A thermogenic secondary sexual character in male sea lamprey

Yu Wen Chung-Davidson, M. Cody Priess, Chu Yin Yeh, Cory O. Brant, Nicholas S. Johnson, Ke Li, Kaben G. Nanlohy, Mara B. Bryan, Charles Brown, Jongeun Choi, Weiming Li

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Secondary sexual characters in animals are exaggerated ornaments or weapons for intrasexual competition. Unexpectedly, we found that a male secondary sexual character in sea lamprey (Petromyzon marinus) is a thermogenic adipose tissue that instantly increases its heat production during sexual encounters. This secondary sexual character, developed in front of the anterior dorsal fin of mature males, is a swollen dorsal ridge known as the 'rope' tissue. It contains nerve bundles, multivacuolar adipocytes and interstitial cells packed with small lipid droplets and mitochondria with dense and highly organized cristae. The fatty acid composition of the rope tissue is rich in unsaturated fatty acids. The cytochrome c oxidase activity is high but the ATP concentration is very low in the mitochondria of the rope tissue compared with those of the gill and muscle tissues. The rope tissue temperature immediately rose up to 0.3°C when the male encountered a conspecific. Mature males generated more heat in the rope and muscle tissues when presented with a mature female than when presented with a male (paired t-test, P>0.05). On average, the rope generated 0.027±0.013 W cm-3 more heat than the muscle in 10 min. Transcriptome analyses revealed that genes involved in fat cell differentiation are upregulated whereas those involved in oxidative- phosphorylation-coupled ATP synthesis are downregulated in the rope tissue compared with the gill and muscle tissues. Sexually mature male sea lamprey possess the only known thermogenic secondary sexual character that shows differential heat generation toward individual conspecifics.

Original languageEnglish (US)
Pages (from-to)2702-2712
Number of pages11
JournalJournal of Experimental Biology
Volume216
Issue number14
DOIs
StatePublished - Jul 1 2013
Externally publishedYes

Fingerprint

Petromyzon
Petromyzon marinus
ropes
Muscles
muscle tissues
Hot Temperature
muscle
Adipocytes
adipocytes
heat
Mitochondria
Adenosine Triphosphate
gills
mitochondrion
mitochondria
Weapons
Thermogenesis
Oxidative Phosphorylation
Gene Expression Profiling
Electron Transport Complex IV

Keywords

  • Electron transport chain
  • Petromyzon marinus
  • Sea lamprey
  • Sexual character
  • Thermogenic
  • Uncoupling protein

ASJC Scopus subject areas

  • Animal Science and Zoology
  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Physiology
  • Insect Science
  • Aquatic Science

Cite this

Chung-Davidson, Y. W., Priess, M. C., Yeh, C. Y., Brant, C. O., Johnson, N. S., Li, K., ... Li, W. (2013). A thermogenic secondary sexual character in male sea lamprey. Journal of Experimental Biology, 216(14), 2702-2712. https://doi.org/10.1242/jeb.085746

A thermogenic secondary sexual character in male sea lamprey. / Chung-Davidson, Yu Wen; Priess, M. Cody; Yeh, Chu Yin; Brant, Cory O.; Johnson, Nicholas S.; Li, Ke; Nanlohy, Kaben G.; Bryan, Mara B.; Brown, Charles; Choi, Jongeun; Li, Weiming.

In: Journal of Experimental Biology, Vol. 216, No. 14, 01.07.2013, p. 2702-2712.

Research output: Contribution to journalArticle

Chung-Davidson, YW, Priess, MC, Yeh, CY, Brant, CO, Johnson, NS, Li, K, Nanlohy, KG, Bryan, MB, Brown, C, Choi, J & Li, W 2013, 'A thermogenic secondary sexual character in male sea lamprey', Journal of Experimental Biology, vol. 216, no. 14, pp. 2702-2712. https://doi.org/10.1242/jeb.085746
Chung-Davidson YW, Priess MC, Yeh CY, Brant CO, Johnson NS, Li K et al. A thermogenic secondary sexual character in male sea lamprey. Journal of Experimental Biology. 2013 Jul 1;216(14):2702-2712. https://doi.org/10.1242/jeb.085746
Chung-Davidson, Yu Wen ; Priess, M. Cody ; Yeh, Chu Yin ; Brant, Cory O. ; Johnson, Nicholas S. ; Li, Ke ; Nanlohy, Kaben G. ; Bryan, Mara B. ; Brown, Charles ; Choi, Jongeun ; Li, Weiming. / A thermogenic secondary sexual character in male sea lamprey. In: Journal of Experimental Biology. 2013 ; Vol. 216, No. 14. pp. 2702-2712.
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