Skip to main content

Advertisement

Log in

Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living

  • Review
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

A central question in behavioral ecology has been why animals live in groups. Previous theories about the evolution of sociality focused on the potential benefits of decreased risk of predation, increased foraging or feeding efficiency, and mutual aid in defending resources and/or rearing offspring. This paper argues that access to mutualistic endosymbiotic microbes is an underappreciated benefit of group living and sets out to reinvigorate Troyer’s hypothesis that the need to obtain cellulolytic microbes from conspecifics influenced the evolution of social behavior in herbivores and to extend it to nonherbivores. This extension is necessary because the benefits of endosymbionts are not limited to nutrition; endosymbionts also help protect their hosts from pathogens. When hosts must obtain endosymbionts from conspecifics, they are forced to interact. Thus, complex forms of sociality may be more likely to evolve when hosts must repeatedly obtain endosymbionts from conspecifics than when endosymbionts can be obtained either directly from the environment, are vertically transmitted, or when repeated inoculations are not necessary. Observations from a variety of taxa are consistent with the ideas that individuals benefit from group living by gaining access to endosymbionts and the complexity of social behavior is associated with the mode of acquisition of endosymbionts. Ways to test this theory include (a) experiments designed to examine the effects of endosymbionts on host fitness and how endosymbionts are obtained and (b) using phylogenetic analyses to examine endosymbiont–host coevolution with the goal of determining the relationship between the mode of endosymbiont acquisition and host sociality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alexander RD (1974) The evolution of social behavior. Ann Rev Ecolog Syst 5:325–383

    Google Scholar 

  • Anderson RM, May RM (1991) Infectious diseases of humans. Oxford University Press, New York

    Google Scholar 

  • Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396

    PubMed  CAS  Google Scholar 

  • Bandi C, Sironi M, Damiani G, Magrassi L, Nalepa CA, Laudani U, Sacchi L (1995) The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc R Soc Lond B 259:293–299

    CAS  Google Scholar 

  • Baumann P, Baumann L, Clark MA, Thao ML (1998) Buchnera aphidicola: the endosymbiont of aphids. ASM News 64:203–209

    Google Scholar 

  • Bjorndal K (1980) Nutritional and grazing behavior of the green turtle, Chelonia mydas. Mar Biol 56:147–154

    CAS  Google Scholar 

  • Bjorndal K (1987) Digestive efficiency in a temperate herbivorous reptile, Gopherus polyphemus. Copeia 1987:714–720

    Google Scholar 

  • Bjorndal K (1989) Flexibility of digestive responses in two generalist herbivores, the tortoises Geochelone carbonaria and Geochelone denticulata. Oecologia 78:317–321

    Google Scholar 

  • Bjorndal K (1996) Foraging ecology and nutrition of sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 199–231

    Google Scholar 

  • Bokkenheuser V (1993) The friendly anaerobes. Clin Infect Dis 16(Suppl 4):S427–S434

    PubMed  CAS  Google Scholar 

  • Bonds MH, Keenan DC, Leidner AJ, Rohani P (2005) Higher disease prevalence can induce greater sociality: a game theoretic coevolutionary model. Evolution 59:1859–1866

    PubMed  Google Scholar 

  • Bosch I (1992) Symbiosis between bacteria and oceanic clonal sea star larvae in the western North Atlantic Ocean. Mar Biol 114:495–502

    Google Scholar 

  • Bowden TA, Mansberger AR, Lykens LE (1981) Pseudomembraneous enterocolitis: mechanisms of restoring floral homeostasis. Am Surg 4:178–183

    Google Scholar 

  • Breznak JA (1982) Intestinal microbiota of termites and xylophagus insects. Annu Rev Microbiol 36:323–343

    PubMed  CAS  Google Scholar 

  • Brigmon RL, DeRidder C (1998) Symbiotic relationship of Thiothrix spp. with an echinoderm. Appl Environ Microbiol 64:3491–3495

    PubMed  CAS  Google Scholar 

  • Brown JL (1987) Helping and comunal breeding in birds. Princeton University Press, Princeton

    Google Scholar 

  • Brunel A, Gouet P (1989) Intestinal microflora of the newborn rat as related to mammary, faecal, and vaginal staphylococci strains isolated from the dam. Can J Microbiol 35:989–993

    PubMed  CAS  Google Scholar 

  • Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Wiley, New York

    Google Scholar 

  • Burnett WJ, McKenzie JD (1997) Subcuticular bacteria from the brittle star Ophiactis balli (Echinodermata: Ophiuroidea) represent a new lineage of extracellular marine symbionts in the α subdivision of the class Proteobacteria. Appl Environ Microbiol 63:1721–1724

    PubMed  CAS  Google Scholar 

  • Cahan SH, Blumstein DT, Sundström L, Liebig J, Griffin A (2002) Social trajectories and the evolution of social behavior. Oikos 96:206–216

    Google Scholar 

  • Cannon JP, Lee TA, Bolanos JT, Danziger LH (2005) Pathogenic relevance of Lactobacillus: a retrospective review of over 200 cases. Eur J Clin Microbiol Infect Dis 24:31–40

    PubMed  CAS  Google Scholar 

  • Cary SC, Giovannoni SJ (1993) Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc Natl Acad Sci USA 90:5695–5699

