Journal of Chemical Ecology

, Volume 44, Issue 9, pp 785–795 | Cite as

Pheromones Regulating Reproduction in Subsocial Beetles: Insights with References to Eusocial Insects

  • Sandra Steiger
  • Johannes Stökl
Review Article


Beetles have evolved diverse strategies to cope with environmental challenges. Although parents of the vast majority of beetle species do not take care of their offspring, there are some species, in which parents provide elaborate post-hatching care and remain temporarily associated with their offspring to defend them from competitors or to provision them with food. Usually, socially induced reproductive “control” is a core feature of eusocial societies, but here we highlight that already in small family groups, socially induced reproductive regulation can play a fundamental role. By discussing the family life of burying beetles, we illustrate the mechanisms behind such a reproductive “control” and show that – similar to eusocial insects – pheromones can be an important regulating factor. However, apart from burying beetles, our knowledge of pheromones or other signals mediating reproductive regulation is surprisingly rudimentary for social beetles. More data are required to broaden our currently patchy picture.


Family life Fertility signal Parental care Nicrophorus Anti-aphrodisiac Juvenile hormone 



We thank Etya Amsalem and Abraham Hefetz for inviting us to contribute this review. We acknowledge funding provided by the German Research Foundation (DFG) to SS (STE 1874/3-3 and STE 1874/7-1) and to JS (STO 966/2-1), and by the HMWK via the LOEWE Center for Insect Biotechnology and Bioresources.


  1. Amsalem E, Hefetz A (2010) The appeasement effect of sterility signaling in dominance contests among Bombus terrestris workers. Behav Ecol Sociobiol 64:1685–1694Google Scholar
  2. Amsalem E, Twele R, Francke W, Hefetz A (2009) Reproductive competition in the bumble-bee Bombus terrestris: do workers advertise sterility? Proc R Soc B 276:1295–1304PubMedGoogle Scholar
  3. Arce AN, Johnston PR, Smiseth PT, Rozen DE (2012) Mechanisms and fitness effects of antibacterial defences in a carrion beetle. J Evol Biol 25:930–937PubMedGoogle Scholar
  4. Ashe JS (1987) Egg chamber production, egg protection and clutch size among fungivorus beetles of the genus Eumicrota (Coleoptera: Staphylinidae) and their evolutionary implications. Zool J Linnean Soc 90:255–273Google Scholar
  5. Bartlett J (1987) Evidence for a sex attractant in burying beetles. Ecol Entomol 12:471–472Google Scholar
  6. Bartlett J (1988) Male mating success and paternal care in Nicrophorus vespilloides (Coleoptera: Silphidae). Behav Ecol Sociobiol 23:297–304Google Scholar
  7. Beeler AE, Rauter CM, Moore AJ (2002) Mate discrimination by females in the burying beetle Nicrophorus orbicollis: the influence of male size on attractiveness to females. Ecol Entomol 27:1–6Google Scholar
  8. Biedermann PHW, Taborsky M (2011) Larval helpers and age polyethism in ambrosia beetles. Proc Natl Acad Sci 108:17064–17069PubMedGoogle Scholar
  9. Birkhead TR, Atkin L, Møller AP (1987) Copulation behaviour of birds. Behaviour 101:101–138Google Scholar
  10. Burger BBV (2015) First investigation of the semiochemistry of South African dung beetle species. In: Mucignal-Caretta C (ed) Neurobiology of chemical communication. CRC Press, Boca Raton, pp 57–97Google Scholar
  11. Butler CG, Callow RK, Johnston CJ (1962) The isolation and synthesis of queen substance, 9-oxodec-trans-2-enoic acid, a honeybee pheromone. Proc R Soc B 155:417–432Google Scholar
  12. Byers JA (2004) Chemical ecology of bark beetles in a complex olfactory landscape. In: Lieutier F, Day KR, Battisti A, Grégoire J-C and Evans HF (eds.) Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis. Springer, Dordrecht, pp 89–134Google Scholar
