, Volume 22, Issue 10, pp 1461–1466 | Cite as

Endocrine disruption of sexual selection by an estrogenic herbicide in the mealworm beetle (Tenebrio molitor)

  • Malcolm L. McCallum
  • Makensey Matlock
  • Justin Treas
  • Barroq Safi
  • Wendy Sanson
  • Jamie L. McCallum


The role that endocrine disruption could play in sexual selection remains relatively untested, and although estrogens occur in insects, little information exists about their biological role in insect reproduction. Atrazine is a commonly applied herbicide that mimics estrogen in vertebrates. Tenebrio molitor were raised from egg to adult under a gradation of environmentally relevant atrazine exposures and a non-treated control. Atrazine was delivered in the drinking water ad libitum. Female T. molitor were provided with a choice between unrelated males raised under three levels of atrazine exposures. Female preference for males demonstrated a non-monotonic inverted U-shaped response to atrazine exposure. There was no significant difference between the control and the high exposure to atrazine. Excluding the control, female preference increased as exposure concentration increased. These results have important repercussions for nonlethal effects of endocrine disruption on populations, their capacity to interfere with sexual selection, and the role of estrogen in pheromone communication among insects.


Atrazine Endocrine disruption Sexual selection Estrogen Non-monotonic response 



We thank Ann Paterson for discussion of an early version of this manuscript and Beverly Burden for demonstrating how to sex pupae and beetles. Funding for this project was provided by Malcolm McCallum.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Andersson M, Iwasa Y (1996) Sexual selection. Trends Ecol Evol 11(2):53–58CrossRefGoogle Scholar
  2. August CJ (1971) The role of male and female pheromones in the mating behavior of Tenebrio molitor. J Insect Phys 17:739–751CrossRefGoogle Scholar
  3. Barth RH, Lester LJ (1973) Neuro-hormonal control of sexual behavior in insects. Annu Rev Entomol 18:445-472Google Scholar
  4. Beckage NE, Foreman RC, Palmatier CM, Tan FF (2002) Inhibition of the larval ecdysis and emergence behaviour of the parasitoid Cotesia congregate by methoprene. J Insect Physiol 48:725–732CrossRefGoogle Scholar
  5. Becker JB, Breedlove SM, Crews D, McCarthy MM (2002) Behavioral endocrinology. MIT Press, CambridgeGoogle Scholar
  6. Brown M, Sharp PA (1990) Human estrogen receptor forms multiple protein–DNA complexes. J Biol Chem 265(19):11238–11243Google Scholar
  7. Cheek AO, Bouwer TH, Carroll S, Manning S, McLachlan JA, Brouwer M (2001) Experimental evaluation of vitellogenin as a predictive biomarker of reproductive disruption. Environ Health Perspect 109(7):681–690CrossRefGoogle Scholar
  8. Coe TS, Hamilton PB, Hodgson D, Paull GC, Stevens JR, Sumner K, Tyler CR (2008) An environmental estrogen alters reproductive hierarchies, disrupting sexual selection in group-spawning fish. Environ Sci Technol 42:5020–5025CrossRefGoogle Scholar
  9. Contreras-Garduño J, Córdoba-Aguilar A, Lanz-Mendoza H, Cordero Rivera A (2009) Territorial behaviour and immunity are mediated by juvenile hormone: the physiological basis of honest signaling? Funct Ecol 23:157–163CrossRefGoogle Scholar
  10. Crews D, Willingham E, Skipper JK (2000) Endocrine disruptors: present issues, future directions. Q Rev Biol 75:243–260CrossRefGoogle Scholar
  11. De Loof A (2006) Ecdysteroids: the overlooked sex steroids of insects? Males: the black box. Insect Sci 13(5):325–338CrossRefGoogle Scholar
  12. Dewey SL (1986) Effects of the herbicide atrazine on aquatic insect community structure and emergence. Ecology 67(1):148–162CrossRefGoogle Scholar
  13. Drnevich JM, Papke RS, Rauser CL, Rutowski RL (2001) Material benefits from multiple mating in female mealworm beetles (Tenebrio molitor L.). J Insect Behav 14:215–230CrossRefGoogle Scholar
  14. Dussault EB, Balakrishnan VK, Solomon KR, Sibley PK (2008) Chronic toxicity of the synthetic hormone 17alpa-ethinylestradiol to Chironomus tentans and Hyalella azteca. Environ Toxicol Chem 27(12):2521–2529CrossRefGoogle Scholar
  15. Gonzalez G, Sorel G, Smith LC (2001) Testosterone and sexual signaling in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 50:557–562Google Scholar
  16. Gruessner B, Watzin MC (1996) Response of aquatic communities from a vermont stream to environmentally realistic atrazine exposure in laboratory microcosms. Environ Toxicol Chem 15(4):410–419CrossRefGoogle Scholar
