Maternal care and offspring begging in social insects: chemical signalling, hormonal regulation and evolution

Animal Behaviour

Volumn 76, Issue 4, 2008, Pages 1121-1131

  Mas, Flore ^a   Kölliker, Mathias ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

begging behaviour; chemical cue; juvenile hormone; maternal care; parent offspring conflict; pheromone; signal; social insect

Indexed keywords

BEGGING BEHAVIOR; DEVELOPMENTAL BIOLOGY; FOOD AVAILABILITY; HATCHING; INTERSPECIFIC COMPETITION; INTERSPECIFIC INTERACTION; JUVENILE; MATERNAL CARE; PARENT-OFFSPRING INTERACTION; PHEROMONE; SOCIAL INSECT;

HEXAPODA; VERTEBRATA;

EID: 51549093539     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2008.06.011     Document Type: Review

References (131)

1. Agrawal A.F., Brodie E.D., and Brown J. Parent-offspring coadaptation and the dual genetic control of maternal care. Science 292 (2001) 1710-1712
2. Agrawal A.F., Combs N., and Brodie E.D. Insights into the costs of complex maternal care behavior in the burrower bug (Sehirus cinctus). Behavioral Ecology and Sociobiology 57 (2005) 566-574
3. Bellés X., Martin D., and Piulachs M.D. The mevalonate pathway and the synthesis of juvenile hormone in insects. Annual Review of Entomology 50 (2005) 181-199
4. den Boer S., and Duchateau M. A larval hunger signal in the bumblebee Bombus terrestris. Insectes Sociaux 53 (2006) 369-373
5. Borges M., and Aldrich J.R. Instar-specific defensive secretions of stink bugs (Heteroptera, Pentatomidae). Experientia 48 (1992) 893-896
6. Bourke A.F.G., and Ratnieks F.L.W. Kin conflict over caste determination in social Hymenoptera. Behavioral Ecology and Sociobiology 46 (1999) 287-297
7. Bristow C.M. Treehoppers transfer parental care to ants: a new benefit of mutualism. Science 220 (1983) 532-533
8. Brossut R. Allomonal secretions in cockroaches. Journal of Chemical Ecology 9 (1983) 143-158
9. Budden A.E., and Wright J. Begging in nestling birds. Current Ornithology 16 (2001) 83-118
10. Caussanel C., Olivier A., Arnault C., Breuzet M., and Karlinsky A. Mechanisms and control of egg-laying of the earwig Labidura riparia (Dermaptera, Labiduridae). Annales de la Société Entomologique de France 22 (1986) 119-128
11. Clutton-Brock T.H. The Evolution of Parental Care (1991), Princeton University Press, Princeton, New Jersey
12. Cocroft R.B. Insect vibrational defence signals. Nature 382 (1996) 679-680
13. Cocroft R.B. Offspring-parent communication in a subsocial treehopper (Hemiptera: Membracidae: Umbonia crassicornis). Behaviour 136 (1999) 1-21
14. Cocroft R.B. Vibrational communication and the ecology of group-living, herbivorous insects. American Zoologist 41 (2001) 1215-1221
15. Cocroft R.B. Antipredator defense as a limited resource: unequal predation risk in broods of an insect with maternal care. Behavioral Ecology 13 (2002) 125-133
16. Costa J.T. The Other Insect Society (2006), Harvard University Press, Cambridge, Massachusetts
17. Crook T.C., Flatt T., and Smiseth P.T. Hormonal modulation of larval begging and growth in the burying beetle Nicrophorus vespilloides. Animal Behaviour 75 (2008) 71-77
18. Edgerly J.S. Life beneath silk walls: a review of the primitively social Embiidina. In: Choe J.C., and Crespi B.J. (Eds). The Evolution of Social Behavior in Insects and Arachnids (1997), Cambridge University Press, Cambridge 14-25
19. Eggert A.K., and Müller J.K. Joint breeding in female burying beetles. Behavioral Ecology and Sociobiology 31 (1992) 237-242
20. Eggert A.-K., and Müller J.K. Biparental care and social evolution in burying beetles: lessons from the larder. In: Choe J.C., and Crespi B.J. (Eds). The Evolution of Social Behavior in Insects and Arachnids (1997), Cambridge University Press, Cambridge 216-236