    PubMed  CAS  Google Scholar 

  • Cary SC, Warren WD, Anderson E, Giovannoni SJ (1993) Identification and localization of bacterial endosymbionts in hydrothermal vent taxa with symbiont specific polymerase chain reaction amplification and in situ hybridization techniques. Mol Mar Bio Biotechnol 2:51–62

    CAS  Google Scholar 

  • Cash HL, Hooper LV (2005) Commensal bacteria shape intestinal immune system development. ASM News 71:77–83

    Google Scholar 

  • Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342

    PubMed  CAS  Google Scholar 

  • Chen D-Q, Purcell AH (1997) Occurrence and transmission of facultative endosymbionts in aphids. Curr Microbiol 34:220–225

    PubMed  CAS  Google Scholar 

  • Childress JJ, Felbeck H, Somero GN (1987) Symbiosis in the deep sea. Sci Am 256:114–120

    Article  Google Scholar 

  • Cleveland LR, Hall SR, Sanders EP, Collier J (1934) The wood-feeding roach Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem Am Acad Arts Sci 17:185–342

    Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • Cohen CR, Duerr A, Pruithithada N, Rugpao S, Hillier S, Garcia P, Nelson K (1995) Bacterial vaginosis and HIV seroprevalence among female commercial sex workers in Chiang Mai, Thailand. AIDS 9:1093–1097

    PubMed  CAS  Google Scholar 

  • Côté IM, Poulin R (1995) Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159–165

    Google Scholar 

  • Crespi BJ (1990) Subsociality and female reproductive success in a mycophagus thrips: an observational and experimental analysis. J Insect Behav 3:61–74

    Google Scholar 

  • Crespi BJ (1992) Eusociality in Australian gall thrips. Nature 359:724–726

    Google Scholar 

  • Crespi BJ, Choe JC (1997) Explanation and evolution of social systems. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 499–524

    Google Scholar 

  • Crespi BJ, Yanega D (1995) The definition of eusociality. Behav Ecol 6:109–115

    Google Scholar 

  • Currie CR (2001) A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 55:357–380

    PubMed  CAS  Google Scholar 

  • Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704

    CAS  Google Scholar 

  • Dale C, Plague GR, Wang B, Ochman H, Moran NA (2002) Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Sci USA 99:12397–12402

    PubMed  CAS  Google Scholar 

  • Daw MA, Falkiner FR (1996) Bacteriocins: nature, function and structure. Micron 27:467–479

    PubMed  CAS  Google Scholar 

  • deWaal FBM (1989) Peacemaking among primates. Cambridge University Press, Cambridge

    Google Scholar 

  • Distel DL (1998) Evolution of chemoautotrophic endosymbioses in bivalve. Bioscience 48:277–286

    Google Scholar 

  • Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676–8680

    PubMed  CAS  Google Scholar 

  • Douglas AE (1994) Symbiotic interactions. Oxford University Press, New York

    Google Scholar 

  • Duffy JE (1996) Eusociality in a coral-reef shrimp. Nature 381:512–514

    CAS  Google Scholar 

  • Dyer BD (1998) A hypothesis about the significance of symbionts as a source of protein in the evolution of eusocial mole rats. Symbiosis 24:369–384

    Google Scholar 

  • Evans JD, Armstrong T-N (2005) Inhibition of the American foulbrood bacterium, Paenibacillus larvae larvae, by bacteria isolated from honey bees. J Apic Res 44:168–171

    CAS  Google Scholar 

  • Evans TA, Wallis RJ, Elgar MA (1995) Making a meal of mother. Nature 376:299

    CAS  Google Scholar 

  • Ewald PW (1987) Transmission modes and the evolution of the parasitism–mutualism continuum. Ann N Y Acad Sci 503:295–306

    PubMed  CAS  Google Scholar 

  • Ewald PW (1994) The evolution of infectious diseases. Oxford University Press, New York

    Google Scholar 

  • Falk PG, Hooper LV, Midtvedt T, Gordon JI (1998) Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol Mol Biol Rev 62:1157–1170

    PubMed  CAS  Google Scholar 

  • Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011–2027

    PubMed  CAS  Google Scholar 

  • Felbeck H, Distel DL (1992) Prokaryotic symbionts in marine invertebrates. In: Ballows A, Trüper H, Harder W, Schleifer KH (eds) The prokaryotes. Springer, Berlin Heidelberg New York, pp 3891–3906

    Google Scholar 

  • Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436

    CAS  Google Scholar 

  • Foster KR, Wenseleers T (2006) A general model for the evolution of mutualisms. J Evol Biol 19:1283–1293

    PubMed  CAS  Google Scholar 

  • Frank SA (1995) The origin of synergistic symbiosis. J Theor Biol 176:403–410

    PubMed  CAS  Google Scholar 

  • Frank SA (1996) Host control of symbiont transmission: the separation of symbionts into germ and soma. Am Nat 148:1113–1124

    Google Scholar 

  • Frank SA (1997) Models of symbiosis. Am Nat 150:S80–S99

    PubMed  Google Scholar 

  • Frank SA (2003) Perspective: repression of competition and the evolution of cooperation. Evolution 57:693–705

    PubMed  Google Scholar 

  • Freeland WJ (1976) Pathogens and the evolution of primate sociality. Biotropica 8:12–24

    Google Scholar 

  • Freeland WJ (1979) Primate social groups as biological islands. Ecology 60:719–728

    Google Scholar 

  • Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66:365–378

    PubMed  CAS  Google Scholar 

  • Fuller R (1994) Probiotics: an overview. In: Gibson SAW (ed) Human health: the contribution of microorganisms. Springer, Berlin Heidelberg New York, pp 63–73

