The social brain hypothesis (SBH) posits that the demands imposed on individuals by living in cohesive social groups exert a selection pressure favouring the evolution of large brains and complex cognitive abilities. Using volumetry and the isotropic fractionator to determine the size of and numbers of neurons in specific brain regions, here we test this hypothesis in African mole-rats (Bathyergidae). These subterranean rodents exhibit a broad spectrum of social complexity, ranging from strictly solitary through to eusocial cooperative breeders, but feature similar ecologies and life history traits. We found no positive association between sociality and neuroanatomical correlates of information-processing capacity. Solitary species are larger, tend to have greater absolute brain size and have more neurons in the forebrain than social species. The neocortex ratio and neuronal counts correlate negatively with social group size. These results are clearly inconsistent with the SBH and show that the challenges coupled with sociality in this group of rodents do not require brain enlargement or fundamental reorganization. These findings suggest that group living or pair bonding per se does not select strongly for brain enlargement unless coupled with Machiavellian interactions affecting individual fitness.

Department of Biological Sciences University of Cape Town 7701 Rondebosch South Africa

Department of General Zoology Faculty for Biology University of Duisburg Essen 45117 Essen Germany

Department of Zoology Faculty of Science Charles University Viničná 7 CZ 128 44 Praha 2 Czech Republic

Department of Zoology Faculty of Science University of South Bohemia Branišovská 1760 CZ 370 05 České Budějovice Czech Republic

Mammal Research Institute Department of Zoology and Entomology University of Pretoria Pretoria 0002 South Africa

Zobrazit více v PubMed

Dunbar RI. The social brain hypothesis. Evol. Anthropol. 1998;6:178–190. doi: 10.1002/(SICI)1520-6505(1998)6:5<178::AID-EVAN5>3.0.CO;2-8. DOI

Dunbar RI, Shultz S. Evolution in the social brain. Science. 2007;317:1344–7. doi: 10.1126/science.1145463. PubMed DOI

van der Bijl W, Kolm N. Why direct effects of predation complicate the social brain hypothesis. BioEssays. 2016;38:568–577. doi: 10.1002/bies.201500166. PubMed DOI

Chojnacka, D., Isler, K., Barski, J. J. & Bshary, R. Relative brain and brain part sizes provide only limited evidence that machiavellian behaviour in cleaner wrasse is cognitively demanding. PLoS One10 (2015). PubMed PMC

Weisbecker V, Blomberg S, Goldizen AW, Brown M, Fisher D. The evolution of relative brain size in marsupials is energetically constrained but not driven by behavioral complexity. Brain. Behav. Evol. 2015;85:125–135. doi: 10.1159/000377666. PubMed DOI

Matějů J, et al. Absolute, not relative brain size correlates with sociality in ground squirrels. Proc. R. Soc. B. 2016;283:20152725. doi: 10.1098/rspb.2015.2725. PubMed DOI PMC

Sayol F, et al. Environmental variation and the evolution of large brains in birds. Nat. Commun. 2016;7:13971. doi: 10.1038/ncomms13971. PubMed DOI PMC

DeCasien AR, Williams SA, Higham JP. Primate brain size is predicted by diet but not sociality. Nat. Ecol. Evol. 2017;1:0112. doi: 10.1038/s41559-017-0112. PubMed DOI

Powell LE, Isler K, Barton RA. Re-evaluating the link between brain size and behavioural ecology in primates. Proc. R. Soc. B. 2017;284:20171765. doi: 10.1098/rspb.2017.1765. PubMed DOI PMC

Fox KC, Muthukrishna M, Shultz S. The social and cultural roots of whale and dolphin brains. Nat. Ecol. Evol. 2017;1:1699. doi: 10.1038/s41559-017-0336-y. PubMed DOI

Dunbar RIM, Shultz S. Why are there so many explanations for primate brain evolution? Phil. Trans. R. Soc. B. 2017;372:20160244. doi: 10.1098/rstb.2016.0244. PubMed DOI PMC

Byrne, R. W. & Whiten, A. (eds). Machiavellian Intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans. (Clarendon Press, 1989).

