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Covariation in superoxide, sperm telomere length and sperm velocity in a polymorphic reptile

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Abstract

Telomeres are DNA-protein caps at the ends of chromosomes that have been shown to be associated with male fertility may be heritable, reflect environmental influences and predict life span in some taxa. If heritable, paternal telomere length would be transmitted via sperm in the form of sperm telomere length (STL). We, therefore, investigated STL, sperm number and velocity in the Australian-painted dragon lizard, Ctenophorus pictus, an agamid lizard with distinct male colour morphs and related reproductive tactics. We measured telomere length in the sperm and blood as well as superoxide levels, as a measure for the potential for oxidative stress and ejaculate quality. We also noted a male’s head colour (red, orange, yellow or blue) and whether or not they had a yellow gular bib. Previous research has reported that yellow males outcompete red males in sperm competition; we found that yellow males had significantly shorter STL than red males. Males with bibs had greater STL than did males without bibs. Superoxide levels measured in the blood were negatively correlated with STL. Whole blood TL and body length were weakly but positively correlated with STL. Superoxide measurements were negatively correlated with progressive sperm motility and straight line sperm velocity across all males. The ejaculates of males with bibs had lower sperm counts and velocity than males without bibs. Our research adds to the growing research that indicates the importance of considering both somatic and gametic telomeres when assessing the interaction between telomere dynamics, life history and reproductive strategies.

Significance statement

Telomeres are DNA-protein caps at the ends of chromosomes that reflect environmental stress may be heritable and epigenetically modified, may predict life span in some taxa and may influence the probability of paternity in sperm competition. Ours is one of the first studies to examine correlates of sperm telomere length in a non-mammalian, polymorphic species, but much more remains to be done. Telomere research in non-model species has focused on survival consequences of variation in telomere traits with less attention paid to the fact that sperm (and egg) telomere biology can link life history traits directly to reproductive physiology. We chose to investigate sperm velocity and sperm telomere length (STL) in the painted dragon lizard, Ctenophorus pictus, an agamid lizard with distinct male morphs and associated reproductive tactics. We also observed morph-specific differences in ejaculate quality and STL; in particular, males with yellow bibs had longer STL but poorer ejaculate quality metrics (e.g., number of sperm, velocity and proportion of progressively motile sperm) than males without the throat patch. The differences in STL between the morphs and the negative relationship between sperm velocity and STL, along with previous work on this species, suggest that telomere length and dynamics may be linked with the reproductive tactics of colour morphs within this species.

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Data availability

All data generated or analysed during this study are included in this published article (and its supplementary information files).

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Acknowledgements

We thank Chalene Bezzina, Joanna Sudyka, Mathieu Giraudeau and Adele Haythornthwaite for husbandry and logistical support. We also thank Emily Uhrig, the editors and four anonymous reviewers for their sagacious comments and edits, all of which helped us to improve this manuscript.

Funding

This material is based in part upon work supported by the National Science Foundation (DBI-1308394 to CRF), University of Wollongong, University of Sydney, and the Australian Research Council (to MO).

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Authors and Affiliations

  1. School Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW, 2522, Australia

    Christopher R Friesen, Mark Wilson & Mats Olsson

  2. Illawarra Health and Medical Research Institute (IHMRI), University of Wollongong, Wollongong, NSW, 2522, Australia

    Christopher R Friesen & Mark Wilson

  3. School of Life and Environmental Sciences, University of Sydney, Heydon-Laurence Building (A08), Camperdown, NSW, 2006, Australia

    Nicky Rollings, Camilla M Whittington & Richard Shine

  4. Department of Biological Sciences, Macquarie University, Sydney, NSW, 2109, Australia

    Richard Shine

  5. Department of Biological & Environmental Sciences, University of Gothenburg, Gothenburg, Sweden

    Mats Olsson

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  1. Christopher R Friesen
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  3. Mark Wilson
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by CRF, MW, NR, CMW and MO. The first draft of the manuscript was written by NR and CRF, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Christopher R Friesen.

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The authors declare that they have no conflict of interest.

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All applicable international, national, and institutional guidelines for the use of animals were followed. Animals were collected under a permit issued by NSW National Parks and Wildlife Service (SL100352), and experiments were conducted in accordance with the University of Sydney ethics approval (AEC-2013/6050).

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Communicated by S. Joy Downes

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Friesen, C.R., Rollings, N., Wilson, M. et al. Covariation in superoxide, sperm telomere length and sperm velocity in a polymorphic reptile. Behav Ecol Sociobiol 74, 74 (2020). https://doi.org/10.1007/s00265-020-02855-8

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