    Google Scholar 

  • Gil R, Latorre A, Moya A (2004) Bacterial endosymbionts of insects: insights from comparative genomics. Environ Microbiol 6:1109–1122

    PubMed  CAS  Google Scholar 

  • Gilliam M (1971) Microbial sterility of the intestinal content of the immature honey bee, Apis mellifera. Ann Entomol Soc Am 64:315–316

    Google Scholar 

  • Gilliam M, Taber S III, Lorenz BJ, Prest DB (1988) Factors affecting development of chalkbrood disease in colonies of honey bees, Apis mellifera, fed pollen contaminated with Ascosphaera apis. J Invertebr Pathol 52:314–325

    Google Scholar 

  • Gil-Turner MS, Hay ME, Fenical W (1989) Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246:116–118

    Google Scholar 

  • Gorbach SL, Chang T-W, Goldin B (1987) Successful treatment of relapsing Clostridium difficile colitis with Lactobacillus GG. Lancet 330:1519

    Google Scholar 

  • Gorbach SL, Barza M, Giuliano M, Jacobus NV (1988) Colonization resistance of the human intestinal microflora: testing the hypothesis in normal volunteers. Eur J Clin Microbiol Infect Dis 7:98–102

    PubMed  CAS  Google Scholar 

  • Graf J, Ruby EG (1998) Host-derived amino acids support the proliferation of symbiotic bacteria. Proc Natl Acad Sci USA 95:1818–1822

    PubMed  CAS  Google Scholar 

  • Grajal A, Strahl SD, Parra R, Dominguez MG, Neher A (1989) Foregut fermentation in the hoatzin, a neotropical leaf-eating bird. Science 245:1236–1238

    PubMed  CAS  Google Scholar 

  • Grandcolas P (1999) Systematics, endosymbiosis, and biogeography of Cryptocercus clevelandi and C. punctulatus (Blatteria: Polyphagidae) from North America: a phylogenetic perspective. Ann Entomol Soc Am 92:285–291

    Google Scholar 

  • Grandcolas P, Deleporte P (1996) The origin of protistan symbionts in termites and cockroaches: a phylogenetic perspective. Cladistics 12:93–98

    Google Scholar 

  • Gros O, Darrasse A, Frenkiel L, Moeza M (1996) Environmental transmission of a sulfur-oxidizing bacterial gill endosymbiont in the tropical lucinid bivalve Codakia orbicularis. Appl Environ Microbiol 62:2324–2330

    PubMed  CAS  Google Scholar 

  • Guthrie DM, Tindall AR (1968) The biology of the cockroach. Edward Arnold, London

    Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behavior. J Theor Biol 7:1–52

    PubMed  CAS  Google Scholar 

  • Hamilton WD (1990) Mate choice near or far. Am Zool 30:341–352

    Google Scholar 

  • Hamilton J, Coe M (1982) Feeding, digestion and assimilation of a population of giant tortoises (Geochelone gigantea) on Aldabra atoll. J Arid Environ 5:127–144

    Google Scholar 

  • Harder B (2002) Germs that do a body good. Sci News 161:72–74

    Google Scholar 

  • Hawes S, Hillier SL (1996) Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis 174:1048

    Google Scholar 

  • Hentges DJ (1983) Human intestinal microflora in health and disease. Academic, New York

    Google Scholar 

  • Hentges DJ (1993) The anaerobic microflora of the human body. Clin Infect Dis 16(Suppl 4):S175–S180

    PubMed  Google Scholar 

  • Herceg RJ, Peterson LR (1997) Normal flora in health and disease. In: Shulman ST, Phair JP, Peterson LR, Warren JR (eds) The biologic and clinical basis of infectious diseases. W. B. Saunders, Philadelphia, pp 5–14

    Google Scholar 

  • Herthelius M, Gorbach SL, Molloy R, Nord CE, Petterson I, Winberg J (1989) Elimination of vaginal colonization with Escherichia coli by administration of indigenous flora. Infect Immunol 57:2447–2451

    CAS  Google Scholar 

  • Hess G (1996) Disease in metapopulation models: implications for conservation. Ecology 77:1617–1632

    Google Scholar 

  • Hildemann WH (1959) A cichlid fish, Symphysodon discus with unique nurture habits. Am Nat 93:27–34

    Google Scholar 

  • Hillier S (1998) The vaginal microbial ecosystem and resistance to HIV. AIDS Res Hum Retrovir 14:S17–S21

    PubMed  Google Scholar 

  • Hillier S, Holmes KK (1999) Bacterial vaginosis. In: Holmes KK, Mardh PA, Sparling PF (eds) Sexually transmitted diseases, 3rd edn. McGraw Hill, New York, pp 563–586

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Google Scholar 

  • Hooper LV, Bry L, Falk PG, Gordon JI (1998) Host–microbial symbiosis in the mammalian intestine: exploring an internal ecosystem. Bioessays 20:336–343

    PubMed  CAS  Google Scholar 

  • Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host–microbial relationships in the intestine. Science 291:881–884

    PubMed  CAS  Google Scholar 

  • Hooper LV, Stappenbeck TS, Hong CV, Gordon JI (2003) Angiogenins: a new class of microbicial proteins involved in innate immunity. Nat Immunol 4:269–273

    PubMed  CAS  Google Scholar 

  • Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T (2006) Strict host–symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol 4:e337. DOI 10.1371/journal.pbio.0040337