Shultz S, Dunbar RIM. The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proc. R. Soc. B. 2007;274:2429–2436. doi: 10.1098/rspb.2007.0693. PubMed DOI PMC

Dunbar RI, Shultz S. Bondedness and sociality. Behaviour. 2010;147:775–803. doi: 10.1163/000579510X501151. DOI

Emery NJ, Seed AM, Von Bayern AM, Clayton NS. Cognitive adaptations of social bonding in birds. Proc. R. Soc. B. 2007;362:489–505. PubMed PMC

Burkart JM, Hrdy SB, Van Schaik CP. Cooperative breeding and human cognitive evolution. Evol. Antropol. 2009;18:175–186. doi: 10.1002/evan.20222. DOI

Isler K, van Schaik CP. Allomaternal care, life history and brain size evolution in mammals. J. Hum. Evol. 2012;63:52–63. doi: 10.1016/j.jhevol.2012.03.009. PubMed DOI

Iwaniuk AN, Arnold KE. Is cooperative breeding associated with bigger brains? A comparative test in the Corvida (Passeriformes) Ethology. 2004;110:203–220. doi: 10.1111/j.1439-0310.2003.00957.x. DOI

Thornton A, McAuliffe K. Cognitive consequences of cooperative breeding? A critical appraisal. J. Zool. 2015;295:12–22. doi: 10.1111/jzo.12198. DOI

Healy SD, Rowe C. A critique of comparative studies of brain size. Proc. R. Soc. B. 2007;274:453–464. doi: 10.1098/rspb.2006.3748. PubMed DOI PMC

Logan, C. J. et al. Beyond Brain Size: uncovering the neural correlates of behavioral and cognitive specialization. Comparative Cognition & Behavior Reviews 13, 55–90, 10.3819/CCBR.2018.130008.

Bennett, N. C. & Faulkes, C. G. African mole-rats: ecology and eusociality. (Cambridge University Press, 2000).

Bennett NC, Jarvis JUM. Coefficients of digestibility and nutritional values of geophytes and tubers eaten by southern African mole‐rats (Rodentia: Bathyergidae) J. Zool. 1995;236:189–198. doi: 10.1111/j.1469-7998.1995.tb04487.x. DOI

Faulkes CG, et al. Ecological constraints drive social evolution in the African mole-rats. Proc. R Soc. B. 1997;264:1619–1627. doi: 10.1098/rspb.1997.0226. PubMed DOI PMC

Bennett, N. C., Gundula, H. G. & Faulkes, C. G. The reproductive physiology and endocrinology of the African mole-rats: with special reference to southern African mole-rats species in Subterranean rodents: news from underground (ed. Begall, S., Burda, H. & Schleich, C. E.) 61–79 (Springer, 2007).

Burda, H. From natural histories to life histories — a homage to a comparative approach in Subterranean rodents: news from underground (ed. Begall, S., Burda, H. & Schleich, C. E.) 197–203 (Springer, 2007).

Burda H, Honeycutt RL, Begall S. Are naked and common mole-rats eusocial and if so, why? Behav. Ecol. Sociobiol. 2000;47:293–303. doi: 10.1007/s002650050669. DOI

Jarvis JUM, O’Riain MJ, Bennett NC, Sherman PW. Mammalian eusociality: A family affair. Trends Ecol. Evol. 1994;9:47–51. doi: 10.1016/0169-5347(94)90267-4. PubMed DOI

Bennett NC, Jarvis JUM, Aguilar GH, McDaid EJ. Growth and development in six species of African mole‐rats (Rodentia: Bathyergidae) J. Zool. 1991;225:13–26. doi: 10.1111/j.1469-7998.1991.tb03798.x. DOI

Sherman, P. W., Jarvis, J. U. M. & Alexander, R. D. Biology of the Naked Mole-rat (Princeton University Press, 1991).

