Skip to main content

Social Behavior in Naked Mole-Rats: Individual Differences in Phenotype and Proximate Mechanisms of Mammalian Eusociality

  • Chapter
  • First Online:
The Extraordinary Biology of the Naked Mole-Rat

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1319))

Abstract

Naked mole-rats (Heterocephalus glaber) are small rodents native to east Africa, living in subterranean colonies of up to 300 individuals. Within each colony, reproduction is restricted to a single breeding female and 1–3 breeding males; all other colony members are reproductively suppressed and socially subordinate unless removed from the suppressive cues of the colony. Due to their striking reproductive skew, naked mole-rats are often considered eusocial mammals. Consistent with this idea, there are behavioral specializations and at least some evidence for morphological distinctions within and between the breeding and non-breeding members of the colony. Importantly, naked mole-rats show plasticity in their behavioral phenotype whereby changes in the social environment influence expression of both type and amount of social behavior. Thus, naked mole-rats provide the opportunity to examine the proximate mechanisms controlling individual differences in social behavior, shedding light on how mammals live in complex social groups.

figure a

Photo Credit: Gil Wizen

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allard MW, Honeycutt RL (1992) Nucleotide sequence variation in the mitochondrial 12S rRNA gene and the phylogeny of African mole-rats (Rodentia: Bathyergidae). Mol Biol Evol 9:27–40

    CAS  PubMed  Google Scholar 

  • Barker AJ, Koch U, Lewin GR, Pyott SJ (2021) Hearing and vocalizations in the naked mole-rat. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 157–195

    Google Scholar 

  • Beery AK, Bicks L, Mooney SJ, Goodwin NL, Holmes MM (2016) Sex, social status, and CRF receptor densities in naked mole-rats. J Comp Neurol 524:228–243

    Article  CAS  Google Scholar 

  • Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46(1):413e440

    Article  Google Scholar 

  • Blecher AS, Bennett NC, Medger K, Hagenah N, Ganswindt A, Oosthuizen MK (2020) Effect of colony disruption and social isolation on naked mole-rat endocrine correlates. Gen Comp Endocrinol 295:113520

    Article  CAS  Google Scholar 

  • Braude SH (1991) Which naked mole-rats volcano? In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 185–194

    Google Scholar 

  • Braude S (2000) Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating. Behav Ecol 11:7–12

    Article  Google Scholar 

  • Braude S, Ciszek D, Berg NE, Shefferly N (2001) The ontogeny and distribution of countershading in colonies of the naked mole-rat (Heterocephalus glaber). J Zool Lond 253:351–357

    Google Scholar 

  • Braude S, Holtze S, Hildebrandt T, Koch R (2020) Naked mole-rats do not disperse or deliver pups in correlation with moon phase. Afr J Ecol 00:1–4

    Google Scholar 

  • Brett RA (1991) The population structure of naked mole-rat colonies. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 97–136

    Google Scholar 

  • Buffenstein R, Craft W (2021) The idiosyncratic physiological traits of the naked mole-rat; a resilient animal model of aging, longevity, and healthspan. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 221–254

    Google Scholar 

  • Clarke FM, Faulkes CG (1997) Dominance and queen succession is captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc Roy Soc B 264(1384):993–1000

    Google Scholar 

  • Clarke FM, Faulkes CG (1998) Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat, Heterocephalus glaber. Proc Roy Soc B 265:1391–1399

    Google Scholar 

  • Clarke FM, Faulkes CG (1999) Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber. Proc Roy Soc B 266(1432):1995–2002

    Google Scholar 

  • Clarke FM, Faulkes CG (2001) Intracolony aggression in the eusocial naked mole-rat, Heterocephalus glaber. Anim Behav 61:311–324

    Google Scholar 

  • Coen CW, Bennett N, Holmes MM, Faulkes CG (2021) Neuropeptidergic and neuroendocrine systems underlying eusociality and the concomitant social regulation of reproduction in naked mole-rats: a comparative approach. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 59–103

