The Science of Nature

, 104:81 | Cite as

Skin lipids of the striped plateau lizard (Sceloporus virgatus) correlate with female receptivity and reproductive quality alongside visual ornaments

  • Jay K. Goldberg
  • Alisa K. Wallace
  • Stacey L. Weiss
Original Paper

Abstract

Sex pheromones can perform a variety of functions ranging from revealing the location of suitable mates to being honest signals of mate quality, and they are used in the mate selection process by many species of reptile. In this study, we determined whether the skin lipids of female striped plateau lizards (Sceloporus virgatus) can predict the reproductive quality of females, thereby having the potential to serve as pheromones. Using gas chromatography/mass spectrometry, we identified 17 compounds present in skin lipids of female lizards. Using principal component analysis to compare the skin lipid profile of receptive and non-receptive females, we determined that an uncharacterized compound may allow for chemical identification of receptive mates. We also compared extracted principal components to measures of female fitness and reproductive qualities and found that the level of two 18 carbon fatty acids present in a female’s skin lipids may indicate her clutch size. Finally, we compared the information content of the skin lipids to that of female-specific color ornaments to assess whether chemical and visual cues transmit different information or not. We found that the chroma of a female’s orange throat patch is also related to her clutch size, suggesting that chemical signals may reinforce the information communicated by visual ornamentation in this species which would support the “backup signals” hypothesis for multiple signals.

Keywords

Chemical cues Lizards Multimodal communication Pheromones Reptilian Skin lipids 

Notes

Acknowledgements

We thank Eric Scharrer and John Hanson for their help with chemical analysis, James Bernhard for statistical help, and Mark Martin for helpful comments on an early draft of the manuscript. We also thank all the staff and volunteers at the Southwestern Research Station.

Compliance with Ethical Standards

Ethical approval

This work was conducted under Arizona Game and Fish scientific collecting permit SP603461 and with University of Puget Sound IACUC approval (F0708-01). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