Bennett NC, Jarvis JUM. The reproductive biology of the Cape mole‐rat, Georychus capensis (Rodentia, Bathyergidae) J. Zool. 1988;214:95–106. doi: 10.1111/j.1469-7998.1988.tb04989.x. DOI

Herbst M, Jarvis JUM, Bennett NC. A field assessment of reproductive seasonality in the threatened wild Namaqua dune mole-rat (Bathyergus janetta) J. Zool. 2004;263:259–268. doi: 10.1017/S0952836904005114. DOI

Šumbera R, Burda H, Chitaukali WN. Reproductive biology of a solitary subterranean bathyergid rodent, the silvery mole-rat (Heliophobius argenteocinereus) J. Mammal. 2003;84:278–287. doi: 10.1644/1545-1542(2003)084<0278:RBOASS>2.0.CO;2. DOI

Sichilima AM, Faulkes CG, Bennett NC. Field evidence for aseasonality of reproduction and colony size in the Afrotropical giant mole-rat Fukomys mechowii (Rodentia: Bathyergidae) Afr. Zool. 2008;43:144–149. doi: 10.1080/15627020.2008.11657231. DOI

Sichilima AM, Bennett NC, Faulkes CG. Field evidence for colony size and aseasonality of breeding and in Ansell’s mole-rat, Fukomys anselli (Rodentia: Bathyergidae) Afr. Zool. 2011;46:334–339.

Oosthuizen MK, Bennett NC, Lutermann H, Coen CW. Reproductive suppression and the seasonality of reproduction in the social Natal mole-rat (Cryptomys hottentotus natalensis) Gen. Comp. Endocrinol. 2008;159:236–240. doi: 10.1016/j.ygcen.2008.09.004. PubMed DOI

Šklíba J, Šumbera R, Chitaukali WN, Burda H. Home‐range dynamics in a solitary subterranean rodent. Ethology. 2009;115:217–226. doi: 10.1111/j.1439-0310.2008.01604.x. DOI

Lövy M, Šklíba J, Šumbera R. Spatial and temporal activity patterns of the free-living giant mole-rat (Fukomys mechowii), the largest social bathyergid. PloS One. 2013;8:e55357. doi: 10.1371/journal.pone.0055357. PubMed DOI PMC

Jarvis J. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science. 1981;212:571–573. doi: 10.1126/science.7209555. PubMed DOI

Bennett NC. Behaviour and social organization in a colony of the Damaraland mole‐rat Cryptomys damarensis. J. Zool. 1990;220:225–247. doi: 10.1111/j.1469-7998.1990.tb04305.x. DOI

Burda H, Kawalika M. Evolution of eusociality in the Bathyergidae. The case of the giant mole rats (Cryptomys mechowi) Naturwissenschaften. 1993;80:235–237. doi: 10.1007/BF01175742. PubMed DOI

Jarvis JUM, Bennett NC. Eusociality has evolved independently in two genera of bathyergid mole-rats—but occurs in no other subterranean mammal. Behav. Ecol. Sociobiol. 1993;33:253–260. doi: 10.1007/BF02027122. DOI

Burda H. Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents. Experientia. 1995;51:411–413. doi: 10.1007/BF01928906. PubMed DOI

Spinks AC, Jarvis JUM, Bennett NC. Comparative patterns of philopatry and dispersal in two common mole-rat populations: Implications for the evolution of mole-rat sociality. J. Anim. Ecol. 2000;69:224–234. doi: 10.1046/j.1365-2656.2000.00388.x. DOI

Bappert MT, Burda H, Begall S. To mate or not to mate? Mate preference and fidelity in monogamous Ansell’s mole-rats, Fukomys anselli, Bathyergidae. Folia Zool. 2012;61:71–83. doi: 10.25225/fozo.v61.i1.a11.2012. DOI