    PubMed  Google Scholar 

  • Hungate RE (1966) The rumen and its microbes. Academic, New York

    Google Scholar 

  • Hunt JH, Nalepa CA (1994a) Nourishment and evolution in insect societies. Westview, Boulder

    Google Scholar 

  • Hunt JH, Nalepa CA (1994b) Nourishment, evolution and insect sociality. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview, Boulder, pp 1–19

    Google Scholar 

  • Hutchenson DP, Savage DC, Parker DS, Miles RD, Bootwalla SM (1991) Direct fed microbials in animal production. National Feed Ingredients Association, West Des Moines

    Google Scholar 

  • Iverson JB (1980) Colic modifications in iguanine lizards. J Morphol 163:79–93

    Google Scholar 

  • Iverson JB (1982) Adaptations to herbivory in iguanine lizards. In: Burghardt GM, Rand AS (eds) Iguanas of the world: their behavior, ecology, and conservation. Noyes, Park Ridge, pp 60–76

    Google Scholar 

  • Johnstone RA, Bshary R (2002) From parasitism to mutualism: partner control in asymmetric interactions. Ecol Lett 5:634–639

    Google Scholar 

  • Kandel JS, Horn MH, Van Antwerp W (1994) Volatile fatty acids in the hindguts of herbivorous fishes from temperate and tropical marine waters. J Fish Biol 45:527–529

    CAS  Google Scholar 

  • Kellner RLL (1999) What is the basis of pederin polymorphism in Paederus riparius rove beetles? The endosymbiotic hypothesis. Entomol Exp Appl 93:41–49

    CAS  Google Scholar 

  • Kelly MS, McKenzie JD (1995) Survey of the occurrence and morphology of subcuticular bacteria in shelf echinoderms from the north-east Atlantic Ocean. Mar Biol 123:741–756

    Google Scholar 

  • Kelly MS, Barker MF, McKenzie JD, Powell J (1995) The incidence and morphology of subcuticular bacteria in the echinoderm fauna of New Zealand. Biol Bull 189:91–105

    Google Scholar 

  • Kent DS, Simpson JA (1992) Eusociality in the beetle Austroplatupus incompertus. Naturwissenschaften 79:86–87

    Google Scholar 

  • Kirkendall LR, Kent DS, Raffa KA (1997) 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 JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 181–215

    Google Scholar 

  • Kitano H, Oda K (2006) Robustness trade-offs and host–microbial symbiosis in the immune system. Molec Syst Biol 2:E1–E10

    Google Scholar 

  • Klebanoff SJ, Coombs RW (1991) Virucidal effect of Lactobacillus acidophillus on human immunodeficiency virus type-1: possible role in heterosexual transmission. J Exp Med 174:289–292

    PubMed  CAS  Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

    Google Scholar 

  • Krueger DM, Gustafson RG, Cavanaugh CM (1996) Vertical transmission of chemoautotrophic symbionts in the bivalve Solemya velum (Bivalvia: Protobranchia). Biol Bull 190:195–202

    PubMed  CAS  Google Scholar 

  • Kukor JJ, Martin MM (1983) Acquisition of digestive enzymes by siricid woodwasps from a fungal symbiont. Science 220:1161–1163

    PubMed  CAS  Google Scholar 

  • Kulkarni S, Heeb P (2007) Social and sexual behaviours aid transmission of bacteria in birds. Behav Processes 74:88–92

    PubMed  Google Scholar 

  • Kullman E (1972) Evolution of social behavior in spiders (Arachneae; Eresidae and Theridiidae). Am Zool 12:419–426

    Google Scholar 

  • Kyle PD, Kyle GZ (1993) An evaluation of the role of microbial flora in the salivary transfer technique for hand-rearing Chimney Swifts. Wildl Rehabil 8:65–71

    Google Scholar 

  • Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London

    Google Scholar 

  • Lamb RJ (1976) Parental behavior in the Dermaptera with special reference to Forficula auricularia (Dermaptera: Forficulidae). Can Entomol 108:609–619

    Google Scholar 

  • Law R (1985) Evolution in a mutualistic environment. In: Boucher DH (ed) The biology of mutualism. Oxford University Press, New York, pp 145–170

    Google Scholar 

  • Lee K-H, Ruby EG (1994) Effect of squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl Environ Microbiol 60:1565–1571

    PubMed  CAS  Google Scholar 

  • Lesser MP, Blakemore RP (1990) Description of a novel symbiotic bacterium from the brittle star Amphipholis squamata. Appl Environ Microbiol 56:2436–2440

    PubMed  CAS  Google Scholar 

  • Levine ND (1972) Relationship between certain protozoa and other animals. In: Chen TT (ed) Research in protozoology, vol 4. Pergamon, New York, pp 291–350

    Google Scholar 

  • Lewis RW (1970) Fish cutaneous mucus: a new source of skin surface lipids. Lipids 5:947–949

    CAS  Google Scholar 

  • Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Human gut microbes associated with obesity. Nature 444:1022–1023

    PubMed  CAS  Google Scholar 

  • Ligon JD (1999) The evolution of avian breeding systems. Oxford University Press, New York

    Google Scholar 

  • Lin N, Michener CD (1972) Evolution of sociality in insects. Q Rev Biol 47:131–159

    Google Scholar 

  • Little TJ, Kraaijeveld AR (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol Evol 19:58–60