21. Eggert A.K., Reinking M., and Müller J.K. Parental care improves offspring survival and growth in burying beetles. Animal Behaviour 55 (1998) 97-107
22. Eisner T., Rossini C., and Eisner M. Chemical defense of an earwig (Doru taeniatum). Chemoecology 10 (2000) 81
23. Endler J.A., and Basolo A.L. Sensory ecology, receiver biases and sexual selection. Trends in Ecology & Evolution 13 (1998) 415-420
24. Fetherston I.A., Scott M.P., and Traniello J.F.A. Parental care in burying beetles: the organization of male and female brood-care behavior. Ethology 85 (1990) 177-190
25. Field J. The evolution of progressive provisioning. Behavioral Ecology 16 (2005) 770-778
26. Fulton B.B. Some habits of earwigs. Annals of the Entomological Society of America 17 (1924) 357-367
27. Godfray H.C.J. Signaling of need by offspring to their parents. Nature 352 (1991) 328-330
28. Godfray H.C.J. Signalling of need between parents and young: parent-offspring conflict and sibling rivalry. American Naturalist 146 (1995) 1-24
29. Groothuis T.G.G., and Ros A.F.H. The hormonal control of begging and early aggressive behavior: experiments in black-headed gull chicks. Hormones & Behavior 48 (2005) 207-215
30. Gwynne D.T. Reproductive behavior of ground weta (Orthoptera: Anostostomatidae): drumming behavior, nuptial feeding, post-copulatory guarding and maternal care. Journal of the Kansas Entomological Society 77 (2004) 414-428
31. Halffter G. Subsocial behavior in Scarabeinae beetles. In: Choe J.C., and Crespi B.J. (Eds). The Evolution of Social Behavior in Insects and Arachnids (1997), Cambridge University Press, Cambridge 237-259
32. Hölldobler B., Stanton R.C., and Markl H. Recruitment and food-retrieving behavior in Novomessor (Formicidae, Hymenoptera). 1. Chemical Signals. Behavioral Ecology and Sociobiology 4 (1978) 163-181
33. Huang Z.Y., and Otis G.W. Inspection and feeding of larvae by worker honey-bees (Hymenoptera, Apidae): effect of starvation and food quantity. Journal of Insect Behavior 4 (1991) 305-317
34. Hunt J., and Simmons L.W. Optimal maternal investment in the dung beetle Onthophagus taurus?. Behavioral Ecology and Sociobiology 55 (2004) 302-312
35. Ishay J., and Landau E.M. Vespa larvae send out rhythmic hunger signals. Nature 237 (1972) 286-287
36. Ishay J., and Schwartz A. Acoustical communication between members of an oriental hornet (Vespa orientalis) colony. Journal of the Acoustical Society of America 53 (1973) 640-649
37. Johnstone R.A. Begging and sibling competition: how should offspring respond to their rivals?. American Naturalist 163 (2004) 388-406
38. Kaitala A., and Mappes J. Parental care and reproductive investment in shield bugs (Acanthosomatidae, Heteroptera). Oikos 80 (1997) 3-7
39. Kaptein N., Billen J., and Gobin B. Larval begging for food enhances reproductive options in the ponerine ant Gnamptogenys striatula. Animal Behaviour 69 (2005) 293-299
40. Kight S.L. Factors influencing maternal behaviour in a burrower bug, Sehirus cinctus (Heteroptera: Cydnidae). Animal Behaviour 53 (1997) 105-112
41. Kilner R., and Johnstone R.A. Begging the question: are offspring solicitation behaviours signals of needs. Trends in Ecology & Evolution 12 (1997) 11-15
42. Kirkendall L.R., Kent D.S., and Raffa K.A. Interactions among males, females and offspring in bark and ambrosia beetles: the significance of living in tunnels for the evolution of social behavior. In: Choe J.C., and Crespi B.J. (Eds). The Evolution of Social Behavior in Insects and Arachnids (1997), Cambridge University Press, Cambridge 181-215
43. Klemperer H.G. Parental behavior in Copris lunaris (Coleoptera, Scarabaeidae): care and defense of brood balls and nest. Ecological Entomology 7 (1982) 155-167