  13. Capodeanu-Nägler A, Keppner EM, Vogel H, Ayasse M, Eggert AK, Sakaluk SK, Steiger S (2016) From facultative to obligatory parental care: interspecific variation in offspring dependency on post-hatching care in burying beetles. Sci Rep 6:29323PubMedPubMedCentralGoogle Scholar
  14. Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241–244PubMedGoogle Scholar
  15. Chemnitz J, Jentschke PC, Ayasse M, Steiger S (2015) Beyond species recognition: somatic state affects long-distance sex pheromone communication. Proc R Soc B 282:20150832PubMedGoogle Scholar
  16. Chemnitz J, Bagrii N, Ayasse M, Steiger S (2017a) Staying with the young enhances the fathers' attractiveness in burying beetles. Evolution 71:985–994PubMedGoogle Scholar
  17. Chemnitz J, Bagrii N, Ayasse M, Steiger S (2017b) Variation in sex pheromone emission does not reflect immunocompetence but affects attractiveness of male burying beetles - a combination of laboratory and field experiments. Sci Nat 104:53Google Scholar
  18. Costa JT (2006) The other insect societies. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  19. Cotter SC, Topham E, Price AJP, Kilner RM (2010) Fitness costs associated with mounting a social immune response. Ecol Lett 13:1114–1123PubMedGoogle Scholar
  20. Creighton JC, Smith AN, Komendat A, Belk MC (2014) Dynamics of biparental care in a burying beetle: experimental handicapping results in partner compensation. Behav Ecol Sociobiol 69:265–271Google Scholar
  21. Degenkolb T, During RA, Vilcinskas A (2011) Secondary metabolites released by the burying beetle Nicrophorus vespilloides: chemical analyses and possible ecological functions. J Chem Ecol 37:724–735PubMedGoogle Scholar
  22. Dorrington J, Gore-Langton RE (1981) Prolactin inhibits oestrogen synthesis in the ovary. Nature 290:600–602PubMedGoogle Scholar
  23. Duarte A, Welch M, Swannack C, Wagner J, Kilner RM (2018) Strategies for managing rival bacterial communities: lessons from burying beetles. J Anim Ecol 87:414–427PubMedGoogle Scholar
  24. Ebie JD, Hölldobler B, Liebig J (2015) Larval regulation of worker reproduction in the polydomous ant Novomessor cockerelli. Naturwissenschaften 102:72PubMedGoogle Scholar
  25. Eggert A-K (1992) Alternative male mate-finding tactics in burying beetles. Behav Ecol 3:243–254Google Scholar
  26. Eggert AK, Müller JK (1989) Pheromone-mediated attraction in burying beetles. Ecol Entomol 14:235–238Google Scholar
  27. Eggert A-K, Müller JK (1997) Biparental care and social evolution in burying beetles: lessons from the larder. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge. Cambridge University Press, New York, pp 216–236Google Scholar
  28. Eggert A-K, Müller JK (2000) Timing of oviposition and reproductive skew in cobreeding female burying beetles (Nicrophorus vespilloides). Behav Ecol 11:357–366Google Scholar
  29. Eggert A-K, Sakaluk SK (1995) Female-coerced monogamy in burying beetles. Behav Ecol Sociobiol 37:147–153Google Scholar
  30. Eggert A-K, Sakaluk SK (2000) Benefits of communal breeding in burying beetles: a field experiment. Ecol Entomol 25:262–266Google Scholar
  31. Eggert A-K, Reinking M, Müller JK (1998) Parental care improves offspring survival and growth in burying beetles. Anim Behav 55:97–107PubMedGoogle Scholar
  32. Engel KC, von Hoermann C, Eggert A-K, Müller JK, Steiger S (2014) When males stop having sex: adaptive insect mating tactics during parental care. Anim Behav 90:245–253Google Scholar
  33. Engel KC, Männer L, Ayasse M, Steiger S (2015) Acceptance threshold theory can explain occurrence of homosexual behaviour. Biol Lett 11:20140603PubMedPubMedCentralGoogle Scholar
  34. Engel KC, Stökl J, Schweizer R, Vogel H, Ayasse M, Ruther J, Steiger S (2016) A hormone-related female anti-aphrodisiac signals temporary infertility and causes sexual abstinence to synchronize parental care. Nat Commun 7:11035PubMedPubMedCentralGoogle Scholar
