, Volume 51, Issue 1, pp 97–105 | Cite as

Sex-specific asymmetry within the cloacal microbiota of the striped plateau lizard, Sceloporus virgatus

  • Mark O. MartinEmail author
  • Frances R. Gilman
  • Stacey L. Weiss


The structure and diversity of microbial communities in wild vertebrate populations remain poorly understood, but are expected to have important consequences for individual survival and reproductive success. For instance, recent work has demonstrated that cloacal microbe assemblages of wild birds are related to the phenotypic quality of the host. To contribute to this field of study, we examined the composition and diversity of the cloacal microbiota of free-ranging striped plateau lizards, Sceloporus virgatus, using 16s rRNA-based culture independent techniques. Our dataset, generated from cloacal swabs of six males and six females, and based on twenty five 16s rRNA clones from each sample, revealed (i) low overall microbial diversity, (ii) a striking sex asymmetry in microbial community composition with males displaying cloacal microbiota more typical of gastrointestinal residents found in other organisms, while females display only gammaproteobacterial phylotypes, (iii) a significant sex difference in microbial community structure, with females having significantly lower microbial diversity and richness than do males, and (iv) that the diversity of the female microbial community is negatively correlated to her ectoparasitic mite load. It is not yet clear if the female-specific paucity of cloacal microbial diversity is due to host function or microbe-microbe interactions, or whether the relationship to female mite load is causal, however these findings are expected to have relevance to the species’ life history and ecology. Although the diversity of microbiota from humans, mice, birds, zebrafish, and invertebrates is widely investigated, this is one of only a few reports in the literature describing the cloacal microbiota of a wild vertebrate, and is perhaps the first report for wild reptiles that utilizes culture-independent techniques.


Microbiota Lizard Culture-independent Sex asymmetry Wild vertebrates 



Generous support for this research was provided by start up funds from the University of Puget Sound (M.O.M. and S.L.W.), the University Enrichment Committee of the University of Puget Sound (to M.O.M.), the NASA Motivating Undergraduates in Science and Technology program (MUST) (to F.R.G), and the Murdock Charitable Trust (to S.L.W.). Support was received from Rachel Hood and Michal Morrison at the University of Puget Sound and from the staff of the American Museum of Natural History’s Southwestern Research Station. Patient advice regarding plotting of phylotype data was courtesy of Brian Jacobs. Finally, we thank Min Young Chun, Matt Dubin, and Sandy Olenic for their help collecting lizards.

Supplementary material

13199_2010_78_MOESM1_ESM.pdf (655 kb)
ESM 1 (PDF 654 kb)