  17. Happ GM (1969) Multiple sex pheromones of the mealworm beetle, Tenebrio molitor L. Nature 222:180–181CrossRefGoogle Scholar
  18. Hayes TB, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, Vonk A (2002) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine after low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476–5480CrossRefGoogle Scholar
  19. Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A (2003) Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ Health Persp 111:568–575CrossRefGoogle Scholar
  20. Hurd H, Parry G (1991) Metacestode-induced depression of the production, and responses to, sex pheromone in the intermediate host Tenebrio molitor. J Invert Pathol 58:82–87CrossRefGoogle Scholar
  21. Huybrechts R, De Loof A (1977) Induction of vitellogenin synthesis in male Sarcophaga bullata by ecdysterone. J Insect Physiol 23:1359–1362CrossRefGoogle Scholar
  22. Jašarević E, Sieli PT, Twellman EE, Welsh TH Jr, Schachtman TR, Roberts RM, Geary DC, Rosenfeld CS (2011) Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. Proc Natl Acad Sci 108:11715–11720CrossRefGoogle Scholar
  23. Jiang M, Hart GW (1997) A subpopulation of estrogen receptors are modified by O-linked N-acetylglucosamine. J Biol Chem 272(4):2421–2428CrossRefGoogle Scholar
  24. Jobling S, Casey D, Rodgers-Gray T, Oehlmann J, Schulte-Oehlmann U, Pawlowski S, Baunbeck T, Turner AP, Tyler CR (2004) Comparative responses of mollusks and fish to environmental estrogens and an estrogenic effluent. Aquat Toxicol 66:207–222CrossRefGoogle Scholar
  25. Keshan B, Ray AK (2000) Estradiol-17β in Bombyx mori: possible significance and its effect on silk production. J Insect Phys 46(6):1061–1068CrossRefGoogle Scholar
  26. Kivleniece I, Krams I, Daukšte J, Krama T, Rantala MJ (2010) Sexual attractiveness of immune-challenged male mealworm beetles suggests terminal investment in reproduction. Animal Behav 80:1015–1021CrossRefGoogle Scholar
  27. Krams I, Daukšte J, Kivleniece I, Krama T, Rantala MJ, Ramey G, Šauša (2011) Female choice reveals terminal investment in male mealworm beetles, Tenebrio molitor, after a repeated activation of the immune system. J Insect Sci 11:56–79CrossRefGoogle Scholar
  28. Lomolino MV, Creighton JC, Schnell JD, Certain DL (1995) Ecology and conservation of the endangered American burying beetle (Nicrophorus americanus). Conserv Biol 9(3):605–614CrossRefGoogle Scholar
  29. McGlothlin JW, Neudorf DLH, Casto JM, Nolan V Jr, Ketterson ED (2004) Elevated testosterone reduced choosiness in female dark-eyed juncos (Junco hyemalis): evidence for a hormonal constraint on sexual selection. Proc Royal Soc Lond B 271:1377–1384CrossRefGoogle Scholar
  30. Mechoulam R, Brueggemeier RW, Denlinger DL (2005) Estrogens in insects. Cell Mol Life Sci 40(9):942–944CrossRefGoogle Scholar
  31. Millam JR, Craig-Veit CB, Quaglino AE, Erichsen AL, Famula TR, Fry DM (2001) Posthatch oral estrogen exposure impairs adult reproductive performance of zebra finch in sex-specific manner. Horm Behav 40(4):542–549CrossRefGoogle Scholar
  32. Miota F, Siegfried BD, Scharf ME, Lydy MJ (1999) Atrazine inductioin of cytochrome P450 in Chironomus tentans larvae. Chemosphere 40(3):285–291CrossRefGoogle Scholar
  33. Miranda JE, de Bortoli SA, Takahashi R (2002) Development and silk production by silkworm larvae after topical application of methoprene. Sci Agricola 59:585–588CrossRefGoogle Scholar
  34. O’Connor JC, Chapin RE (2003) Critical evaluation of observed adverse effects of endocrine active substances on reproduction and development, the immune system, and the nervous system. Pure Appl Chem 75(11–12):2099–2123CrossRefGoogle Scholar
  35. Ouyang X, Xi G, Bu C, Wang H, Zhan G, Hong F (2009) Molecular cloning and expression of an estrogen receptor-related receptor gene in the ant Polyrhachis vicina (Hymenoptera: formicidae). Ann Entomol Soc Am 102(4):295–302CrossRefGoogle Scholar
  36. Picchi MS, Avolio L, Azzani L, Brombin O, Camerini G (2013) Fireflies and land use in an urban landscape: the case of Luciola italic L. (Coleoptera: Lampyridae) in the city of Turin. J Insect Conserv. doi: 10.1007/s10841-013-9562-z Google Scholar
  37. Pierce AM, Pierce HD, Borden JH, Oehlschlager AC (1986) Enhanced production of aggregation pheromones in four stored-product coleopterans feeding on methoprene-treated oats. Experientia 42:164–165CrossRefGoogle Scholar
  38. Porter WP, Jaeger JW, Carlson IH (1999) Endocrine, immune, and behavioral affects of aldicarb (carbamate), atrazine (triazine) and nitrate (fertilizer) mixtures at groundwater concentrations. Toxicol Ind Health 15:133–150CrossRefGoogle Scholar