  35. Farbre JH (1899) Souvenirs entomologiques - Sixième série. ParisGoogle Scholar
  36. Fowler K, Partridge L (1989) A cost of mating in female fruitflies. Nature 338:760Google Scholar
  37. Geiselhardt SF, Geiselhardt S, Peschke K (2006) Chemical mimicry of cuticular hydrocarbons – how does Eremostibes opacus gain access to breeding burrows of its host Parastizopus armaticeps (Coleoptera, Tenebrionidae)? Chemoecology 16:59–68Google Scholar
  38. Geiselhardt S, Jakobschy D, Ockenfels P, Peschke K (2008) A sex pheromone in the desert tenebrionid beetle Parastizopus armaticeps. J Chem Ecol 34:1065–1071PubMedGoogle Scholar
  39. Gilbert AN (1986) Mammary number and litter size in Rodentia: the “one-half rule”. Proc Natl Acad Sci 83:4828–4830PubMedGoogle Scholar
  40. Godfray HCJ (1991) Signalling of need by offspring to their parents. Nature 352:328–330Google Scholar
  41. Godfray HCJ (1995) Evolutionary theory of parent offspring conflict. Nature 376:133–138PubMedGoogle Scholar
  42. Godfray HCJ, Partridge L, Harvey PH (1991) Clutch size. Annu Rev Ecol Syst 22:409–429Google Scholar
  43. Haberer W, Schmitt T, Peschke K, Schreier P, Müller JK (2008) Ethyl 4-methyl heptanoate: a male-produced pheromone of Nicrophorus vespilloides. J Chem Ecol 34:94–98PubMedGoogle Scholar
  44. Haberer W, Steiger S, Müller JK (2010) (E)-Methylgeranate, a chemical signal of juvenile hormone titre and its role in the partner recognition system of burying beetles. Anim Behav 79:17–24Google Scholar
  45. Haberer W, Schmitt T, Schreier P, Müller JK (2011) Intended and unintended receivers of the male pheromones of the burying beetles Nicrophorus humator and Nicrophorus vespilloides. Entomol Exp Appl 140:122–126Google Scholar
  46. Haberer W, Steiger S, Müller JK (2014) Dynamic changes in volatile emissions of breeding burying beetles. Physiol Entomol 39:153–164Google Scholar
  47. Haberer W, Schmitt T, Schreier P, Eggert A-K, Müller JK (2017) Volatiles emitted by calling males of burying beetles and Ptomascopus morio (Coleoptera: Silphidae: Nicrophorinae) are biogenetically related. J Chem Ecol 43:971–977PubMedGoogle Scholar
  48. Hall CL, Wadsworth NK, Howard DR, Jennings EM, Farrell LD, Magnuson TS, Smith RJ (2011) Inhibition of microorganisms on a carrion breeding resource: the antimicrobial peptide activity of burying beetle (Coleoptera: Silphidae) oral and anal secretions. Environ Entomol 40:669–678PubMedGoogle Scholar
  49. Hamada Y, Schlaff S, Kobayashi Y, Santulli R, Wright KH, Wallach EE (1980) Inhibitory effect of prolactin on ovulation in the in vitro perfused rabbit ovary. Nature 285:161–163PubMedGoogle Scholar
  50. Hanski I, Cambefort Y (1991) Dung beetle ecology. Princeton University PressGoogle Scholar
  51. Happ GM (1969) Multiple sex pheromones of the mealworm beetle, Tenebrio molitor L. Nature 222:180–181PubMedGoogle Scholar
  52. Hardy ICW, Griffiths NT, Godfray HCJ (1992) Clutch size in a parasitoid wasp: a manipulation experiment. J Anim Ecol 61:121–129Google Scholar
  53. Head ML, Berry LK, Royle NJ, Moore AJ (2012) Paternal care: direct and indirect genetic effects of fathers on offspring performance. Evolution 66:3570–3581PubMedGoogle Scholar
  54. Head ML, Hinde CA, Moore AJ, Royle NJ (2014) Correlated evolution in parental care in females but not males in response to selection on paternity assurance behaviour. Ecol Lett 17:803–810PubMedPubMedCentralGoogle Scholar
  55. Heinze J, Trunzer B, Oliveira P, Hölldobler B (1996) Regulation of reproduction in the neotropical ponerine ant, Pachycondyla villosa. J Insect Behav 9:441–450Google Scholar
  56. Hemptinne J-L, Lognay G, Doumbia M, Dixon AFG (2001) Chemical nature and persistence of the oviposition deterring pheromone in the tracks of the larvae of the two spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Chemoecology 11:43–47Google Scholar
