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Relationship between gene expression networks and muscle contractile physiology differences in Anolis lizards

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Abstract

Muscles facilitate most animal behavior, from eating to fleeing. However, to generate the variation in behavior necessary for survival, different muscles must perform differently; for instance, sprinting requires multiple rapid muscle contractions, whereas biting may require fewer contractions but greater force. Here, we use a transcriptomic approach to identify genes associated with variation in muscle contractile physiology among different muscles from the same individual. We measured differential gene expression between a leg and jaw muscle of Anolis lizards known to differ in muscle contractile physiology and performance. For each individual, one muscle was used to measure muscle contractile physiology, including contractile velocity (Vmax and V40), specific tension, power ratio, and twitch time, whereas the contralateral muscle was used to extract RNA for transcriptomic sequencing. Using the transcriptomic data, we found clear clustering of muscle type. Expression of genes clustered in gene ontology (GO) terms related to muscle contraction and extracellular matrix was, on average, negatively correlated with Vmax and slower twitch times but positively correlated to power ratio and V40. Conversely, genes related to the GO terms related to aerobic respiration were downregulated in muscles with higher power ratio and V40, and over-expressed as twitch time decreased. Determining the molecular mechanisms that underlie variation in muscle contractile physiology can begin to explain how organisms are able to optimize behavior under variable conditions. Future studies pursuing the effects of differential gene expression across muscle types in different environments might inform researchers about how differences develop across species, populations, and individuals varying in ecological history.

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Availability of data and material

Physiology data have been made available in the tables found in the online resources this manuscript. RNA-seq data is available through NCBI’s GEO.

Code availability

Code is available at www.github.com/alliebl/anolis_j_v_l.

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Acknowledgements

We would like to thank James Stroud for animal collection assistance in Florida and Rachel Drown for animal care assistance at USD.

Funding

This work was supported by the National Science Foundation (IOS 1354620 to T.J.R.); the University of South Dakota Arts and Sciences (to A.L.L. and C.V.A.); the University of South Dakota Center for Academic and Global Engagement (to L.B.S.); and the University of South Dakota Sanford School of Medicine Scholarship Pathways Program (to L.B.S.).

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Author notes

  1. Luke B. Smith and Christopher V. Anderson contributed equally to this manuscript.

Authors and Affiliations

  1. Department of Biology, University of South Dakota, Vermillion, SD, USA

    Luke B. Smith, Christopher V. Anderson, Miyuraj H. Hikkaduwa Withangage, Andrew Koch & Andrea L. Liebl

  2. Sanford School of Medicine, University of South Dakota, Vermillion, SD, USA

    Luke B. Smith

  3. College of Dentistry and Dental Clinics, University of Iowa, Iowa City, IA, USA

    Miyuraj H. Hikkaduwa Withangage

  4. Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA

    Thomas J. Roberts

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Contributions

The study was conceived and designed by ALL, CVA, LBS, and TJR. Experiments were completed by CVA, LBS, and ALL. Data were analyzed by LBS, ALL, AK, and MHHW. The first draft of the manuscript was written by LBS, ALL, and CVA, and all authors commented on subsequent versions of the manuscript.

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Correspondence to Andrea L. Liebl.

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No conflicts of interests or competing interests are declared.

Ethics approval

All live animal research methods were approved by the University of South Dakota’s IACUC committee (AUP 16–35) and research in Costa Rica was performed under research (SINAC-SE-CUSBSE-PI-R-0126–2017), collection (189–2017), and export (III-DGVS-2018) permits to C.V.A.

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Communicated by H.V. Carey.

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Smith, L.B., Anderson, C.V., Withangage, M.H.H. et al. Relationship between gene expression networks and muscle contractile physiology differences in Anolis lizards. J Comp Physiol B 192, 489–499 (2022). https://doi.org/10.1007/s00360-022-01441-w

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  • DOI: https://doi.org/10.1007/s00360-022-01441-w

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