Patzenhauerová H, Šklíba J, Bryja J, Šumbera R. Parentage analysis of Ansell’s mole-rat family groups indicates a high reproductive skew despite relatively relaxed ecological constraints on dispersal. Mol. Ecol. 2013;22:4988–5000. doi: 10.1111/mec.12434. PubMed DOI

Bray TC, Bloomer P, O’Riain MJ, Bennett NC. How attractive is the girl next door? An assessment of spatial mate acquisition and paternity in the solitary cape dune mole-rat, Bathyergus suillus. PLoS One. 2012;7:e39866. doi: 10.1371/journal.pone.0039866. PubMed DOI PMC

Patzenhauerová H, Bryja J, Šumbera R. Kinship structure and mating system in a solitary subterranean rodent, the silvery mole-rat. Behav. Ecol. Sociobiol. 2010;64:757–767. doi: 10.1007/s00265-009-0893-4. DOI

Bennett NC, Faulkes CG, Jarvis JUM. Socially induced infertility, incest avoidance and the monopoly of reproduction in cooperatively breeding African mole-rats, family Bathyergidae. Adv. Study Behav. 1999;28:75–114. doi: 10.1016/S0065-3454(08)60216-8. DOI

Clarke FM, Faulkes CG. Intracolony aggression in the eusocial naked mole-rat. Heterocephalus glaber. Anim. Behav. 2001;61:311–324. doi: 10.1006/anbe.2000.1573. DOI

Bednářová R, Hrouzková-Knotková E, Burda H, Sedláček F, Šumbera R. Vocalisations of the giant mole-rat (Fukomys mechowii), a subterranean rodent with the richest vocal repertoire. Bioacoustics. 2013;22:87–107. doi: 10.1080/09524622.2012.712749. DOI

Dvořáková V, Hrouzková E, Šumbera R. Vocal repertoire of the social Mashona mole-rat (Fukomys darlingi) and how it compares with other mole-rats. Bioacoustics. 2016;25:1–14. doi: 10.1080/09524622.2016.1141117. DOI

Faulkes CG, Bennett NC. Plasticity and constraints on social evolution in African mole-rats: ultimate and proximate factors. Philos. Trans. R. Soc. B. 2013;368:20120347. doi: 10.1098/rstb.2012.0347. PubMed DOI PMC

Shultz S, Dunbar R. Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc. Natl. Acad. Sci. USA. 2010;107:21582–21586. doi: 10.1073/pnas.1005246107. PubMed DOI PMC

Bishop JM, Jarvis JUM, Spinks AC, Bennett NC, O’Ryan C. Molecular insight into patterns of colony composition and paternity in the common mole-rat Cryptomys hottentotus hottentotus. Mol. Ecol. 2004;13:1217–1229. doi: 10.1111/j.1365-294X.2004.02131.x. PubMed DOI

O’Riain MJ, Jarvis JUM, Faulkes CG. A dispersive morph in the naked mole-rat. Nature. 1996;380:619–621. doi: 10.1038/380619a0. PubMed DOI

Scantlebury M, Speakman JR, Oosthuizen MK, Roper TJ, Bennett NC. Energetics reveals physiologically distinct castes in a eusocial mammal. Nature. 2006;440:795–797. doi: 10.1038/nature04578. PubMed DOI

Mooney SJ, Filice DCS, Douglas NR, Holmes MM. Task specialization and task switching in eusocial mammals. Anim. Behav. 2015;109:227–233. doi: 10.1016/j.anbehav.2015.08.019. DOI

Zöttl M, et al. Differences in cooperative behavior among Damaraland mole rats are consequences of an age-related polyethism. Proc. Natl. Acad. Sci. USA. 2016;113:201607885. doi: 10.1073/pnas.1607885113. PubMed DOI PMC

Šklíba J, Lövy M, Burda H, Šumbera R. Variability of space-use patterns in a free living eusocial rodent, Ansell’s mole-rat indicates age-based rather than caste polyethism. Sci. Rep. 2016;6:37497. doi: 10.1038/srep37497. PubMed DOI PMC