  57. Högstedt G (1980) Evolution of clutch size in birds: adaptive variation in relation to territory quality. Science 210:1148–1150PubMedGoogle Scholar
  58. Holman L, Lanfear R, d'Ettorre P (2013) The evolution of queen pheromones in the ant genus Lasius. J Evol Biol 26:1549–1558PubMedGoogle Scholar
  59. Hopwood PE, Moore AJ, Royle NJ (2014) Effects of resource variation during early life and adult social environment on contest outcomes in burying beetles: a context-dependent silver spoon strategy? Proc Biol Sci 281:20133102PubMedPubMedCentralGoogle Scholar
  60. House CM, Hunt J, Moore AJ (2007) Sperm competition, alternative mating tactics and context-dependent fertilization success in the burying beetle, Nicrophorus vespilloides. Proc R Soc B 274:1309–1315PubMedGoogle Scholar
  61. House CM, Evans GMV, Smiseth PT, Stamper CE, Walling CA, Moore AJ (2008) The evolution of repeated mating in the burying beetle, Nicrophorus vespilloides. Evolution 62:2004–2014PubMedGoogle Scholar
  62. House CM, Walling CA, Stamper CE, Moore AJ (2009) Females benefit from multiple mating but not multiple mates in the burying beetle Nicrophorus vespilloides. J Evol Biol 22:1961–1966PubMedGoogle Scholar
  63. Hulcr J, Stelinski LL (2017) The ambrosia symbiosis: from evolutionary ecology to practical management. Annu Rev Entomol 62:285–303PubMedGoogle Scholar
  64. Jacobs CG, Steiger S, Heckel DG, Wielsch N, Vilcinskas A, Vogel H (2016) Sex, offspring and carcass determine antimicrobial peptide expression in the burying beetle. Sci Rep 6:25409PubMedPubMedCentralGoogle Scholar
  65. Jarrett BJ, Schrader M, Rebar D, Houslay TM, Kilner RM (2017) Cooperative interactions within the family enhance the capacity for evolutionary change in body size. Nat Ecol Evol 1:0178PubMedPubMedCentralGoogle Scholar
  66. Kalinova B, Podskalska H, Ruzicka J, Hoskovec M (2009) Irresistible bouquet of death-how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschaften 96:889–899PubMedGoogle Scholar
  67. Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794Google Scholar
  68. Kent DS, Simpson JA (1992) Eusociality in the beetle Austroplatypus incompertus (Coleoptera: Curculionidae). Naturwissenschaften 79:86–87Google Scholar
  69. Keppner EM, Prang M, Engel KC, Ayasse M, Stokl J, Steiger S (2017) Beyond cuticular hydrocarbons: chemically mediated mate recognition in the subsocial burying beetle Nicrophorus vespilloides. J Chem Ecol 43:84–93PubMedGoogle Scholar
  70. Kilner RM, Hinde CA (2012) Parent-offspring conflict. In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 119–132Google Scholar
  71. Kilner R, Johnstone RA (1997) Begging the question: are offspring solicitation behaviours signals of need? Trends Ecol Evol 12:11–15PubMedGoogle Scholar
  72. Kirkendall LR, Kent DS, Raffa KF (1997) Interactions among males, females and offspring in bark and ambrosia beetles: the significance of living in tunnels for the evolution of social behavior. Cambridge University Press, Cambridge, pp 181–215Google Scholar
  73. Kirkendall LR, Biedermann PH, Jordal BH (2015) Evolution and diversity of bark and ambrosia beetles. In: Bark beetles: biology and ecology of native and invasive species. Academic Press, San Diego, pp 85–156Google Scholar
  74. Klemperer HG (1982) Parental behaviour in Copris lunaris (Coleoptera, Scarabaeidae): Care and defence of brood balls and nest. Ecological Entomology 7:155–167Google Scholar
  75. Kölliker M, Chuckalovcak JP, Haynes KF, Brodie ED (2006) Maternal food provisioning in relation to condition-dependent offspring odours in burrower bugs (Sehirus cinctus). Proc R Soc B 273:1523–1528PubMedGoogle Scholar
  76. Konner M, Worthman C (1980) Nursing frequency, gonadal function, and birth spacing among !Kung hunter-gatherers. Science 207:788–791PubMedGoogle Scholar