    PubMed  Google Scholar 

  • Lo N, Bandi C, Watanabe H, Nalepa CA, Beninati T (2003) Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol Biol Evol 20:907–913

    PubMed  CAS  Google Scholar 

  • Loehle C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76:326–335

    Google Scholar 

  • Lombardo MP, Thorpe PA, Power HW (1999) The beneficial sexually transmitted microbe (bSTM) hypothesis of avian copulation. Behav Ecol 10:333–337

    Google Scholar 

  • Lubin YD (1982) Does the social spider Achaearanea wau (Theridiidae) feed its young? Z Tierpsychol 60:127–134

    Google Scholar 

  • Lucas FS, Heeb P (2005) Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit P. caeruleus nestlings. J Avian Biol 36:510–516

    Google Scholar 

  • Lynn DH, Struder-Kypke M (2002) Phylogenetic position of Licnophora, Lechriophyta, and Schizocaryum, three unusual ciliates (Phylum Ciliophora) endosymbiotic in echinoderms (Phylum Echinodermata). J Eukaryot Microbiol 49:460–468

    PubMed  Google Scholar 

  • Macpherson AJ, Harris NL (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4:478–485

    PubMed  CAS  Google Scholar 

  • Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New Haven

    Google Scholar 

  • Margulis L (1993) Symbiosis in cell evolution, 2nd edn. Freeman, San Francisco

    Google Scholar 

  • Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation. MIT Press, Cambridge

    Google Scholar 

  • Marinier SL, Alexander AJ (1995) Coprophagy as an avenue for foals to the domestic horse to learn food preferences from their dams. J Theor Biol 173:121–124

    Google Scholar 

  • Martin MM (1992) The evolution of insect–fungus associations from contact to stable symbiosis. Am Zool 32:593–605

    Google Scholar 

  • Mazmanian SK, Kasper DL (2006) The love–hate relationship between bacterial polysaccharides and the host immune system. Nat Rev Immunol 6:849–858

    PubMed  CAS  Google Scholar 

  • McBee RH (1977) Fermentation in the hindgut. In: Clarke RTJ, Bauchop T (eds) Microbial ecology of the gut. Academic, London, pp 185–222

    Google Scholar 

  • McFall-Ngai MJ (1998) The development of cooperative associations between animals and bacteria: establishing détente among domains. Am Zool 38:593–608

    CAS  Google Scholar 

  • McFall-Ngai MJ (1999) Consequences of evolving with bacterial symbionts: insights from the squid–vibrio association. Ann Rev Ecolog Syst 30:235–256

    Google Scholar 

  • McNab JM (1973) The avian caeca: a review. World Poult Sci J 29:251–263

    Google Scholar 

  • Mills TK, Lombardo MP, Thorpe PA (1999) Microbial colonization of the cloacae of nestling Tree Swallows. Auk 116:947–956

    Google Scholar 

  • Moore J (1995) The behavior of parasitized animals. Bioscience 45:91–96

    Google Scholar 

  • Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford

    Google Scholar 

  • Moran NA (2001) The coevolution of bacterial endosymbionts and phloem-feeding insects. Ann Mo Bot Gard 88:35–44

    Google Scholar 

  • Moran NA (2006) Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci USA 103:12803–12806

    PubMed  CAS  Google Scholar 

  • Moran NA, Baumann P (2000) Bacterial endosymbionts in animals. Curr Opin Microbiol 3:270–275

    PubMed  CAS  Google Scholar 

  • Moran NA, Wernergreen JJ (2000) Are mutualism and parasitism irreversible evolutionary alternatives for endosymbiotic bacteria? Insights from molecular phylogenies and genomics. Trends Ecol Evol 15:321–326

    PubMed  Google Scholar 

  • Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H (2005) The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA 102:16919–16926

    PubMed  CAS  Google Scholar 

  • Moret Y, Schmid-Hempel P (2001) Immune defence in bumble-bee offspring. Nature 414:506

    PubMed  CAS  Google Scholar 

  • Morton ES (1978) Avian arboreal folivores: why not? In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institute, Washington, DC, pp 123–130

    Google Scholar 

  • Moyle PB, Cech JJ Jr (2000) Fishes: and introduction to ichthyology. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Nagy KA (1977) Cellulose digestion and nutrient assimilation in Sauromalus obesus, a plant-eating lizard. Copeia 1977:355–362

    Google Scholar 

  • Nalepa CA (1984) Colony composition, protozoan transfer and some life history characteristics of the woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae). Behav Ecol Sociobiol 14:273–279

    Google Scholar 

  • Nalepa CA (1991) Ancestral transfer of symbionts between cockroaches and termites: an unlikely scenario. Proc R Soc Lond B 246:185–189

    CAS  Google Scholar 

  • Nalepa CA (1994) Nourishment and the origin of termite eusociality. In: Hunt J, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview Press, Boulder, pp 57–104

    Google Scholar 

  • Nalepa CA, Bell WJ (1997) Postovulation parental investment and parental care in cockroaches. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 26–51

    Google Scholar 

  • Nalepa CA, Bignell DE, Bandi C (2001) Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera. Insectes Soc 48:194–201

    Google Scholar 

  • Netherwood T, Gilbert HJ, Parker DS, O’Donnell AG (1999) Probiotics shown to change bacterial community structure in the avian gastrointestinal tract. Appl Environ Microbiol 65:5134–5138

