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.
↵* Present address: USGS, Great Lakes Science Center, Hammond Bay Biological Station, 11188 Ray Road, Millersburg, MI 49759, USA
↵† Present address: Energy Biosciences Institute, University of California, Berkeley, 130 Calvin Laboratory, MC 5230, Berkeley, CA 94720, USA
Y.-W.C.-D. and W.L. conceived the hypotheses, designed the study and prepared the manuscript. Y.-W.C.-D. performed all the experiments and data analyses. N.S.J. collected rope tissue samples for histology and electron microscopy. K.L. performed the GC-MS. C.-Y.Y. helped with the mitochondrial cytochrome c oxidase and ATP assays, temperature measurements and behavioral recordings. C.O.B. helped with the temperature measurements and behavioral recordings. C.P. and J.C. provided assistance and the model for temperature measurements. K.G.N. and C.T.B. provided the computational assistance for GO analyses. M.B.B. performed the AD treatment on immature male sea lamprey. All authors discussed the results and commented on the manuscript.
Supplementary material available online at http://jeb.biologists.org/cgi/content/full/216/14/2702/DC1
No competing interests declared.
This study is supported by grants from the Great Lakes Fishery Commission, the US National Institute of General Medical Sciences (grant number 5R24GM83982) and the US National Science Foundation (grant number IOB 0517491) to W.L. Deposited in PMC for release after 12 months.
- © 2013. Published by The Company of Biologists Ltd