  77. Kramer J, Meunier J (2017) The evolution of social life in family groups. bioRxiv.
  78. Le Conte Y, Hefetz A (2008) Primer pheromones in social hymenoptera. Annu Rev Entomol 53:523–542PubMedGoogle Scholar
  79. Leonhardt SD, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164:1277–1287PubMedGoogle Scholar
  80. Lessels C (2012) Sexual conflict. In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 150–170Google Scholar
  81. Lung O, Tram U, Finnerty CM, Eipper-Mains MA, Kalb JM, Wolfner MF (2002) The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression. Genetics 160:211–224PubMedPubMedCentralGoogle Scholar
  82. Maisonnasse A, Lenoir J-C, Beslay D, Crauser D, Le Conte Y (2010) E-β-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLoS ONE 5:e13531PubMedPubMedCentralGoogle Scholar
  83. Malouines C (2017) Counter-perfume: using pheromones to prevent female remating. Biol Rev Camb Philos Soc 92:1570–1581PubMedGoogle Scholar
  84. Mas F, Kölliker M (2008) Maternal care and offspring begging in social insects: chemical signalling, hormonal regulation and evolution. Anim Behav 76:1121–1131Google Scholar
  85. Matsuura K, Himuro C, Yokoi T, Yamamoto Y, Vargo EL, Keller L (2010) Identification of a pheromone regulating caste differentiation in termites. Proc Natl Acad Sci 107:12963–12968PubMedGoogle Scholar
  86. Müller JK (1987) Replacement of a lost clutch - a strategy for optimal resource utilization in Necrophorus vespilloides (Coleoptera, Silphidae). Ethology 76:74–80Google Scholar
  87. Müller JK, Eggert A-K (1987) Effects of carrion-independent pheromone emission by male burying beetles (Silphidae: Necrophorus). Ethology 76:297–304Google Scholar
  88. Müller JK, Eggert AK (1989) Paternity assurance by helpful males adaptations to sperm competition in burying beetles. Behav Ecol Sociobiol 24:245–250Google Scholar
  89. Müller JK, Eggert AK, Dressel J (1990a) Intraspecific brood parasitism in the burying beetle Necrophorus vespilloides Coleoptera Silphidae. Anim Behav 40:491–499Google Scholar
  90. Müller JK, Eggert AK, Furlkröger E (1990b) Clutch size regulation in the burying beetle Necrophorus vespilloides Herbst Coleoptera Silphidae. J Insect Behav 3:265–270Google Scholar
  91. Müller JK, Braunisch V, Hwang WB, Eggert AK (2007) Alternative tactics and individual reproductive success in natural associations of the burying beetle, Nicrophorus vespilloides. Behav Ecol 18:196–203Google Scholar
  92. Oi CA, van Zweden JS, Oliveira RC, Van Oystaeyen A, Nascimento FS, Wenseleers T (2015) The origin and evolution of social insect queen pheromones: novel hypotheses and outstanding problems. Bioessays 37:808–821PubMedGoogle Scholar
  93. Otronen M (1988) The effect of body size on the outcome of fights in burying beetles Nicrophorus. Ann Zool Fenn 25:191–201Google Scholar
  94. Palmer WJ, Duarte A, Schrader M, Day JP, Kilner R, Jiggins FM (2016) A gene associated with social immunity in the burying beetle Nicrophorus vespilloides. Proc R Soc B 283Google Scholar
  95. Parker GA, Royle NJ, Hartley IR (2002) Intrafamilial conflict and parental investment: a synthesis. Philos Trans R Soc B 357:295–307Google Scholar
  96. Peso M, Elgar MA, Barron AB (2015) Pheromonal control: reconciling physiological mechanism with signalling theory. Biol Rev Camb Philos Soc 90:542–559PubMedGoogle Scholar