    Google Scholar 

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

    Article  Google Scholar 

  • Dengler-Crish CM, Catania KC (2007) Phenotypic plasticity in female naked mole-rats after removal from reproductive suppression. J Exp Biol 210:4351–4358

    Article  Google Scholar 

  • Dengler-Crish CM, Catania KC (2009) Cessation of reproduction-related spine elongation after multiple breeding cycles in female naked mole-rats. Anat Rec 292(1):131–137

    Article  Google Scholar 

  • Dennis JC, Stilwell NK, Smith TD, Park TJ, Bhatnagar KP, Morrison EE (2020) Is the mole rat vomeronasal organ functional? Anat Rec 303:318–329

    Article  Google Scholar 

  • Edwards PD, Mooney SJ, Bosson CO, Toor I, Palme R, Holmes MM, Boonstra R (2020) The stress of being alone: removal from the colony, but not social subordination, increases fecal cortisol metabolite levels in eusocial naked mole-rats. Horm Behav 121:104720

    Article  CAS  Google Scholar 

  • Faulkes CG, Abbott DH (1993) Evidence that primer pheromones do not cause social suppression of reproduction in male and female naked mole-rats (Heterocephalus glaber). J Reprod Fertil 99:225–230

    Google Scholar 

  • Faulkes CG, Bennett NC (2021) Social evolution in African mole-rats – a comparative overview. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 1–33

    Google Scholar 

  • Faykoo-Martinez M, Mooney SJ, Holmes MM (2018) Oxytocin manipulation alters neural activity in response to social stimuli in eusocial naked mole-rats. Front Behav Neurosci 12:272

    Article  CAS  Google Scholar 

  • Finn KT, Parker DM, Bennett NC, Zöttl M (2018) Contrasts in body size and growth suggest that high population density results in faster pace of life in Damaraland mole-rats (Fukomys damarensis). Can J Zool 96:920–927

    Google Scholar 

  • Gilbert JD, Rossiter SJ, Faulkes CG (2020) The relationship between individual phenotype and the division of labour in naked mole-rats: it’s complicated. Peer J 8:e9891

    Google Scholar 

  • Goldman SL, Forger NG, Goldman BD (2006) Influence of gonadal sex hormones on behavioral components of the reproductive hierarchy in naked mole-rats. Horm Behav 50:77–84

    Article  CAS  Google Scholar 

  • Hathaway GA, Faykoo-Martinez M, Peragine DE, Mooney SJ, Holmes MM (2016) Subcaste differences in neural activation suggest a prosocial role for oxytocin in eusocial naked mole-rats. Horm Behav 79:1–7

    Article  CAS  Google Scholar 

  • Henry EC, Dengler-Crish CM, Catania KC (2007) Growing out of a caste--reproduction and the making of the queen mole-rat. J Exp Biol 210:261–268

    Article  Google Scholar 

  • Hetling JR, Baig-Silva MS, Comer CM, Pardue MT, Samaan DY, Qtaishat NM, Pepperberg DR, Park TJ (2005) Features of visual function in the naked mole-rat Heterocephalus glaber. J Comp Physiol A 191:317–330

    Google Scholar 

  • Hochberg ME, Noble RJ, Braude S (2016) A hypothesis to explain cancers in confined colonies of naked mole-rats. Biorxiv. https://doi.org/10.1101/079012

  • Holmes MM, Goldman BD, Goldman SL, Seney ML, Forger NG (2009) Neuroendocrinology and sexual differentiation in eusocial mammals. Front Neuroendocrinol 30(4):519–33

    Google Scholar 

  • Jacobs DS, Jarvis JUM (1996) No evidence for the work-conflict hypothesis in the eusocial naked mole-rat (Heterocephalus glaber). Behav Ecol Sociobiol 39:401–409