44. Klemperer H.G. The evolution of parental behavior in scarabaeinae (Coleoptera, Scarabaeidae): an experimental approach. Ecological Entomology 8 (1983) 49-59
45. Klemperer H.G. Subsocial behavior in Oniticellus cinctus (Coleoptera, Scarabaeidae): effect of the brood on parental care and oviposition. Physiological Entomology 8 (1983) 393-402
46. Klosternmeyer E.C. The life history and habits of the ring-legged earwig, Eurobellia annulipes (Lucus [sic]) (Order Dermaptera). Journal of the Kansas Entomological Society 15 (1942) 13-18
47. Kohno K. Possible influences of habitat characteristics on the evolution of semelparity and cannibalism in the hump earwig Anechura harmandi. Researches on Population Ecology 39 (1997) 11-16
48. Kölliker M. Benefits and costs of earwig (Forficula auricularia) family life. Behavioral Ecology and Sociobiology 61 (2007) 1489-1497
49. Kölliker M., Brodie III E.D., and Moore A.J. The coadaptation of parental supply and offspring demand. American Naturalist 166 (2005) 505-516
50. Kölliker M., Chuckalovcak J.P., and Brodie III E.D. Offspring chemical cues affect maternal provisioning in burrower bugs (Sehirus cinctus). Animal Behaviour 69 (2005) 959-966
51. Kölliker M., Chuckalovcak J.P., Haynes K.F., and Brodie E.D. Maternal food provisioning in relation to condition-dependent offspring odours in burrower bugs (Sehirus cinctus). Proceedings of the Royal Society of London, Series B 273 (2006) 1523-1528
52. Kudô S. Brooding behavior in Elasmucha putoni (Heteroptera, Acanthosomatidae), and a possible nymphal alarm substance triggering guarding responses. Applied Entomology and Zoology 25 (1990) 431-437
53. Kudô S.I. The guarding posture of females in the subsocial bug Elasmucha dorsalis (Heteroptera: Acanthosomatidae). European Journal of Entomology 97 (2000) 137-139
54. Lamb R.J. Dispersal by nesting earwigs, Forficula auricularia (Dermaptera, Forficulidae). Canadian Entomologist 108 (1976) 213-216
55. Lamb R.J. Parental behavior in Dermaptera with special reference to Forficula auricularia (Dermaptera, Forficulidae). Canadian Entomologist 108 (1976) 609-619
56. Lazarus J., and Inglis I.R. Shared and unshared parental investment, parent offspring conflict and brood size. Animal Behaviour 34 (1986) 1791-1804
57. Le Conte Y., Arnold G., Trouiller J., and Masson C. Identification of a brood pheromone in honeybees. Naturwissenschaften 77 (1990) 334-336
58. Le Conte Y., Sreng L., and Poitout S.H. Brood pheromone can modulate the feeding behavior of Apis mellifera workers (Hymenoptera, Apidae). Journal of Economic Entomology 88 (1995) 798-804
59. Le Conte Y., Mohammedi A., and Robinson G.E. Primer effects of a brood pheromone on honeybee behavioural development. Proceedings of the Royal Society of London, Series B 268 (2001) 163-168
60. Ledoux A. Biologie et comportement de l'Embioptère Monotylota ramburi. Annales des Sciences Naturelles, Zoologie 20 (1958) 515-523
61. Lessells C.M. Neuroendocrine control of life histories: what do we need to know to understand the evolution of phenotypic plasticity?. Philosophical Transactions of the Royal Society of London, Series B 363 (2008) 1589-1598
62. Lock J.E., Smiseth P.T., and Moore A.J. Selection, inheritance, and the evolution of parent-offspring interactions. American Naturalist 164 (2004) 13-24
63. Lockwood J.A., and Story R.N. Bifunctional pheromone in the 1st instar of the southern green stink bug, Nezara viridula (L) (Hemiptera, Pentatomidae): its characterization and interaction with other stimuli. Annals of the Entomological Society of America 78 (1985) 474-479