  97. Pilson D, Rausher MD (1988) Clutch size adjustment by a swallowtail butterfly. Nature 333:361Google Scholar
  98. Pukowski E (1933) Ökologische untersuchungen an Necrophorus F. Z Morphol Okol Tiere 27:518–586Google Scholar
  99. Rasa O (1990) Evidence for subsociality and division of labor in a desert tenebrionid beetle Parastizopus armaticeps Peringuey. Naturwissenschaften 77:591–592Google Scholar
  100. Rasa OAE (1999) Division of labour and extended parenting in a desert Tenebrionid beetle. Ethology 105:37–56Google Scholar
  101. Reid ML, Roitberg BD (1994) Benefits of prolonged male residence with mates and brood in Pine Engravers (Coleoptera: Scolytidae). Oikos 70:140Google Scholar
  102. Robertson IC (1993) Nest intrusions, infanticide, and parental care in the burying beetle, Nicrophorus orbicollis (Coleoptera: Silphidae). J Zool 231:583–593Google Scholar
  103. Royle NJ (2016) Parental care: when the sex has to stop. Curr Biol 26:R478–R480PubMedGoogle Scholar
  104. Royle NJ, Hopwood PE (2017) Chapter four - covetable corpses and plastic beetles—the socioecological behavior of burying beetles. In: Naguib M, Podos J, Simmons LW, Barrett L, Healy SD, Zuk M (eds) Advances in the study of behavior. Academic Press, pp 101–146Google Scholar
  105. Schedwill P, Eggert A-K, Müller JK (2018) How burying beetles spread their seed: the Coolidge effect in real life. Zool Anz 273:210–217Google Scholar
  106. Schlechter-Helas J, Schmitt T, Peschke K (2011) A contact anti-aphrodisiac pheromone supplied by the spermatophore in the rove beetle Aleochara curtula: mode of transfer and evolutionary significance. Naturwissenschaften 98:855PubMedGoogle Scholar
  107. Schultner E, Oettler J, Helanterä H (2017) The role of brood in eusocial Hymenoptera. Q Rev Biol 92:39–78PubMedGoogle Scholar
  108. Scott MP (1994) The benefit of paternal assistance in intra- and interspecific competition for the burying beetle, Nicrophorus defodiens. Ethol Ecol Evol 6:537–543Google Scholar
  109. Scott MP (1998) The ecology and behavior of burying beetles. Annu Rev Entomol 43:595–618PubMedGoogle Scholar
  110. Scott MP, Panaitof SC (2004) Social stimuli affect juvenile hormone during breeding in biparental burying beetles (Silphidae: Nicrophorus). Horm Behav 45:159–167PubMedGoogle Scholar
  111. Scott MP, Traniello JFA (1987) Behavioral cues trigger ovarian development in the burying beetle, Nicrophorus tomentosus. J Insect Physiol 33:693–696Google Scholar
  112. Scott MP, Traniello JFA (1990) Behavioral and ecological correlates of male and female parental care and reproductive success in burying beetles Nicrophorus spp. Anim Behav 39:274–283Google Scholar
  113. Scott MP, Lee WJ, van der Reijden ED (2007) The frequency and fitness consequences of communal breeding in a natural population of burying beetles: a test of reproductive skew. Ecol Entomol 32:651–661Google Scholar
  114. Shukla SP, Vogel H, Heckel DG, Vilcinskas A, Kaltenpoth M (2017) Burying beetles regulate the microbiome of carcasses and use it to transmit a core microbiota to their offspring. Mol EcolGoogle Scholar
  115. Sikes DS, Venables C (2013) Molecular phylogeny of the burying beetles (Coleoptera: Silphidae: Nicrophorinae). Mol Phylogenet Evol 69:552–565PubMedGoogle Scholar