    Google Scholar 

  • Jarvis JUM (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212:571–573

    Article  CAS  Google Scholar 

  • Jarvis JUM (1991) Reproduction of naked mole-rats. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 384–425

    Google Scholar 

  • Jarvis JUM, Bennett NC (1993) Eusociality has evolved independently in two genera of bathyergid mole-rats—but occurs in no other subterranean mammal. Behav Ecol Sociobiol 33:253–260

    Article  Google Scholar 

  • Jarvis JUM, O’Riain J, McDaid E (1991) Growth and factors affecting body size in naked mole-rats. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Bology of the Naked Mole-Rat. Princeton University Press, Princeton, p 358–383

    Google Scholar 

  • Judd TM, Sherman PW (1996) Naked mole-rats recruit colony mates to food sources. Anim Behav 52(5):957–969

    Article  Google Scholar 

  • Kalamatianos T, Faulkes CG, Oosthuizen MK, Poorun R, Bennett NC, Coen CW (2010) Telencephalic binding sites for oxytocin and social organization: a comparative study of eusocial naked mole-rats and solitary cape mole-rats. J Comp Neurol 518(10):1792–1813

    Article  CAS  Google Scholar 

  • Kelley JB, Carter SN, Goldman BD, Goldman S, Freeman DA (2019) Mechanism for establishing and maintaining the reproductive hierarchy in a eusocial mammal, the Damaraland mole-rat. Anim Behav 158:193e200

    Article  Google Scholar 

  • Kutsukake N, Inada M, Sakamoto SH, Okanoya K (2012) A distinct role of the queen in coordinated workload and soil distribution in eusocial naked mole-rats. PLoS One 7(9):e44584

    Article  CAS  Google Scholar 

  • Kutsukake N, Inada M, Sakamoto SH, Okanoya K (2019) Behavioural interference among eusocial naked mole-rats during work. J Ethol 37:101–109

    Google Scholar 

  • Lacey EA, Sherman PW (1991) Social organization of naked mole-rat colonies: evidence for divisions of labor. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 275–336

    Google Scholar 

  • Lacey EA, Alexander RD, Braude SH, Sherman PW, Jarvis JUM (1991) An ethogram for the naked mole-rat: nonvocal behaviors. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 209–242

    Google Scholar 

  • Lewin GR, Smith ESJ, Reznick J, Debus K, Barker A, Park TJ (2021) The somatosensory world of the African naked mole-rat. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 197–220

    Google Scholar 

  • Lewis KN, Buffenstein R (2016) Chapter 6: the naked mole-rat: a resilient rodent model of aging, longevity, and healthspan. In: Kaeberlein MR, Martin GM (eds) Handbook of the Biology of Aging, 8th edn. Elsevier, pp 179–204

    Google Scholar 

  • Medger K, Bennett NC, Ganswindt SB, Ganswindt A, Hart DW (2019) Changes in prolactin, cortisol and testosterone concentrations during queen succession in a colony of naked mole-rats (Heterocephalus glaber): a case study. Sci Nat 106:26

    Google Scholar 

  • Mongillo DL, Kosyachkova EA, Nguyen TM, Holmes MM (2013) Differential effects of chronic fluoxetine on the behavior of dominant and subordinate naked mole-rats. Behav Brain Res 258C:119–126

    Google Scholar 

  • Mooney SJ, Holmes MM (2013) Social condition and oxytocin neuron number in the hypothalamus of naked mole-rats (Heterocephalus glaber). Neuroscience 230:56–61

    Google Scholar 

  • Mooney SJ, Douglas NR, Holmes MM (2014) Peripheral administration of oxytocin increases social affiliation in the naked mole-rat (Heterocephalus glaber). Horm Behav 65(4):380–385

    Google Scholar 

  • Mooney SJ, Filice DCS, Douglas NR, Holmes MM (2015a) Task specialization and task-switching in eusocial mammals. Anim Behav 109:227–233