O’Donnell S, et al. Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae) Proc. R Soc. B. 2015;282:20150791. doi: 10.1098/rspb.2015.0791. PubMed DOI PMC

Dunbar RIM. Neocortex size as a constraint on group size in primates. J. Hum. Evol. 1992;22:469–493. doi: 10.1016/0047-2484(92)90081-J. DOI

Dunbar RIM, Bever J. Neocortex size predicts group size in carnivores and some insectivores. Ethology. 1998;104:695–708. doi: 10.1111/j.1439-0310.1998.tb00103.x. DOI

Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE. Brain size and social complexity: A computed tomography study in Hyaenidae. Brain. Behav. Evol. 2011;77:91–104. doi: 10.1159/000323849. PubMed DOI

Marino L. What can dolphins tell us about primate evolution? Evol. Anthropol. 1996;5:81–85. doi: 10.1002/(SICI)1520-6505(1996)5:3<81::AID-EVAN3>3.0.CO;2-Z. DOI

MacLean EL, et al. The evolution of self-control. Proc. Natl. Acad. Sci. USA. 2014;111:E2140–E2148. doi: 10.1073/pnas.1323533111. PubMed DOI PMC

Deaner RO, Isler K, Burkart J, van Schaik C. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav. Evol. 2007;70:115–124. doi: 10.1159/000102973. PubMed DOI

Herculano-Houzel S. Brains matter, bodies maybe not: The case for examining neuron numbers irrespective of body size. Ann. N. Y. Acad. Sci. 2011;1225:191–199. doi: 10.1111/j.1749-6632.2011.05976.x. PubMed DOI

Olkowicz S, et al. Birds have primate-like numbers of neurons in the forebrain. Proc. Natl. Acad. Sci. USA. 2016;113:7255–7260. doi: 10.1073/pnas.1517131113. PubMed DOI PMC

Willemet R. Reconsidering the evolution of brain, cognition, and behavior in birds and mammals. Front. Psychol. 2013;4:396. doi: 10.3389/fpsyg.2013.00396. PubMed DOI PMC

Dicke U, Roth G. Neuronal factors determining high intelligence. Phil. Trans. R. Soc. B. 2016;371:20150180. doi: 10.1098/rstb.2015.0180. PubMed DOI PMC

Pérez-Barbería FJ, Shultz S, Dunbar RIM. Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution. 2007;61:2811–2821. doi: 10.1111/j.1558-5646.2007.00229.x. PubMed DOI

Barton RA, Harvey PH. Mosaic evolution of brain structure in mammals. Nature. 2000;405:1055–1058. doi: 10.1038/35016580. PubMed DOI

Finlay BL, Darlington RB. Linked regularities in the development and evolution of mammalian brains. Science. 1995;268:1578–1584. doi: 10.1126/science.7777856. PubMed DOI

Herculano-Houzel S, et al. Updated neuronal scaling rules for the brains of Glires (rodents/lagomorphs) Brain Behav. Evol. 2011;78:302–314. doi: 10.1159/000330825. PubMed DOI PMC

Herculano-Houzel S. Encephalization, neuronal excess, and neuronal index in rodents. Anat. Rec. 2007;290:1280–1287. doi: 10.1002/ar.20598. PubMed DOI

Herculano-Houzel S. Numbers of neurons as biological correlates of cognitive capability. Curr. Opin. Behav. Sci. 2017;16:1–7. doi: 10.1016/j.cobeha.2017.02.004. DOI

Toor I, Clement D, Carlson EN, Holmes MM. Olfaction and social cognition in eusocial naked mole-rats. Heterocephalus glaber. Anim. Behav. 2015;107:175–181. doi: 10.1016/j.anbehav.2015.06.015. DOI

Brothers L. The social brain: a project for integrating primate behavior and neurophysiology in a new domain. Concepts Neurosci. 1990;1:27–51.