64. Lockwood J.A., and Story R.N. Adaptive functions of nymphal aggregation in the southern green stink bug, Nezara viridula (L) (Hemiptera, Pentatomidae). Environmental Entomology 15 (1986) 739-749
65. Lockwood J.A., and Story R.N. Defensive secretion of the southern green stink bug (Hemiptera, Pentatomidae) as an alarm pheromone. Annals of the Entomological Society of America 80 (1987) 686-691
66. Matsuura M., and Yamane S. Biology of the Vespine Wasps (1984), Springer, Berlin
67. Maynard Smith J., and Harper D. Animal Signals (2003), Oxford University Press, New York
68. Melber A., Holscher L., and Schmidt G.H. Further studies on the social behavior and its ecological significance in Elasmucha grisea L (Hem-Het, Acanthosomatidae). Zoologischer Anzeiger 205 (1980) 27-38
69. Montheit G.B., and Storey R.I. The biology of Cephalodesmius, a genus of dung beetles which synthesizes 'dung' from plant material (Coleoptera: Scarabaeidae: Scarabaeinae). Memoires of Queensland Museum 20 (1981) 253-277
70. Müller W., Lessells C.M., Korsten P., and von Engelhardt N. Manipulative signals in family conflict? On the function of maternal yolk hormones in birds. American Naturalist 169 (2007) E84-E96
71. Nalepa C.A. Colony composition, protozoan transfer and some life-history characteristics of the woodroach Cryptocercus punctulatus scudder (Dictyoptera, Cryptocercidae). Behavioral Ecology and Sociobiology 14 (1984) 273-279
72. Nalepa C.A. Early development of nymphs and establishment of hindgut symbiosis in Cryptocercus punctulatus (Dictyoptera, Cryptocercidae). Annals of the Entomological Society of America 83 (1990) 786-789
73. Nalepa C.A., and Bell W.J. Postovulation parental investment and parental care in cockroaches. In: Choe J.C., and Crespi B.J. (Eds). The Evolution of Social Behavior in Insects and Arachnids (1997), Cambridge Univeristy Press, Cambridge 26-51
74. Nault L.R., Wood T.K., and Goff A.M. Treehopper (Membracidae) alarm pheromones. Nature 249 (1974) 387-388
75. Nijhout H.F. Insect Hormones (1994), Princeton University Press, Princeton, New Jersey
76. Pankiw T. Brood pheromone modulation of pollen forager turnaround time in the honey bee (Apis mellifera L.). Journal of Insect Behavior 20 (2007) 173-180
77. Parker G.A., and Macnair M.R. Models of parent-offspring conflict. 4. Suppression: evolutionary retaliation by the parent. Animal Behaviour 27 (1979) 1210-1235
78. Parker G.A., Royle N.J., and Hartley I.R. Intrafamilial conflict and parental investment: a synthesis. Philosophical Transactions of the Royal Society of London, Series B 357 (2002) 295-307
79. Parr A., Tallamy D.W., Monaco E.L., and Pesek J.D. Proximate factors regulating maternal options in the eggplant lace bug, Gargaphia solani (Heteroptera: Tingidae). Journal of Insect Behavior 15 (2002) 495-511
80. Quillfeldt P., Masello J.F., Strange I.J., and Buchanan K.L. Begging and provisioning of thin-billed prions, Pachyptila belcheri, are related to testosterone and corticosterone. Animal Behaviour 71 (2006) 1359-1369
81. Rankin S.M., Fox K.M., and Stotsky C.E. Physiological correlates to courtship, mating, ovarian development and maternal-behavior in the ring-legged earwig. Physiological Entomology 20 (1995) 257-265
82. Rankin S.M., Palmer J.O., Larocque L., and Risser A.L. Life history characteristics of ringlegged earwig (Dermaptera: Labiduridae): emphasis on ovarian development. Annals of the Entomological Society of America 88 (1995) 887-893
83. Rankin S.M., Palmer J.O., Yagi K.J., Scott G.L., and Tobe S.S. Biosynthesis and release of juvenile hormone during the reproductive cycle of the ring-legged earwig. Comparative Biochemistry and Physiology C 110 (1995) 241-251