    Article  Google Scholar 

  • Mooney SJ, Coen CW, Holmes MM, Beery AK (2015b) Region specific associations of sex and social status on oxytocin receptor density in the brains of eusocial rodents. Neuroscience 303:261–269

    Article  CAS  Google Scholar 

  • Mooney SJ, Forger NG, Holmes MM (2021) Adult neural plasticity in naked mole-rats: implications of fossoriality, longevity and sociality on the brain’s capacity for change. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 105–135

    Google Scholar 

  • O’Riain MJ, Braude S (2001) Inbreeding versus outbreeding in captive and wild populations of naked mole-rats. In: Clobert J, Danchin E, Dhondt A, Nichols J (eds) Dispersal. Oxford University Press, Oxford, pp 143–154

    Google Scholar 

  • O’Riain MJ, Jarvis JUM (1997) Colony member recognition and xenophobia in the naked mole-rat. Anim Behav 53:487–498

    Article  Google Scholar 

  • O’Riain MJ, Jarvis JUM (1998) The dynamics of growth in naked mole-rats: the effects of litter order and changes in social structure. J Zool 246:49–60

    Article  Google Scholar 

  • O’Riain MJ, Jarvis JUM, Faulkes CG (1996) A dispersive morph in the naked mole-rat. Nature 380(6575):619–621

    Article  Google Scholar 

  • O’Riain MJ, Jarvis JUM, Alexander R, Buffenstein R, Peeters C (2000) Morphological castes in a vertebrate. Proc Natl Acad Sci USA 97(24):13194–13197

    Article  Google Scholar 

  • Pepper JW, Braude SH, Lacey EA, Sherman PW (1991) Vocalizations of the naked mole-rat. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 243–274

    Google Scholar 

  • Reeve HK (1992) Queen activation of lazy workers in colonies if the eusocial naked mole-rat. Nature 358:147–149

    Article  CAS  Google Scholar 

  • Reeve HK, Sherman PW (1991) Intracolonial aggression and nepotism by the breeding female naked mole-rat. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The Biology of the Naked Mole-Rat. Princeton University Press, Princeton, pp 337–357

    Google Scholar 

  • Riccio AP, Goldman BD (2000) Circadian rhythms of locomotor activity in naked mole-rats (Heterocephalus glaber). Physiol Behav 71:1–13

    Google Scholar 

  • Ruby JG, Smith M, Buffenstein R (2018) Naked mole-rat mortality rates defy Gompertzian laws by not increasing with age. eLife 7:e31157

    Google Scholar 

  • Schieffelin JS, Sherman PW (1995) Tugging contests reveal feeding hierarchies in naked mole-rat colonies. Anim Behav 49(2):537–541

    Article  Google Scholar 

  • Smith TE, Faulkes DH, Abbott DH (1997) Combined olfactory contact with the parent colony and direct contact with nonbreeding animals does not maintain reproductive suppression of ovulation in female naked mole-rats (Heterocephalus glaber). Horm Behav 31:277–288

    Google Scholar 

  • Smith TD, Bhatnagar KP, Dennis JC, Morrison EE, Park TJ (2007) Growth-deficient vomeronasal organs in the naked mole-rat (Heterocephalus glaber). Brain Res 1132(1):78–83

    Google Scholar 

  • Swift-Gallant A, Mo K, Peragine DE, Monks DA, Holmes MM (2015) Removal of reproductive suppression reveals latent sex differences in brain steroid hormone receptors in naked mole-rats, Heterocephalus glaber. Biol Sex Diff 6:31

    Google Scholar 

  • Thorley J, Mendonça R, Vullioud P, Torrents-Ticó M, Zöttl M, Gaynor D, Clutton-Brock T (2018a) No task specialization among helpers in Damaraland mole-rats. Anim Behav 143:9–24

    Article  Google Scholar 

  • Thorley J, Katlein N, Goddard K, Zöttl M, Clutton-Brock T (2018b) Reproduction triggers adaptive increases in body size in female mole-rats. Proc R Soc B 285:20180897