Benson-Amram S, Dantzer B, Stricker G, Swanson EM, Holekamp KE. Brain size predicts problem-solving ability in mammalian carnivores. Proc. Natl. Acad. Sci. USA. 2016;113:2532–2537. doi: 10.1073/pnas.1505913113. PubMed DOI PMC

Faulkes CG, Abbott DH, Jarvis JUM. Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats. Heterocephalus glaber. J. Reprod. Fertil. 1990;88:559–568. doi: 10.1530/jrf.0.0880559. PubMed DOI

Faulkes CG, Abbott DH, Jarvis JUM. Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber. J. Reprod. Fertil. 1991;91:593–604. doi: 10.1530/jrf.0.0910593. PubMed DOI

Bennett NC, Faulkes CG, Molteno AJ. Reproductive suppression in subordinate, non-breeding female Damaraland mole-rats: two components to a lifetime of socially induced infertility. Proc. R. Soc. B. 1996;263:1599–1603. doi: 10.1098/rspb.1996.0234. PubMed DOI

Buffenstein R, Yahav S. Is the naked mole-rat Hererocephalus glaber an endothermic yet poikilothermic mammal? J. Therm. Biol. 1991;16:227–232. doi: 10.1016/0306-4565(91)90030-6. DOI

Fang WQ, Yuste R. Overproduction of neurons is correlated with enhanced cortical ensembles and increased perceptual discrimination. Cell Rep. 2017;21:381–392. doi: 10.1016/j.celrep.2017.09.040. PubMed DOI PMC

Jerison, H. J. Evolution of the Brain and Intelligence. (Academic Press, 1973).

Van Schaik CP. Why are diurnal primates living in groups? Behaviour. 1983;87:120–144. doi: 10.1163/156853983X00147. DOI

Janzen FJ, Tucker JK, Paukstis GL. Experimental analysis of an early life-history stage: Avian predation selects for larger body size of hatchling turtles. J. Evol. Biol. 2000;13:947–954. doi: 10.1046/j.1420-9101.2000.00234.x. DOI

Basolo AL, Wagner WE. Covariation between predation risk, body size and fin elaboration in the green swordtail. Xiphophorus helleri. Biol. J. Linn. Soc. 2004;83:87–100. doi: 10.1111/j.1095-8312.2004.00369.x. DOI

Reddon AR, et al. No evidence for larger brains in cooperatively breeding cichlid fishes. Can. J. Zool. 2016;94:373–378. doi: 10.1139/cjz-2015-0118. DOI

Kudo H, Dunbar RIM. Neocortex size and social network size in primates. Anim. Behav. 2001;62:711–722. doi: 10.1006/anbe.2001.1808. DOI

Schillaci M. Primate mating systems and the evolution of neocortex size. J. Mammal. 2008;89:58–63. doi: 10.1644/06-MAMM-A-417.1. DOI

Striedter, G. F. Priciples of brain evolution. (Sinauer Associates, 2005).

Finlay BL, Brodsky P. Cortical evolution as the expression of a program for disproportionate growth and the proliferation of areas. Evol. Nerv. Syst. 2010;3:73–96.

Kalamatianos T, et al. Telencephalic binding sites for oxytocin and social organization: A comparative study of eusocial naked mole‐rats and solitary cape mole‐rats. J. Comp. Neurol. 2010;518:1792–1813. doi: 10.1002/cne.22302. PubMed DOI

Coen CW, et al. Sociality and the telencephalic distribution of corticotrophin‐releasing factor, urocortin 3, and binding sites for CRF type 1 and type 2 receptors: A comparative study of eusocial naked mole‐rats and solitary Cape mole‐rats. J. Comp. Neurol. 2015;523:2344–2371. doi: 10.1002/cne.23796. PubMed DOI

Amrein, I. et al. Adult neurogenesis and its anatomical context in the hippocampus of three mole-rat species. Front. Neuroanat. 8 (2014). PubMed PMC

Isler K, van Schaik CP. Metabolic costs of brain size evolution. Biol. Lett. 2006;2:557–560. doi: 10.1098/rsbl.2006.0538. PubMed DOI PMC