  39. Postlethwait JH, Weiser K (1973) Vitellogenesis induced by juvenile hormone in the female sterile mutant apterous-four in Drosophila melanogaster. Nat New Biol 244:284–285CrossRefGoogle Scholar
  40. Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence? Proc R Soc Lond B 269:1681–1685CrossRefGoogle Scholar
  41. Rantala MJ, Vainikka A, Kortet R (2003a) The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompentence handicap principle. Proc R Soc Lond B 270:2257–2261CrossRefGoogle Scholar
  42. Rantala MJ, Kortet R, Kotiaho JS, Vainikka A, Suhonen J (2003b) Condition dependence of pheromones and immune function in the grain beetle Tenbrio molitor. Funct Ecol 17:534–540CrossRefGoogle Scholar
  43. Reddy GVP, Guerrero A (2004) Interactions of insect pheromones and plant semichemicals. Trends Plant Sci 9:253–261CrossRefGoogle Scholar
  44. Reeder AL, Ruiz MO, Pessier A, Brown LE, Levengood JM, Phillips CA, Wheeler MB, Warner RE, Beasley VR (2005) Intersexuality and the cricket frog decline: historic and geographic trends. Environ Health Perspect 113(3):261–265CrossRefGoogle Scholar
  45. Saaristo M, Craft JA, Lehtonen KK, Björk H, Lindström K (2009) Disruption of sexual selection in sand gobies (Pomatoschistus minutes) by 17α-ethinyl estradiol, an endocrine disruptor. Horm Behav 55:530–537CrossRefGoogle Scholar
  46. Sadd B, Holman L, Armitage H, Lock F, Marland R, Siva-Jothy MT (2005) Modulation of sexual signaling by immune challenged male mealworm beetles (Tenebrio molitor, L.): evidence for terminal investment and dishonesty. J Evol Biol 19:321–325CrossRefGoogle Scholar
  47. Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17(10):474–480CrossRefGoogle Scholar
  48. Shenoy K, Crowley PH (2010) Endocrine disruption of male mating signals: ecological and evolutionary implications. Funct Ecol 25:433–448CrossRefGoogle Scholar
  49. Su XH, Xi GS (2005) Immunocytochemical localization of estrogen receptor in the oogenesis of termites. Shi Yan Sheng Wu Xue Bao 38(6):545–549Google Scholar
  50. Su XH, Xing LX, Yin LF, Xi GS (2007) Immunocytochemical localization of estrogen receptor in the spermatogenesis of termites. Fen Zi Xi Bao Sheng Wu Xue Bao 40(2):173–178Google Scholar
  51. Tanaka Y, Honda H, Ohsawa K, Yamamoto I (1986) A sex attractant of the yellow mealworm, Tenebrio molitor L., and its role in the mating behavior. J Pesticide Sci 11:49–55CrossRefGoogle Scholar
  52. Toft G, Baatrup E (2001) Sexual characteristicsare altered by 4-tert-octylphenol and 17β-estradiol in the adult male guppy (Poecilia reticulata). Ecotoxicol Environ Saf 48:76–84CrossRefGoogle Scholar
  53. Trivers RL (2006) In: Campbell B-G (ed) Sexual selection and the descent of man: the Darwinian pivot. Transaction Publishers, Edison, pp 135–188Google Scholar
  54. Trumbo ST (1997) Juvenile hormone-mediated reproduction in burying beetles: from behavior to physiology. Arch Insect Biochem Phys 35(4):479–490CrossRefGoogle Scholar
  55. Tschinkel W, Willson C, Bern HA (1967) Sex pheromone of the mealworm beetle. Exp Zool 164:81–86CrossRefGoogle Scholar
  56. Vainikka A, Seppala O, Loytynoja K, Rantala MJ (2006) Fitness consequences of female preference for male pheromones in Tenebrio molitor. Evol Ecol Res 8:943–957Google Scholar
  57. Weaver RJ, Pratt GE, Hamnett AF, Jennings RC (1980) The influence of incubation conditions on the rates of juvenile hormone biosynthesis by corpora allata isolated from adult females of the beetle Tenebrio molitor. Insect Biochem 10:245–254CrossRefGoogle Scholar
  58. Worden BD, Parker PG (2001) Polyandry in grain beetles, Tenebrio molitor, leads to greater reproductive success: material or genetic benefits? Behav Ecol 12:761–767CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Malcolm L. McCallum
    • 1
  • Makensey Matlock
    • 2
  • Justin Treas
    • 3
  • Barroq Safi
    • 4
  • Wendy Sanson
    • 5
  • Jamie L. McCallum
    • 6
  1. 1.Department of Molecular Biology and BiochemistrySchool of Biological Sciences, University of Missouri-Kansas CityKansas CityUSA
  2. 2.Biology ProgramTexas A&M University-TexarkanaTexarkanaUSA
  3. 3.The Institute of Environmental and Human HealthTexas Tech UniversityLubbockUSA
  4. 4.Department of Biological SciencesTexas State UniversitySan MarcosUSA
  5. 5.Department of Biological SciencesLouisiana State University-Shreveport, One University PlaceShreveportUSA
  6. 6.Department of Biological and Earth SciencesUniversity of Central MissouriWarrensburgUSA

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