    Article  Google Scholar 

  • Toor I, Clement D, Carlson EN, Holmes MM (2015) Olfaction and social cognition in eusocial naked mole-rats (Heterocephalus glaber). Anim Behav 107:175–181

    Google Scholar 

  • Toor I, Edwards PD, Kaka N, Whitney R, Ziolkowski J, Monks DA, Holmes MM (2020) Aggression and motivation to disperse in eusocial naked mole-rats (Heterocephalus glaber). Anim Behav 168:45–58

    Google Scholar 

  • Torrents-Ticó M, Bennett NC, Jarvis JUM, Zöttl M (2018) Growth affects dispersal success in social mole-rats, but not the duration of philopatry. Biol Lett 14:20180005

    Article  Google Scholar 

  • Vice EN, Lagestee S, Browe BM, Deb D, Smith ESJ, Park TJ (2021) Sensory systems of the African naked mole-rat. In: Buffenstein R, Park TJ, Holmes MM (eds) The Extraordinary Biology of the Naked Mole-Rat. Springer, New York, pp 137–156

    Google Scholar 

  • Watarai A, Arai N, Miyawaki S, Okano H, Miura K, Mogi K, Kikusui T (2018) Responses to pup vocalizations in subordinate naked mole-rats are induced by estradiol ingested through coprophagy of queen’s feces. Proc Natl Acad Sci USA 115(37):9264–9269

    Article  CAS  Google Scholar 

  • Yosida S, Okanoya K (2009) Naked mole-rat is sensitive to social hierarchy encoded in antiphonal vocalization. Ethology 115(9):823–831

    Article  Google Scholar 

  • Yosida S, Okanoya K (2012) Bilateral lesions of the medial frontal cortex disrupt recognition of social hierarchy during antiphonal communication in naked mole-rats (Heterocephalus glaber). J Comp Physiol A 198(2):109–117

    Google Scholar 

  • Yosida S, Kobayasi KI, Ikebuchi M, Ozaki R, Okanoya K (2007) Antiphonal vocalization of a subterranean rodent, the naked mole-rat (Heterocephalus glaber). Ethology 113(7):703–710

    Google Scholar 

  • Zions M, Meehan EF, Kress ME, Thevalingam D, Jenkins EC, Kaila K, Puskarjov M, McCloskey DP (2020) Nest carbon dioxide masks GABA-dependent seizure susceptibility in the naked mole-rat. Curr Biol 30:1–10

    Article  Google Scholar 

  • Zöttl M, Vullioud P, Mendonça R, Torrents Ticó M, Gaynor D, Mitchell A, Clutton-Brock T (2016a) Differences in cooperative behavior among Damaraland mole-rats are consequences of an age-related polyethism. Proc Natl Acad Sci USA 113(37):10382–10387

    Google Scholar 

  • Zöttl M, Thorley J, Gaynor D, Bennett NC, Clutton-Brock T (2016b) Variation in growth of Damaraland mole-rats is explained by competition rather than by functional specialization for different tasks. Biol Lett 12:20160820

    Article  Google Scholar 

  • Zöttl M, Vullioud P, Goddard K, Torrents-Ticó M, Gaynor D, Bennett NC, Clutton-Brock T (2018) Allo-parental care in Damaraland mole-rats is female biased and age dependent, though independent of testosterone levels. Physiol Behav 193:149–153

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Melissa M. Holmes .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Holmes, M.M., Goldman, B.D. (2021). Social Behavior in Naked Mole-Rats: Individual Differences in Phenotype and Proximate Mechanisms of Mammalian Eusociality. In: Buffenstein, R., Park, T.J., Holmes, M.M. (eds) The Extraordinary Biology of the Naked Mole-Rat. Advances in Experimental Medicine and Biology, vol 1319. Springer, Cham. https://doi.org/10.1007/978-3-030-65943-1_2

Download citation

Publish with us

Policies and ethics