Lovegrove BG. The cost of burrowing by the social mole rats (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: the role of soil moisture. Physiol. Zool. 1989;62:449–469. doi: 10.1086/physzool.62.2.30156179. DOI

Barrett L, Henzi P, Rendall D. Social brains, simple minds: does social complexity really require cognitive complexity? Philos. Trans. R. Soc. Lond. B Biol Sci. 2007;362:561–575. doi: 10.1098/rstb.2006.1995. PubMed DOI PMC

Patterson BD, Upham NS. A newly recognized family from the Horn of Africa, the Heterocephalidae (Rodentia: Ctenohystrica) Zool. J. Linnean Soc. 2014;172:942–963. doi: 10.1111/zoj.12201. DOI

Bennett NC, Jarvis JUM, Wallace DB. The relative age structure and body masses of complete wild‐captured colonies of two social mole‐rats, the common mole‐rat, Cryptomys hottentotus hottentotus and the Damaraland mole‐rat, Cryptomys damarensis. J. Zool. 1990;220:469–485. doi: 10.1111/j.1469-7998.1990.tb04319.x. DOI

Clarke FM, Faulkes CG. Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc. R. Soc. B. 1997;264:993–1000. doi: 10.1098/rspb.1997.0137. PubMed DOI PMC

Clarke FM, Faulkes CG. Hormonal and behavioural correlates of male dominance and reproductive status in captive colonies of the naked mole-rat, Heterocephalus glaber. Proc. R. Soc. B. 1998;265:1391–1399. doi: 10.1098/rspb.1998.0447. PubMed DOI PMC

Van Rensburg LJ, Chimimba CT, Van Der Merwe M, Schoeman AS, Bennett NC. Relative age and reproductive status in Cryptomys hottentotus pretoriae (Rodentia: Bathyergidae) from South Africa. J. Mammal. 2004;85:1225–1232. doi: 10.1644/BER-113.1. DOI

Patterson SK, Sandel AA, Miller JA, Mitani JC. Data quality and the comparative method: The case of primate group size. Int. J. Primatol. 2014;35:990–1003. doi: 10.1007/s10764-014-9777-1. DOI

Stephan H. Methodische Studien über den quantitativen Vergleich architektonischer Struktureinheiten des Gehirns. Zwiss Zool. 1960;164:143–172.

Herculano-Houzel S, Lent R. Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J. Neurosci. 2005;25:2518–2521. doi: 10.1523/JNEUROSCI.4526-04.2005. PubMed DOI PMC

Mullen RJ, Buck CR, Smith AM. NeuN, a neuronal specific nuclear protein in vertebrates. Development. 1992;116:201–211. PubMed

R Core Team 2015 R: A Language and Environment for Statistical Computing (R Core Team, Vienna).

Hadfield JD. MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. J. Stat. Softw. 2010;33:1–22. doi: 10.18637/jss.v033.i02. PubMed DOI

Pagel M. Inferring the historical patterns of biological evolution. Nature. 1999;401:877–884. doi: 10.1038/44766. PubMed DOI

Faulkes CG, Verheyen E, Verheyen W, Jarvis JUM, Bennett NC. Phylogeographical patterns of genetic divergence and speciation in African mole-rats (Family: Bathyergidae) Mol. Ecol. 2004;13:613–629. doi: 10.1046/j.1365-294X.2004.02099.x. PubMed DOI

Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–131, https://CRAN.R-project.org/package=nlme (2017).

The evolution of brain neuron numbers in amniotes

Brain size and neuron numbers drive differences in yawn duration across mammals and birds

Individual and age-related variation of cellular brain composition in a squamate reptile

Functional histology of the skin in the subterranean African giant mole-rat: thermal windows are determined solely by pelage characteristics

The evolution of brain structure captured in stereotyped cell count and cell type distributions

Artificial selection on brain size leads to matching changes in overall number of neurons

Brain atlas of the African mole-rat Fukomys anselli