References

  1. Ahern DG, Downing DT (1974) Skin lipids of the Florida indigo snake. Lipids 9:8–14. https://doi.org/10.1007/BF02533208 CrossRefPubMedGoogle Scholar
  2. Alberts AC (1990) Chemical properties of femoral gland secretions in the desert iguana Dipsosaurus dorsalis. J Chem Ecol 16:13–25. https://doi.org/10.1007/BF01021264
  3. Barbosa D, Font E, Desfilis E, Carretero MA (2006) Chemically mediated species recognition in closely related Podarcis wall lizards. J Chem Ecol 32:1587–1598. https://doi.org/10.1007/s10886-006-9072-5 CrossRefPubMedGoogle Scholar
  4. Carazo P, Font E, Desfilis E (2007) Chemosensory assessment of rival competitive ability and scent-mark function in a lizard, Podarcis hispanica. Anim Behav 74:895–902. https://doi.org/10.1016/j.anbehav.2007.02.011
  5. Chaine AS, Lyon BE (2008) Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–462. https://doi.org/10.1126/science.1149167 CrossRefPubMedGoogle Scholar
  6. Chin JSR, Ellis SR, Pham HT, Blanksby SJ, Mori K, Koh QL, Etges WJ, Yew JY (2014) Sex-specific triacylglycerides are widely conserved in Drosophila and mediate mating behavior. ELife 3:e01751. https://doi.org/10.7554/eLife.01751
  7. Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. PNAS 100:10341–10346. https://doi.org/10.1073/pnas.1834281100
  8. Elkin RG (2007) Reducing shell egg cholesterol content. II. Review of approaches utilizing non-nutritive dietary factors or pharmacological agents and an examination of emerging strategies. Worlds Poult Sci J 63:5–32. https://doi.org/10.1017/S0043933907001249 CrossRefGoogle Scholar
  9. Font E, Barbosa D, Sampedro C, Carazo P (2012) Social behavior, chemical communication, and adult neurogenesis: studies of scent mark function in Podarcis wall lizards. Gen Comp Endocr 177:9–17. https://doi.org/10.1016/j.ygcen.2012.02.015 CrossRefPubMedGoogle Scholar
  10. Fritzche AK, Weiss SL (2012) Effect of signaler body size on the response of male striped plateau lizards (Sceloporus virgatus) to conspecific chemical cues. J Herp 46(1):79–84. https://doi.org/10.1670/10-166
  11. Gabriot M, Castilla AM, López P, Mártin J (2010) Differences in chemical signals may explain species recognition between an island lizard, Podarcis atrata, and related mainland lizards, P. hispanica. Biochem Syst Ecol 38:521–528. https://doi.org/10.1016/j.bse.2010.05.008
  12. Hews DK, Date P, Hara E, Castellano MJ (2011) Field presentation of male secretions alters social display in Sceloporus virgatus but not S. undulatus lizards. Behav Ecol Sociobiol 65:1403–1410. https://doi.org/10.1007/s00265-011-1150-1
  13. Houck LD (2009) Pheromone communication in amphibians and reptiles. Annu Rev Physiol 75:161–176. https://doi.org/10.1146/annurev.physiol.010908.163134 CrossRefGoogle Scholar
  14. Ichihara K, Fukubayashi Y (2010) Preparation of fatty acid methyl esters for gas-liquid chromatography. J Lipid Res 51:635–640. https://doi.org/10.1111/j.1469-185X.2007.00009.x CrossRefPubMedPubMedCentralGoogle Scholar
  15. Johanssen BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289CrossRefGoogle Scholar
  16. Johnstone RA (1996) Multiple displays in animal communication: ‘backup signals’ and ‘multiple messages’. Philos Trans R Soc Lond Ser B Biol Sci 351:329–338. https://doi.org/10.1098/rstb.1996.0026 CrossRefGoogle Scholar
  17. Jones T, Fales H, Mulata Y, Yeh H, Pannell L, Mason RT (1991) New ketodienes from the integumental lipids of the guam brown tree snake, Boiga irregularis. J Nat Prod 54:233–240. https://doi.org/10.1021/np50073a024
  18. LeMaster MP, Mason RT (2002) Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. J Chem Ecol 28:1269–1285. https://doi.org/10.1023/A:1016294003641 CrossRefPubMedGoogle Scholar
  19. Mártin J, Civantos E, Amo L, López P (2007) Chemical ornaments of male lizards Psammodromus algirus may reveal their parasite load and health state to females. Behav Ecol Sociobiol 62:173–179. https://doi.org/10.1007/s00265-007-0451-x
  20. Mártin J, López P (2008) Female sensory bias may allow honest chemical signaling by male Iberian rock lizards. Behav Ecol Sociobiol 62:1927–1934. https://doi.org/10.1007/s00265-008-0624-2 CrossRefGoogle Scholar
  21. Mártin J, López P (2010) Condition-dependent pheromone signaling by male rock lizards: more oily scents are more attractive. Chem Senses 35(4):253–262. https://doi.org/10.1093/chemse/bjq009 CrossRefPubMedGoogle Scholar