84. Rankin S.M., Storm S.K., Pieto D.L., and Risser A.L. Maternal behavior and clutch manipulation in the ring-legged earwig (Dermaptera: Carcinophoridae). Journal of Insect Behavior 9 (1996) 85-103
85. Rankin S.M., Chambers J., and Edwards J.P. Juvenile hormone in earwigs: roles in oogenesis, mating, and maternal behaviors. Archives of Insect Biochemistry and Physiology 35 (1997) 427-442
86. Rasa O.A.E. Biparental investment and reproductive success in a subsocial desert beetle: the role of maternal effort. Behavioral Ecology and Sociobiology 43 (1998) 105-113
87. Rasa O.A.E. Division of labour and extended parenting in a desert tenebrionid beetle. Ethology 105 (1999) 37-56
88. Rauter C.M., and Moore A.J. Do honest signalling models of offspring solicitation apply to insects?. Proceedings of the Royal Society of London, Series B 266 (1999) 1691-1696
89. Reid M.L., and Roitberg B.D. Benefits of prolonged male residence with mates and brood in pine engravers (Coleoptera, Scolytidae). Oikos 70 (1994) 140-148
90. Robinson G.E., and Vargo E.L. Juvenile hormone in adult eusocial hymenoptera: gonadotropin and behavioral pacemaker. Archives of Insect Biochemistry and Physiology 35 (1997) 559-583
91. Roth L.M., and Stay B. The occurrence of para-quinones in some arthropods, with emphasis on the quinone-secreting tracheal glands of Diploptera punctata (Blattaria). Journal of Insect Physiology 1 (1958) 305-310
92. Royle N.J., Hartley I.R., and Parker G.A. Begging for control: when are offspring solicitation behaviours honest?. Trends in Ecology & Evolution 17 (2002) 434-440
93. Royle N.J., Hartley I.R., and Parker G.A. Parental investment and family dynamics: interactions between theory and empirical tests. Population Ecology 46 (2004) 231-241
94. Ryan M.J. Sexual selection, sensory systems, and sensory exploitation. Oxford Surveys in Evolutionary Biology 7 (1990) 157-195
95. Schooley D.A., Tobe S.S., and Yagi K.J. JH8: recent progress in juvenile hormone research. Journal of Insect Physiology 51 (2005) 343
96. Schuster J.C., and Schuster L.B. The evolution of social behavior in Passalidae (Coleoptera). In: Choe J.C., and Crespi B.J. (Eds). The Evolution of Social Behavior in Insects and Arachnids (1997), Cambridge University Press, Cambridge 260-269
97. Scott M.P., and Panaitof S.C. Social stimuli affect juvenile hormone during breeding in biparental burying beetles (Silphidae: Nicrophorus). Hormones & Behavior 45 (2004) 159-167
98. Scott M.P., Trumbo S.T., Neese P.A., Bailey W.D., and Roe R.M. Changes in biosynthesis and degradation of juvenile hormone during breeding by burying beetles: a reproductive or social role?. Journal of Insect Physiology 47 (2001) 295-302
99. Sites R.W., and McPherson J.E. Life-history and laboratory rearing of Sehirus cinctus cinctus (Hemiptera, Cydnidae), with descriptions of immature stages. Annals of the Entomological Society of America 75 (1982) 210-215
100. Smiseth P.T., and Moore A.J. Does resource availability affect offspring begging and parental provisioning in a partially begging species?. Animal Behaviour 63 (2002) 577-585
101. Smiseth P.T., and Moore A.J. Signalling of hunger when offspring forage by both begging and self-feeding. Animal Behaviour 67 (2004) 1083-1088
102. Smiseth P.T., Darwell C.T., and Moore A.J. Partial begging: an empirical model for the early evolution of offspring signalling. Proceedings of the Royal Society of London, Series B 270 (2003) 1773-1777
103. Smiseth P.T., Wright J., and Kölliker M. Parent-offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics. Proceedings of the Royal Society of London, Series B 275 (2008) 1823-1830
104. Staerkle, M. & Kölliker, M. In press. Maternal food regurgitation to nymphs in earwigs (Forficula auricularia). Ethology.