  1. Abell AJ (1998) Reproductive and post-reproductive hormone levels in the lizard Sceloporous virgatus. Acta Zool Mex 74:43–57Google Scholar
  2. Allen HK, Cloud-Hansen KA, Wolinski JM, Guan C, Greene S, Lu S, Boeyink M, Broderick NA, Raffa KF, Handelsman J (2009) Resident microbiota of the gypsy moth midgut harbors antibiotic resistance determinants. DNA Cell Biol. doi: 10.1089/dna.2008.0812 PubMedGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Molec Biol 215:403–410PubMedGoogle Scholar
  4. Angenent LT, Kelley ST, St. Amand A, Pace NR, Hernandez MT (2005) Molecular identification of potential pathogens in water and air of a hospital therapy pool. Proc Natl Acad Sci USA 102(13):4860–4865CrossRefPubMedGoogle Scholar
  5. Bates JM, Mittge E, Kuhlman J, Baden KN, Cheesman SE, Guillemin K (2006) Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297:374–386CrossRefPubMedGoogle Scholar
  6. Baumann P, Baumann L, Lau CY, Rouhbakhsh D, Moran NA, Clark MA (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Ann Rev Microbiol 49:55–94CrossRefGoogle Scholar
  7. Becker MH, Brucker RM, Scwantes CR, Harris RN, Minbiole KP (2009) The bacterially produced metabolite violacein is associated with survival of amphibians infected with a lethal fungus. Appl Environ Microbiol 75:6635–6638CrossRefPubMedGoogle Scholar
  8. Borlee BR, Geske GD, Robinson CJ, Robinson CJ, Blackwell HE, Handelsman J (2008) Quorum sensing signals in the microbial community of the cabbage white butterfly larval midgut. ISME J 2:1101–1111CrossRefPubMedGoogle Scholar
  9. Broderick NA, Raffa KF, Goodman RM, Handelsman J (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70:293–300CrossRefPubMedGoogle Scholar
  10. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science. doi: 10.1126/science.1177486 Google Scholar
  11. Espinosa-Aviles D, Salomon-Soto VM, Morales-Martinez S (2008) Hematology, blood chemistry, and bacteriology of the free ranging mexican beaded lizard (Heloderma horridum). J Zoo Wildl Med 39:21–27CrossRefPubMedGoogle Scholar
  12. Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105:17994–17999CrossRefPubMedGoogle Scholar
  13. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391CrossRefGoogle Scholar
  14. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387CrossRefPubMedGoogle Scholar
  15. Hooper LV, Bry L, Falk PG, Gordon JI (1998) Host-microbial symbiosis in the mammalian intestine: exploring an internal ecosystem. BioEssays 20:336–343CrossRefPubMedGoogle Scholar
  16. Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture independent studies on the emerging phylogenetics view of bacterial diversity. J Bacteriol 180:4765–4774PubMedGoogle Scholar
  17. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023CrossRefPubMedGoogle Scholar
  18. Ley RE, Hamady M, Lozupoine C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651CrossRefPubMedGoogle Scholar
  19. Little AEF, Robinson CJ, Peterson SB, Raffa KF, Handelsman J (2008) Rules of engagement: interspecies interactions that regulate microbial communities. Annu Rev Microbiol 62:375–401CrossRefPubMedGoogle Scholar
  20. Lombardo MP, Thorpe PA, Cichewicz R, Henshaw M, Millard C, Steen C, Zeller TK (1996) Communities of cloacal bacteria in tree swallow families. Condor 98:167–172CrossRefGoogle Scholar
  21. Lombardo MP, Thorpe PA, Power HW (1998) The beneficial sexually transmitted microbe hypothesis of avian copulation. Behav Ecol 10:333–350CrossRefGoogle Scholar
  22. Lucas FS, Heeb P (2005) Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit Parus caerulus nestlings. J Avian Biol 36:510–516CrossRefGoogle Scholar
  23. Ma R, Wu X, Jiang H, Pan J, Zhu J, Wang C (2008) Identification of cloaca bacteria from candidate releasing Chinese alligators. Zoo Res 29:253–259CrossRefGoogle Scholar
  24. Martel A, Pasmans F, Hellebuyck T, Haesebrouck F, Vandamme P (2008) Devrisea agamarum gen. nov., sp. nov., a novel actinobacterium associated with dermatitis and septicaemia in agamid lizards. Int J Syst Evol Microbiol 58:2206–2209CrossRefPubMedGoogle Scholar
  25. McFall-Ngai MJ, Henderson B, Ruby EG (eds) (2005) The influence of cooperative bacteria on animal host biology. Cambridge University Press, New YorkGoogle Scholar
  26. McFall-Ngai M (2008) Are biologists in ‘future shock’? Symbiosis integrates biology across domains. Nat Rev Microbiol 6:789–792CrossRefPubMedGoogle Scholar
  27. Meade GC (1997) Bacteria in the gastrointestinal tract of birds. In: Mackie RI, White BA, Isaacson RE (eds) Gastrointestinal microbiology. Chapman and Hall, New YorkGoogle Scholar
  28. Mills TK, Lombardo MP, Thorpe PA (1999) Microbial colonization of the cloacae of nestling tree swallows. The Auk 116:947–956Google Scholar
  29. Moreno J, Briones V, Merino S, Ballesteros C, Sanz JJ, Tomas G (2003) Beneficial effects of cloacal bacteria on growth and fledgling size in nestling pied flycatchers (Ficedula hypoleuca) in Spain. Auk 120:784–790CrossRefGoogle Scholar
  30. Peterson DA, McNulty NP, Guruge JL, Gordon JI (2007) IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2:328–339CrossRefPubMedGoogle Scholar
  31. Phillott AD, Paramenter CJ, Limpus CJ, Harrower KM (2002) Mycobiota as acute and chronic cloacal contaminants of female sea turtles. Austral J Zool 50:687–695CrossRefGoogle Scholar
  32. Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci USA 101:4596–4601CrossRefPubMedGoogle Scholar
  33. Relman DA (2008) ‘Til death do us part’: coming to terms with symbiotic relationships. Nat Rev Microbiol 6:721–724CrossRefPubMedGoogle Scholar
  34. Ruiz-Rodriguez M, Soler JJ, Lucas FS, Heeb P, Palacios MJ, Martin-Galvez D, de Neve L, Perez-Contreras T, Martinez JG, Soler M (2009) Bacterial diversity at the cloaca relates to an immune response in magpie Pica pica and to body condition of great spotted cuckoo Clamator glandarius nestlings. J Avian Biol 40:42–48CrossRefGoogle Scholar
  35. Scupham AJ, Patton TG, Bent E, Bayles DO (2008) Comparison of the cecal microbiota of domestic and wild turkeys. Microb Ecol 56:322–331CrossRefPubMedGoogle Scholar
  36. Shawkey MD, Mills KL, Dale C, Hill GE (2005) Microbial diversity of wild bird feathers revealed through culture-based and culture-independent techniques. Microb Ecol 50:40–47CrossRefPubMedGoogle Scholar
  37. Trauth SE, Cooper WE Jr, Vitt LJ, Perrill SA (1987) Cloacal anatomy of the broad-headed skink, Eumeces laticeps, with a description of the a female pheromonal gland. Herpetologica 43:458–466Google Scholar
  38. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810CrossRefPubMedGoogle Scholar
  39. Visick KL, Ruby EG (2006) Vibrio fischeri and its host: it takes two to tango. Curr Opin Microbiol 9:632–638CrossRefPubMedGoogle Scholar
  40. Weiss SL (2002) Reproductive signals of female lizards: pattern of trait expression and male response. Ethology 108:793–813CrossRefGoogle Scholar
  41. Weiss SL (2006) Female specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol. 17:726-732. doi: 10.1093/beheco/arl00 Google Scholar
  42. Weiss SL, Kennedy EA, Bernhard JA (2009) Female-specific ornamentation predicts offspring quality in the striped plateau lizard, Sceloporus virgatus. Behav Ecol 20:1063–1071CrossRefGoogle Scholar
  43. Williams PA, Mitchell W, Wilson GR, Weldon PJ (1990) Bacteria in the gular and paracloacal glands of the American alligator (Alligator mississippiensis; Reptilia, Crocodilia). Ltr Appl Microbiol 10:73–76CrossRefGoogle Scholar
  44. Wright SAI, Zumoff CH, Schneider L, Beer SV (2001) Pantoea agglomerans strain EH318 produces two antibiotics that inhibit Erwinia amylovora in vitro. App Environ Microbiol 67:284–292CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Mark O. Martin
    • 1
    Email author
  • Frances R. Gilman
    • 1
  • Stacey L. Weiss
    • 1
  1. 1.Biology DepartmentUniversity of Puget SoundTacomaUSA

Personalised recommendations