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Research Article

Physiological responses to gravity in an insect

View ORCID ProfileJon F. Harrison, View ORCID ProfileKhaled Adjerid, Anelia Kassi, C. Jaco Klok, John M. VandenBrooks, Meghan E. Duell, View ORCID ProfileJacob B. Campbell, Stav Talal, Christopher D. Abdo, View ORCID ProfileKamel Fezzaa, Hodjat Pendar, and View ORCID ProfileJohn J. Socha
PNAS January 28, 2020 117 (4) 2180-2186; first published January 13, 2020 https://doi.org/10.1073/pnas.1915424117
Jon F. Harrison
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287-4501;
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  • ORCID record for Jon F. Harrison
  • For correspondence: j.harrison@asu.edu
Khaled Adjerid
bDepartment of Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA 24061;
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Anelia Kassi
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287-4501;
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C. Jaco Klok
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287-4501;
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John M. VandenBrooks
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287-4501;
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Meghan E. Duell
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287-4501;
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Jacob B. Campbell
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287-4501;
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  • ORCID record for Jacob B. Campbell
Stav Talal
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287-4501;
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Christopher D. Abdo
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287-4501;
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Kamel Fezzaa
cX-ray Science Division, Argonne National Laboratory, Lemont, IL 60561
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Hodjat Pendar
bDepartment of Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA 24061;
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John J. Socha
bDepartment of Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA 24061;
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  1. Edited by David L. Denlinger, The Ohio State University, Columbus, OH, and approved December 9, 2019 (received for review September 8, 2019)

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Significance

While it has long been known that vertebrates rely on compensatory responses to gravity with changing body orientation, this topic has not been previously studied in invertebrates. Here, we use synchrotron X-ray imaging and radio-tracing to demonstrate that body orientation has dramatic effects on hemolymph and air distribution in grasshoppers, and that grasshoppers exhibit similar physiological responses to gravity as vertebrates. Our findings suggest that gravity-driven cardiovascular responses may be ancient and widely shared among animals, opening the door for invertebrates as model systems for investigation of cellular and systemic mechanisms of gravity responses. Furthermore, future physiological studies of arthropods should control for body position.

Abstract

Gravity is one of the most ubiquitous environmental effects on living systems: Cellular and organismal responses to gravity are of central importance to understanding the physiological function of organisms, especially eukaryotes. Gravity has been demonstrated to have strong effects on the closed cardiovascular systems of terrestrial vertebrates, with rapidly responding neural reflexes ensuring proper blood flow despite changes in posture. Invertebrates possess open circulatory systems, which could provide fewer mechanisms to restrict gravity effects on blood flow, suggesting that these species also experience effects of gravity on blood pressure and distribution. However, whether gravity affects the open circulatory systems of invertebrates is unknown, partly due to technical measurement issues associated with small body size. Here we used X-ray imaging, radio-tracing of hemolymph, and micropressure measurements in the American grasshopper, Schistocerca americana, to assess responses to body orientation. Our results show that during changes in body orientation, gravity causes large changes in blood and air distribution, and that body position affects ventilation rate. Remarkably, we also found that insects show similar heart rate responses to body position as vertebrates, and contrasting with the classic understanding of open circulatory systems, have flexible valving systems between thorax and abdomen that can separate pressures. Gravitational effects on invertebrate cardiovascular and respiratory systems are likely to be widely distributed among invertebrates and to have broad influence on morphological and physiological evolution.

  • gravity
  • invertebrate
  • insect
  • cardiovascular system
  • respiratory system

Footnotes

  • ↵1To whom correspondence may be addressed. Email: j.harrison{at}asu.edu.
  • ↵2Present address: Sable Systems International, North Las Vegas, NV 89032.

  • ↵3Present address: Department of Physiology, Midwestern University, Glendale, AZ 85308.

  • Author contributions: J.F.H., K.A., and J.J.S. designed research; J.F.H., K.A., A.K., C.J.K., J.M.V., M.E.D., J.B.C., S.T., C.D.A., and J.J.S. performed research; K.F. contributed new reagents/analytic tools; J.F.H., K.A., A.K., C.J.K., J.M.V., M.E.D., J.B.C., S.T., H.P., and J.J.S. analyzed data; and J.F.H., K.A., A.K., S.T., and J.J.S. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1915424117/-/DCSupplemental.

Published under the PNAS license.

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Physiological responses to gravity in an insect
Jon F. Harrison, Khaled Adjerid, Anelia Kassi, C. Jaco Klok, John M. VandenBrooks, Meghan E. Duell, Jacob B. Campbell, Stav Talal, Christopher D. Abdo, Kamel Fezzaa, Hodjat Pendar, John J. Socha
Proceedings of the National Academy of Sciences Jan 2020, 117 (4) 2180-2186; DOI: 10.1073/pnas.1915424117

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Physiological responses to gravity in an insect
Jon F. Harrison, Khaled Adjerid, Anelia Kassi, C. Jaco Klok, John M. VandenBrooks, Meghan E. Duell, Jacob B. Campbell, Stav Talal, Christopher D. Abdo, Kamel Fezzaa, Hodjat Pendar, John J. Socha
Proceedings of the National Academy of Sciences Jan 2020, 117 (4) 2180-2186; DOI: 10.1073/pnas.1915424117
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