  22. Mártin J, Ortega J, López P (2013) Lipophilic compounds in femoral secretions of male collared lizards, Crotaphytus bicinctores (Iguania, Crotaphytidae). Biochem Syst Ecol 47:5–10. https://doi.org/10.1016/j.bse.2012.09.025
  23. Martins EP, Ord TJ, Slaven J, Wright JL, Housworth EA (2006) Individual, sexual, seasonal, and temporal variation in the amount of sagebrush lizard scent marks. J Chem Ecol 32:881–893CrossRefPubMedGoogle Scholar
  24. Mason RT, Gutzke WHN (1990) Sex recognition in the leopard gecko Eublepharis macularius (Sauria: Gekkonidae) possible mediation by skin-derivied semiochemicals. J Chem Ecol 16:27–36Google Scholar
  25. Mason RT, Fales HM, Jones TH, Pannell LK, Chinn JC, Crews D (1989) Sex pheromones in snakes. Science 245:290–292CrossRefPubMedGoogle Scholar
  26. Meinke MC, Friedrich A, Tscherch K, Haag SF, Darvin ME, Vollert H, Groth N, LadeMann J, Rohn S (2013) Influence of dietary carotenoids on radical scavenging capacity of the skin and skin lipids. Eur J Pharm Biopharm 84:365–373CrossRefPubMedGoogle Scholar
  27. Moore FR, Shuker DM, Dougherty L (2016) Stress and sexual signalling: a systematic review and meta analysis. Behav Ecol 27:363–371. https://doi.org/10.1093/beheco/arv195 CrossRefGoogle Scholar
  28. Penn D, Potts WK (1998) Chemical signals and parasite-mediated sexual selection. TREE 13:391–396. https://doi.org/10.1016/S0169-5347(98)01473-6 PubMedGoogle Scholar
  29. Piironen V, Lindsay DG, Miettinen TA, Toivo J, Lampi A (2000) Plant sterols:biosynthesis, biological function and their importance to human nutrition. J Sci Food Agr 80:939–996CrossRefGoogle Scholar
  30. R Core Team (2012) R: language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  31. Roberts JB, Lillywhite HB (1980) Lipid barrier to water exchange in reptile epidermis. Science 207:1077–1079. https://doi.org/10.1126/science.207.4435.1077 CrossRefPubMedGoogle Scholar
  32. Uhrig EJ, Lutterschmidt DI, Mason RT, LeMaster MP (2012) Pheromonal mediation of intraseasonal declines in the attractivity of female red-sided garter snakes, Thamnophis sirtalis parietalis. J Chem Ecol 38:71–80. https://doi.org/10.1007/s10886-011-0054-x
  33. Weiss SL (2001) The effect of reproduction on food intake of a sit-and-wait foraging lizards, Sceloporus virgatus. Herpetologica 57:138–146Google Scholar
  34. Weiss SL (2002) Reproductive signals of female lizards: pattern of trait expression and male response. Ethology 108: 793–813Google Scholar
  35. Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol 17:726–732. https://doi.org/10.1093/beheco/arl001
  36. Weiss SL, Foerster K, Hudon J (2012) Pteridine, not carotenoid, pigments underlie the female-specific orange ornament of striped plateau lizards (Sceloporus virgatus). Comp Biochem Phys B 161:117–123. https://doi.org/10.1016/j.cbpb.2011.10.004 CrossRefGoogle Scholar
  37. Weiss SL, Kennedy EA, Bernhard JA (2009) Female-specific ornamentation predicts offspring quality in the striped plateau lizard, Sceloporus virgatus. Behav Ecol 20:1063–1071. https://doi.org/10.1093/beheco/arp098
  38. Weldon PJ, Flachsbarth B, Schulz S (2008) Natural products from the integument of nonavian reptiles. Nat Prod Rep 25:738–756. https://doi.org/10.1039/B509854H CrossRefPubMedGoogle Scholar
  39. Whittaker DJ, Soini HA, Atwell JW, Hollars C, Novotny MV, Ketterson ED (2010) Songbird chemosignals: volatile compounds in preen gland secretions vary among individuals, sexes, and populations. Behav Ecol 21:608–614. https://doi.org/10.1093/beheco/arq033 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Wiens JJ (1999) Phylogenetic evidence for multiple losses of a sexually selected character in phrynosomatid lizards. Proc R Soc Lond B Biol Sci 266:1529–1535. https://doi.org/10.1098/rspb.1999.0811 CrossRefGoogle Scholar
  41. Wyatt TD (2014) Pheromones and Animal Behavior. 2nd edition. Cambridge University PressGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Jay K. Goldberg
    • 1
    • 2
  • Alisa K. Wallace
    • 1
  • Stacey L. Weiss
    • 1
  1. 1.Department of BiologyUniversity of Puget SoundTacomaUSA
  2. 2.Department of BiologyIndiana UniversityBloomingtonUSA

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