    PubMed  CAS  Google Scholar 

  • Newman J (1995) How breast milk protects newborns. Sci Am 273:76–79

    Article  PubMed  CAS  Google Scholar 

  • Noakes DLG (1979) Parent-touching behavior by young fishes: incidence, function and causation. Environ Biol Fisches 4:389–400

    Google Scholar 

  • Nunn CL, Altizer S (2006) Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Nurmi E, Rantala M (1973) New aspects of Salmonella infection in broiler production. Science 241:210–211

    CAS  Google Scholar 

  • Oliveira MR, Tafuri WL, Afonso LCC, Oliveira MAP, Nicoli JR, Vieira EC, Scott P, Melo MN, Vieira LQ (2005) Germ-free mice produce high levels of interferon-gamma in response to infection with Leishamania major but fail to heal lesions. Parasitology 131:477–488

    PubMed  CAS  Google Scholar 

  • Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102:12795–12800

    PubMed  CAS  Google Scholar 

  • Oppenheimer JR (1970) Mouth brooding in fishes. Anim Behav 18:493–503

    PubMed  CAS  Google Scholar 

  • Persky SE, Brandt LJ (2000) Treatment of recurrent Clostridium difficile-associated diarrhea by administration of donated stool directly through a colonoscope. Am J Gastroenterol 95:3283

    PubMed  CAS  Google Scholar 

  • Porter A (1957) Morphology and affinities of entozoa and endophyta of the naked mole-rat. Proc Zool Soc Lond 128:515–517

    Google Scholar 

  • Prejs A, Blaszczyk M (1977) Relationships between food and cellulase activity in freshwater fishes. J Fish Biol 11:447–452

    CAS  Google Scholar 

  • Pybus V, Onderdonk A (1999) Microbial interactions in the vaginal ecosystem, with emphasis on the pathogenesis of bacterial vaginosis. Microbes Infect 1:285–292

    PubMed  CAS  Google Scholar 

  • Radl RC, Linsenmair KE (1991) Maternal behaviour and nest recognition in the subsocial earwig Labidura riparia Pallas (Dermaptera:Labiduridae). Ethology 89:287–296

    Article  Google Scholar 

  • Rankin SM, Storm SK, Pieto DL, Risser AL (1996) Maternal behavior and clutch manipulation in the ring-legged earwig (Dermaptera: Carcinophoridae). J Insect Behav 9:85–103

    Google Scholar 

  • Rimmer DW, Wiebe WJ (1987) Fermentative microbial digestion in herbivorous fishes. J Fish Biol 31:229–236

    Google Scholar 

  • Rogers KL (1985) Possible physiological and behavioral adaptations of herbivorous dinosaurs. J Vertebr Paleontol 5:371–372

    Article  Google Scholar 

  • Roulin A, Heeb P (1999) The immunological function of allosuckling. Ecol Lett 2:319–324

    Google Scholar 

  • Ruby EG, Lee K-H (1998) The Vibrio fischeriEuprymna scolopes light organ association: current ecological paradigms. Appl Environ Microbiol 64:805–812

    PubMed  CAS  Google Scholar 

  • Ruby EG, Henderson B, McFall-Ngai MJ (2004) We get by with a little help from our (little) friends. Science 303:1305–1307

    PubMed  CAS  Google Scholar 

  • Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79:135–160

    PubMed  Google Scholar 

  • Sadd BM, Kleinlogel Y, Schmid-Hempel R, Schmid-Hempel P (2005) Trans-generational immune priming in a social insect. Biol Lett 1:386–388

    PubMed  Google Scholar 

  • Saffo MB (1992) Invertebrates in endosymbiotic associations. Am Zool 32:557–565

    Google Scholar 

  • Saffo MB (2001) Mutualistic symbioses. In: Encyclopedia of Life Sciences. Macmillan, New York

    Google Scholar 

  • Sandström JP, Russell JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10:217–228

    PubMed  Google Scholar 

  • Sauer C, Stackebrandt E, Gadau J, Hölldobler B, Gross R (2000) Systematic relationships and cospeciation of bacterial endosymbionts and their carpenter ant host species: proposal of the new taxon Candidatus Blochmannia gen. nov. Int J Syst Evol Microbiol 50:1877–1886

    PubMed  CAS  Google Scholar 

  • Savage DC (1969) Microbial interactions between indigenous yeast and lactobacilli in the rodent stomach. J Bacteriol 98:1278

    PubMed  CAS  Google Scholar 

  • Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107–133

    PubMed  CAS  Google Scholar 

  • Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781

    PubMed  CAS  Google Scholar 

  • Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton

    Google Scholar 

  • Schröder D, Deppisch H, Obermayer M, Krohne G, Stackebrandt E, Hölldobler B, Goebel W, Gross R (1996) Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol Microbiol 21:479–489

    PubMed  Google Scholar 

  • Schuster JC, Schuster LB (1997) The evolution of social behavior in Passalidae (Coleoptera). In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 260–269

    Google Scholar 

  • Scott MP (1990) Brood guarding and the evolution of male parental care in burying beetles. Behav Ecol Sociobiol 26:31–39

    Google Scholar 

  • Scott MP, Traniello JFA (1990) Behavioural and ecological correlates of male and female parental care and reproductive success in burying beetles (Necrophorus spp.). Anim Behav 39:274–283

    Google Scholar 

  • Sears CL (2005) A dynamic partnership: celebrating our gut flora. Anaerobe 11:247–251