  116. Simmons R (1990) Copulation patterns of African marsh harriers: evaluating the paternity assurance hypothesis. Anim Behav 40:1151–1157Google Scholar
  117. Simmons LW, Ridsdill-Smith TJ (2011) Ecology and evolution of dung beetles. Wiley, SussexGoogle Scholar
  118. Smiseth PT, Moore AJ (2004) Signalling of hunger when offspring forage by both begging and self-feeding. Anim Behav 67:1083–1088Google Scholar
  119. Smiseth PT, Darwell CT, Moore AJ (2003) Partial begging: an empirical model for the early evolution of offspring signalling. Proc R Soc B 270:1773–1777PubMedGoogle Scholar
  120. Smiseth PT, Ward RJS, Moore AJ (2006) Asynchronous hatching in Nicrophorus vespilloides, an insect in which parents provide food for their offspring. Funct Ecol 20:151–156Google Scholar
  121. Smiseth PT, Kölliker M, Royle NJ (2012) What is parental care? In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 1–17Google Scholar
  122. Smith AA, Liebig J (2017) The evolution of cuticular fertility signals in eusocial insects. Curr Opin Insect Sci 22:79–84PubMedGoogle Scholar
  123. Steiger S, Müller JK (2010) From class-specific to individual discrimination: acceptance threshold changes with risk in the partner recognition system of the burying beetle Nicrophorus vespilloides. Anim Behav 80:607–613Google Scholar
  124. Steiger S, Stökl J (2017) Pheromones involved in insect parental care and family life. Curr Opin Insect Sci 24:89–95Google Scholar
  125. Steiger S, Peschke K, Francke W, Müller JK (2007) The smell of parents: breeding status influences cuticular hydrocarbon pattern in the burying beetle Nicrophorus vespilloides. Proc R Soc B 274:2211–2220PubMedGoogle Scholar
  126. Steiger S, Franz R, Eggert A-K, Müller JK (2008) The Coolidge effect, individual recognition and selection for distinctive cuticular signatures in a burying beetle. Proc R Soc B 275:1831–1838PubMedGoogle Scholar
  127. Steiger S, Gershman SN, Pettinger AM, Eggert A-K, Sakaluk SK (2011a) Sex differences in immunity and rapid upregulation of immune defence during parental care in the burying beetle, Nicrophorus orbicollis. Funct Ecol 25:1368–1378Google Scholar
  128. Steiger S, Haberer W, Müller JK (2011b) Social environment determines degree of chemical signalling. Biol Lett 7:822–824PubMedPubMedCentralGoogle Scholar
  129. Steiger S, Gershman SN, Pettinger AM, Eggert A-K, Sakaluk SK (2012) Dominance status and sex influence nutritional state and immunity in burying beetles Nicrophorus orbicollis. Behav Ecol 23:1126–1132Google Scholar
  130. Sun SJ, Rubenstein DR, Chen BF, Chan SF, Liu JN, Liu M, Hwang W, Yang PS, Shen SF (2014) Climate-mediated cooperation promotes niche expansion in burying beetles. eLife 3:e02440PubMedPubMedCentralGoogle Scholar
  131. Suzuki S (2001) Suppression of fungal development on carcasses by the burying beetle Nicrophorus quadripunctatus (Coleoptera: Silphidae). Entomol Sci 4:403–405Google Scholar
  132. Teseo S, Kronauer DJ, Jaisson P, Chaline N (2013) Enforcement of reproductive synchrony via policing in a clonal ant. Curr Biol 23:328–332PubMedGoogle Scholar
  133. Thomas ML (2011) Detection of female mating status using chemical signals and cues. Biol Rev 86(1):14Google Scholar
  134. Tortosa FS, Redondo T (1992) Frequent copulations despite low sperm competition in white storks (Ciconia ciconia). Behaviour 121:288–314Google Scholar
