horticulturalists. Earlier onset of reproduction and shorter interbirth intervals are associated with reduced BMD for women. Tsimane BMD is lower versus Americans, but only for women, contrary to simple predictions relying on inactivity to explain skeletal fragility. Minimal BMD differences exist between Tsimane and American men, suggesting that systemic factors other than fertility (e.g. diet) do not easily explain Tsimane women's lower BMD. Tsimane fracture prevalence is also higher versus Americans. Lower BMD increases Tsimane fracture risk, but only for women, suggesting a role of weak bone in women's fracture etiology. Our results highlight the role of sex-specific mechanisms underlying skeletal fragility that operate long before menopause.

Data availability

The data that support the findings of this study are available on Dryad (http://dx.doi.org/10.5061/dryad.rf0g0md).

The following data sets were generated

Article and author information

Author details

  1. Jonathan Stieglitz

    Institute for Advanced Study in Toulouse, Universite Toulouse 1 Capitole, Toulouse, France
    For correspondence
    jonathan.stieglitz@iast.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5985-9643
  2. Benjamin C Trumble

    Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. HORUS Study Team

  4. Caleb Finch

    University of Southern California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7617-3958
  5. Dong Li

    Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Matthew J Budoff

    University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Hillard Kaplan

    Chapman University, Orange, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael Gurven

    University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (R01AG024119)

  • Jonathan Stieglitz
  • Benjamin C Trumble
  • Caleb Finch
  • Hillard Kaplan
  • Michael Gurven

Arizona State University

  • Benjamin C Trumble

University of California, Santa Barbara

  • Michael Gurven

Agence Nationale de la Recherche (ANR-17-EURE-0010)

  • Jonathan Stieglitz

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

Ethics

Human subjects: Institutional IRB approval was granted by UNM (HRRC # 07-157) and UCSB (# 3-16-0766), as was informed consent at three levels: (1) Tsimane government that oversees research projects, (2) village leadership and (3) study participants.

Copyright

© 2019, Stieglitz 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

  • 917
    views
  • 102
    downloads
  • 20
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Jonathan Stieglitz
  2. Benjamin C Trumble
  3. HORUS Study Team
  4. Caleb Finch
  5. Dong Li
  6. Matthew J Budoff
  7. Hillard Kaplan
  8. Michael Gurven
(2019)
Computed tomography shows high fracture prevalence among physically active forager-horticulturalists with high fertility
eLife 8:e48607.
https://doi.org/10.7554/eLife.48607

Share this article

https://doi.org/10.7554/eLife.48607

Further reading

    1. Evolutionary Biology
    Matthew Osmond, Graham Coop
    Research Article Updated

    Spatial patterns in genetic diversity are shaped by individuals dispersing from their parents and larger-scale population movements. It has long been appreciated that these patterns of movement shape the underlying genealogies along the genome leading to geographic patterns of isolation-by-distance in contemporary population genetic data. However, extracting the enormous amount of information contained in genealogies along recombining sequences has, until recently, not been computationally feasible. Here, we capitalize on important recent advances in genome-wide gene-genealogy reconstruction and develop methods to use thousands of trees to estimate per-generation dispersal rates and to locate the genetic ancestors of a sample back through time. We take a likelihood approach in continuous space using a simple approximate model (branching Brownian motion) as our prior distribution of spatial genealogies. After testing our method with simulations we apply it to Arabidopsis thaliana. We estimate a dispersal rate of roughly 60 km2/generation, slightly higher across latitude than across longitude, potentially reflecting a northward post-glacial expansion. Locating ancestors allows us to visualize major geographic movements, alternative geographic histories, and admixture. Our method highlights the huge amount of information about past dispersal events and population movements contained in genome-wide genealogies.

    1. Evolutionary Biology
    Dario Galanti, Jun Hee Jung ... Oliver Bossdorf
    Research Article

    Understanding the genomic basis of natural variation in plant pest resistance is an important goal in plant science, but it usually requires large and labor-intensive phenotyping experiments. Here, we explored the possibility that non-target reads from plant DNA sequencing can serve as phenotyping proxies for addressing such questions. We used data from a whole-genome and -epigenome sequencing study of 207 natural lines of field pennycress (Thlaspi arvense) that were grown in a common environment and spontaneously colonized by aphids, mildew, and other microbes. We found that the numbers of non-target reads assigned to the pest species differed between populations, had significant SNP-based heritability, and were associated with climate of origin and baseline glucosinolate contents. Specifically, pennycress lines from cold and thermally fluctuating habitats, presumably less favorable to aphids, showed higher aphid DNA load, i.e., decreased aphid resistance. Genome-wide association analyses identified genetic variants at known defense genes but also novel genomic regions associated with variation in aphid and mildew DNA load. Moreover, we found several differentially methylated regions associated with pathogen loads, in particular differential methylation at transposons and hypomethylation in the promoter of a gene involved in stomatal closure, likely induced by pathogens. Our study provides first insights into the defense mechanisms of Thlaspi arvense, a rising crop and model species, and demonstrates that non-target whole-genome sequencing reads, usually discarded, can be leveraged to estimate intensities of plant biotic interactions. With rapidly increasing numbers of large sequencing datasets worldwide, this approach should have broad application in fundamental and applied research.