    PubMed  Google Scholar 

  • Seibt U, Wickler W (1987) Gerontophagy versus cannibalism in the social spiders Stegodyphus mimosarum Pavesi and Stegodyphus dumicola Pocock. Anim Behav 35:1903–1904

    Google Scholar 

  • Sewankambo N, Gray RH, Wawer MJ, Paxton L, McNaim D, Wabwire-Mangen F, Serwadda D, Li C, Kiwanuka N, Hillier SL, Rabe L, Gaydos CA, Quinn TC, Konde-Lule J (1997) HIV-1 infection associated with abnormal vaginal flora morphology and bacterial vaginosis. Lancet 350:546–550

    PubMed  CAS  Google Scholar 

  • Shaw E, Aronson LR (1954) Oral incubation in Tilapia macrocephala. Bull Am Mus Nat Hist 103:375–416

    Google Scholar 

  • Shellman-Reeve JS (1997) The spectrum of eusociality in termites. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, New York, pp 52–93

    Google Scholar 

  • Sherman PW, Jarvis JUM, Alexander RD (1991) The biology of the naked mole rat. Princeton University Press, Princeton

    Google Scholar 

  • Shine R (1988a) Constraints on reproductive investment: a comparison between aquatic and terrestrial snakes. Evolution 42:17–27

    Google Scholar 

  • Shine R (1988b) Parental care in reptiles. In: Gans C (ed) Biology of the reptilia, vol 16. Liss, New York, pp 276–329

    Google Scholar 

  • Sims W (1964) A pathogenic Lactobacillus. J Pathol Bacteriol 87:99–105

    PubMed  CAS  Google Scholar 

  • Smith HW (1965) Observations on the flora of the alimentary tract of animals and factors affecting its composition. J Pathol Bacteriol 89:95–122

    PubMed  CAS  Google Scholar 

  • Smith HG, Crabb WE (1961) The faecal bacterial flora of animals and man: its development in the young. J Pathol Bacteriol 82:53–66

    Google Scholar 

  • Smith DC, Douglas AE (1987) The biology of symbiosis. Edward Arnold, London

    Google Scholar 

  • Smith TB, Wahl DH, Mackie RI (1996) Volatile fatty acids and anaerobic fermentation in temperate piscivorous and omnivorous freshwater fish. J Fish Biol 48:429–441

    Google Scholar 

  • Soave O, Brand D (1991) Coprophagy in animals: a review. Cornell Vet 81:357–364

    PubMed  CAS  Google Scholar 

  • Sorvari R, Naukkarinen A, Sorvari TE (1977) Anal sucking-like movements in the chicken and chick embryo followed by the transportation of environmental material to the bursa of Fabricius, caeca, and caecal tonsils. Poultry Sci 56:1426–1429

    CAS  Google Scholar 

  • Stamm WE, Holmes KK (1989) Bacterial vaginosis—an ecologic mystery. Ann Intern Med 111:551–553

    Google Scholar 

  • Stappenbeck TS, Hooper LV, Gordon JI (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA 99:15451–15455

    PubMed  CAS  Google Scholar 

  • Stickney RR, Shumway SE (1974) Occurrence of cellulase activity in the stomachs of fishes. J Fish Biol 6:779–790

    CAS  Google Scholar 

  • Sullivan A, Nord CE (2005) Probiotics and gastrointestinal diseases. J Intern Med 257:78–92

    PubMed  CAS  Google Scholar 

  • Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32:1236–1252

    Google Scholar 

  • Taborsky M (1987) Cooperative behaviour in fish: coalitions, kin groups and reciprocity. In: Itô Y, Brown JL, Kikkawa J (eds) Animal societies: theories and facts. Japan Scientific Societies Press, Tokyo, pp 229–237

    Google Scholar 

  • Taha TE, Gray RH, Kumwenda NI, Hoover DR, Mtimavalye LAR, Liomba GN, Chiphangwi JD, Dallabetta GA, Mitotta PG (1999) HIV infection and disturbances of vaginal flora during pregnancy. J Acquir Immune Defic Syndr Human Retrovirol 20:52–59

    CAS  Google Scholar 

  • Tallamy DW (1994) Nourishment and the evolution of paternal investment in subsocial arthropods. In: Hunt JH, Nalepa CA (eds) Nourishment and evolution in insect societies. Westview Press, Boulder, pp 21–55

    Google Scholar 

  • Tannock GW (1990) The microecology of lactobacilli inhabiting the gastrointestinal tract. Adv Microb Ecol 11:147–171

    Google Scholar 

  • Tannock GW (1994) The acquisition of the normal microflora of the gastrointestinal tract. In: Gibson SAW (ed) Human health: the contribution of microorganisms. Springer, Berlin Heidelberg New York, pp 1–16

    Google Scholar 

  • Tannock GW (1995) Normal microflora: an introduction to the microbes inhabiting the human body. Chapman & Hall, New York

    Google Scholar 

  • Thorne BL (1990) A case for ancestral transfer of symbionts between cockroaches and termites. Proc R Soc Lond B 241:37–41

    CAS  Google Scholar 

  • Thorne BL (1991) Ancestral transfer of symbionts between cockroaches and termites: an alternative hypothesis. Proc R Soc Lond B 246:191–195

    CAS  Google Scholar 

  • Timmins CJ (1995) Parental behaviour and early development of Lesnei’s earwig Forficula lesnei (Finot) (Dermaptera: Forficulidae). Entomologist 114:123–127