  135. Traynor KS, Le Conte Y, Page RE Jr (2015) Age matters: pheromone profiles of larvae differentially influence foraging behaviour in the honeybee, Apis mellifera. Anim Behav 99:1–8Google Scholar
  136. Trivers R (1972) Parental investment and sexual selection. In: Cambell B (ed) Sexual selection and the descent of man. Aldine Press, Chicago, pp 139–179Google Scholar
  137. Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264Google Scholar
  138. Trumbo ST (1990a) Interference competition among burying beetles (Silphidae, Nicrophorus). Ecol Entomol 15:347–355Google Scholar
  139. Trumbo ST (1990b) Reproductive benefits of infanticide in a biparental burying beetle Nicrophorus orbicollis. Behav Ecol Sociobiol 27:269–274Google Scholar
  140. Trumbo ST (1992) Monogamy to communal breeding: exploitation of a broad resource base by burying beetles (Nicrophorus). Ecol Entomol 17:289–298Google Scholar
  141. Trumbo ST (1996) Parental care in invertebrates. Adv Study Behav 25:3–51Google Scholar
  142. Trumbo ST (1997) Juvenile hormone-mediated reproduction in burying beetles: from behavior to physiology. Arch Insect Biochem Physiol 35:479–490Google Scholar
  143. Trumbo ST (2006) Infanticide, sexual selection and task specialization in a biparental burying beetle. Anim Behav 72:1159–1167Google Scholar
  144. Trumbo ST, Eggert A-K (1994) Beyond monogamy: territory quality influences sexual advertisement in male burying beetles. Anim Behav 48:1043–1047Google Scholar
  145. Trumbo ST, Robinson GE (2008) Social and nonsocial stimuli and juvenile hormone titer in a male burying beetle, Nicrophorus orbicollis. J Insect Physiol 54:630–635PubMedGoogle Scholar
  146. Trumbo ST, Valletta RC (2007) The costs of confronting infanticidal intruders in a burying beetle. Ethology 113:386–393Google Scholar
  147. Ulrich Y, Burns D, Libbrecht R, Kronauer DJ (2016) Ant larvae regulate worker foraging behavior and ovarian activity in a dose-dependent manner. Behav Ecol Sociobiol 70:1011–1018PubMedGoogle Scholar
  148. Van Oystaeyen A, Oliveira RC, Holman L, van Zweden JS, Romero C, Oi CA, d'Ettorre P, Khalesi M, Billen J, Wäckers F et al (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290PubMedGoogle Scholar
  149. Vogel H, Shukla SP, Engl T, Weiss B, Fischer R, Steiger S, Heckel DG, Kaltenpoth M, Vilcinskas A (2017) The digestive and defensive basis of carcass utilization by the burying beetle and its microbiota. Nat Commun 8:15186PubMedPubMedCentralGoogle Scholar
  150. Walling CA, Stamper CE, Smiseth PT, Moore AJ (2008) The quantitative genetics of sex differences in parenting. Proc Natl Acad Sci 105:18430–18435PubMedGoogle Scholar
  151. Weil T, Hoffmann K, Kroiss J, Strohm E, Korb J (2009) Scent of a queen — cuticular hydrocarbons specific for female reproductives in lower termites. Naturwissenschaften 96:315–319PubMedGoogle Scholar
  152. Wilson DS, Knollenberg WG (1984) Food discrimination and ovarian development in burying beetles (Coleoptera, Silphidae, Nicrophorus). Ann Entomol Soc Am 77:165–170Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Insect BiotechnologyJustus-Liebig-University of GießenGießenGermany
  2. 2.Department of Evolutionary Animal EcologyUniversity of BayreuthBayreuthGermany
  3. 3.Department of Applied EntomologyUniversity of HohenheimStuttgartGermany

Personalised recommendations