105. Tallamy D.W. Insect parental care. Bioscience 34 (1984) 20-24
106. Tallamy. Egg dumping in Lace bugs (Gargaphia solni, Hemiptera, Tingidae). Behavioral Ecology and Sociobiology 17 (1985) 357-362
107. Tallamy D.W., and Brown W.P. Semelparity and the evolution of maternal care in insects. Animal Behaviour 57 (1999) 727-730
108. Tallamy D.W., and Denno R.F. Maternal care in Gargaphia solani (Hemiptera, Tingidae). Animal Behaviour 29 (1981) 771-778
109. Tallamy D.W., and Denno R.F. Life-history trade-offs in Gargaphia solani (Hemiptera, Tingidae): the cost of reproduction. Ecology 63 (1982) 616-620
110. Tallamy D.W., and Wood T.K. Convergence patterns in subsocial insects. Annual Review of Entomology 31 (1986) 369-390
111. Tillman J.A., Seybold S.J., Jurenka R.A., and Blomquist G.J. Insect pheromones: an overview of biosynthesis and endocrine regulation. Insect Biochemistry and Molecular Biology 29 (1999) 481-514
112. Trivers R.L. Parent-offspring conflict. American Zoologist 14 (1974) 249-264
113. Trumbo S.T. Parental care in invertebrates. Advances in the Study of Behavior 25 (1996) 3-51
114. Trumbo S.T. Juvenile hormone-mediated reproduction in burying beetles: from behavior to physiology. Archives of Insect Biochemistry and Physiology 35 (1997) 479-490
115. Trumbo S.T. Hormonal regulation of parental behavior in insects. In: Pfaff D.W., Arnold A.P., Etgen A.M., Fahrbach S.E., Moss R.L., and Rubin R.R. (Eds). Hormones, Brain and Behavior Vol. 3 (2002), Academic Press, New York 115-139
116. Trumbo S.T. Defending young biparentally: female risk-taking with and without a male in the burying beetle, Nicrophorus pustulatus. Behavioral Ecology and Sociobiology 61 (2007) 1717-1723
117. Vancassel M. Le développement du cycle parental de Labidura riparia. Biology of Behaviour 2 (1977) 51-64
118. Vancassel M. Plasticity and adaptive radiation of dermapteran parental behavior: results and perspectives. Advances in the Study of Behavior 14 (1984) 51-80
119. Vancassel M., and Foraste M. Importance of contacts between female and larvae in some Dermaptera. Biology of Behaviour 5 (1980) 269-280
120. Vancassel M., Foraste M., Strambi A., and Strambi C. Normal and experimentally induced changes in hormonal hemolymph titers during parental behavior of the earwig Labidura riparia. General and Comparative Endocrinology 56 (1984) 444-456
121. Vancassel M., Foraste M., Quris R., Strambi A., and Strambi C. The parental response of females Labidura riparia to young and its control. Comparative Endocrinology 6 (1987) 169-173
122. Vander Meer R.K., Breed M.D., Espelic K.E., and Winston M.L. Pheromone Communication in Social Insects (1998), West View Press, Boulder, Colorado
123. West-Eberhard M.J. Developmental Plasticity and Evolution (2003), Oxford University Press, Oxford
124. West M.J., and Alexander R.D. Sub-social behavior in a burrowing cricket Anurogryllus muticus (De Geer). Ohio Journal of Science 63 (1963) 19-24
125. Wheeler D.E. Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. American Naturalist 128 (1986) 13-34
126. Wilson E.O. Insect Societies (1971), Harvard University Press, Cambridge, Massachusetts
127. Wolf J.B., and Brodie III E.D. The coadaptation of parental and offspring characters. Evolution 52 (1998) 299-308
128. Wood T.K. Alarm behavior of brooding female Umbonia crassicornis (Homoptera Membracidae). Annals of the Entomological Society of America 69 (1976) 340-344
129. Wright J., and Leonard M.L. The Evolution of Begging, Competition, Cooperation & Communication (2002), Kluwer Academic, Dordrecht
130. Wyatt T.D. Pheromones and Animal Behaviour (2003), Cambridge University Press, Cambridge
131. Zeh D.W., and Smith R.L. Paternal investment by terrestrial arthropods. American Zoologist 25 (1985) 785-805