    Google Scholar 

  • Topoff H (1972) Theoretical issues concerning the evolution and development of behavior in social insects. Am Zool 12:385–394

    Google Scholar 

  • Traniello JFA, Rosengaus RB, Savoie K (2002) The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc Natl Acad Sci USA 99:6838–6842

    PubMed  CAS  Google Scholar 

  • Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57

    Google Scholar 

  • Trivers RL (1985) Social evolution. Benjamin/Cummins, Menlo Park

    Google Scholar 

  • Troyer K (1982) Transfer of fermentative microbes between generations in a herbivorous lizard. Science 216:540–542

    PubMed  CAS  Google Scholar 

  • Troyer K (1984a) Behavioral acquisition of the hindgut fermentation system of hatchling Iguana iguana. Behav Ecol Sociobiol 14:189–193

    Google Scholar 

  • Troyer K (1984b) Microbes, herbivory and the evolution of social behavior. J Theor Biol 106:157–169

    Google Scholar 

  • Troyer K (1984c) Structure and function of the digestive tract of an herbivorous lizard Iguana iguana. Physiol Zool 57:1–8

    Google Scholar 

  • Troyer K (1991) Role of microbial cellulose degradation in reptile nutrition. In: Haigler CH, Weimer PJ (eds) Biosynthesis and biodegradation of cellulose. Marcel Dekker, New York, pp 311–325

    Google Scholar 

  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031

    PubMed  Google Scholar 

  • van der Waaij D (1989) The ecology of the human intestine and its consequences for overgrowth by pathogens such as Clostridium difficile. Annu Rev Microbiol 43:69–87

    Article  PubMed  Google Scholar 

  • Visick KL, Foster J, Doino J, McFall-Ngai MJ, Ruby EG (2000) Vibrio fischeri lux genes play an important role in colonization of the host light organ. J Bacteriol 182:4578–4586

    PubMed  CAS  Google Scholar 

  • Wagner DM, Warner T, Roberts L, Farmer J, Balish E (1997) Colonization of congenitally immunodeficient mice with probiotic bacteria. Infect Immunol 65:3345–3351

    CAS  Google Scholar 

  • Walker CW, Lesser MP (1989) Nutrition and development of brooded embryos in the brittle star Amphipholis squamata: do endosymbiotic bacteria play a role? Mar Biol 103:519–530

    Google Scholar 

  • Watanabe H, Noda N, Toduka G, Lo N (1998) A cellulase gene of termite origin. Nature 394:330–331

    PubMed  CAS  Google Scholar 

  • Werner DI, Baker EM, Gonzales EC, Sosa IR (1987) Kinship recognition and grouping in hatchling green iguanas. Behav Ecol Sociobiol 21:83–89

    Google Scholar 

  • West-Eberhard MJ (1987) Flexible strategy and social evolution. In: Ito Y, Brown JL, Kikkawa J (eds) Animal societies: theories and facts. Japan Scientific Societies Press, Tokyo, pp 35–51

    Google Scholar 

  • Wheeler WM (1918) A study of some ant larvae, with a consideration of the origin and meaning of the social habit among insects. Proc Am Philos Soc 57:293–343

    Google Scholar 

  • Wheeler WM (1928) The social insects, their origin and evolution. Harcourt Brace, New York

    Google Scholar 

  • Wheeler WM (1930) Societal evolution. In: Cowdry EV (ed) Human biology and racial welfare. Hoeber, New York, pp 139–155

    Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Wilson EO (1975) Sociobiology. Harvard University Press, Cambridge

    Google Scholar 

  • Wilson K, Knell R, Boots M, Koch-Osborne J (2003) Group living and investment in immune defence: an interspecific analysis. J Anim Ecol 72:133–143

    Google Scholar 

  • Wood M (1998) Microbes help bees battle chalkbrood. Agric Res 46:16–17

    Google Scholar 

  • Woyke T, Teeling H, Ivanonva NN, Huntemann M, Richter M, Gloeckner FO, Boffelli D, Anderson IJ, Barry KW, Shapiro HJ, Szeto E, Kyrpides NC, Mussman M, Amann R, Bergin C, Ruehland C, Rubin EM, Dubilier N (2006) Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443:950–955

    PubMed  CAS  Google Scholar 

  • Young CM, Vázquez E, Metaxas A, Tyler PA (1996) Embryology of vestimentiferan tube worms from deep-sea methane/sulphide seeps. Science 381:514–516

    CAS  Google Scholar 

  • Zug GR, Vitt LJ, Cladwell JP (2001) Herpetology, 2nd edn. Academic, New York

    Google Scholar 

Download references

Acknowledgements

B. J. Crespi, S. A. Frank, P. Heeb, H. W. Power, P. A. Thorpe, and anonymous reviewers provided useful comments on early versions of the manuscript. I thank P. Abbot, B. J. Crespi, D. Lynn, M. J. McFall-Nagi, and M. M. Martin for natural history information and P. Heeb and several anonymous reviewers for pointing me in the direction of some useful references. I was supported by a sabbatical leave, funds from the Research and Development Committee, and the Department of Biology at Grand Valley State University during the writing of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael P. Lombardo.

Additional information

Communicated by A. Cockburn

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lombardo, M.P. Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living. Behav Ecol Sociobiol 62, 479–497 (2008). https://doi.org/10.1007/s00265-007-0428-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-007-0428-9

Keywords

Navigation