Subterranean common mole-rats of the genus Fukomys (family Bathyergidae) live in large, cooperatively-breeding families. Odor cues have been hypothesized to play an important role in mediating social behaviors in the underground ecotope, but only little is known about the role of olfactory signaling in burrowing mammals. Here we characterize the so far neglected perioral glands of Fukomys and other African mole-rats as an important source of olfactory social information. Histology demonstrates these structures to be derived sebaceous glands that are developed regardless of sex and reproductive status. However, gland activity is higher in Fukomys males, leading to sexually dimorphic patterns of stain and clotting of the facial pelage. Behavioral assays revealed that conspecifics prefer male but not female perioral swabs over scent samples from the back fur and that male sebum causes similar attraction as anogenital scent, a known source of social information in Fukomys. Finally, we assessed volatile compounds in the perioral sebum of the giant mole-rat (Fukomys mechowii) via GCxGC-MS-based metabolomic profiling. Volatiles display pronounced sex-specific signatures but also allow to differentiate between intrasexual reproductive status groups. These different lines of evidence suggest that mole-rat perioral glands provide complex odor signals which play a crucial role in social communication.

Department of Game Management and Wildlife Biology Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czech Republic

Department of General Zoology Faculty of Biology University of Duisburg Essen 45147 Essen Germany

Department of Zoology Faculty of Science Charles University BIOCEV Vestec Czech Republic

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Burda H. Constraints of pregnancy and evolution of sociality in mole-rats with special reference to reproductive and social patterns in Cryptomys hottentotus (Bathyergidae, Rodentia) J. Zool. Syst. Evol. Res. 1990;28:26–39. doi: 10.1111/j.1439-0469.1990.tb00362.x. DOI

Burland TM, Bennett NC, Jarvis JU, Faulkes CG. Eusociality in African mole-rats: New insights from patterns of genetic relatedness in the Damaraland mole-rat (Cryptomys damarensis) Proc. R. Soc. Lond. Ser. B. Biol. Sci. 2002;269:1025–1030. doi: 10.1098/rspb.2002.1978. PubMed DOI PMC

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

Zöttl M, Vullioud P, Mendonça R, Ticó MT, Gaynor D, Mitchell A, Clutton-Brock T. Differences in cooperative behavior among Damaraland mole rats are consequences of an age-related polyethism. Proc. Natl. Acad. Sci. 2016;113:10382–10387. doi: 10.1073/pnas.1607885113. PubMed DOI PMC

Torrents-Ticó M, Bennett NC, Jarvis JU, Zöttl M. Sex differences in timing and context of dispersal in Damaraland mole-rats (Fukomys damarensis) J. Zool. 2018;306:252–257. doi: 10.1111/jzo.12602. DOI

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

Bennett NC, Jarvis JU. Cryptomys damarensis. Mammal. Species. 2004;2004:1–5. doi: 10.1644/756. DOI

Mynhardt S, Harris-Barnes L, Bloomer P, Bennett NC. Spatial population genetic structure and colony dynamics in Damaraland mole-rats (Fukomys damarensis) from the southern Kalahari. BMC Ecol. Evol. 2021;21:1–17. PubMed PMC

Thorley J, Bensch H, Finn K, Clutton-Brock T, Zöttl M. Damaraland mole-rats are not obligate cooperative breeders. bioRxiv. 2021 doi: 10.1101/2021.12.08.471794. DOI

Young AJ, Bennett NC. Intra-sexual selection in cooperative mammals and birds: Why are females not bigger and better armed? Philos. Trans. R. Soc. B Biol. Sci. 2013;368:20130075. doi: 10.1098/rstb.2013.0075. PubMed DOI PMC

Caspar KR, Müller J, Begall S. Effects of sex and breeding status on skull morphology in cooperatively breeding Ansell’s mole-rats and an appraisal of sexual dimorphism in the Bathyergidae. Front. Ecol. Evol. 2021;9:638754. doi: 10.3389/fevo.2021.638754. DOI

Stathopoulos S, Bishop JM, O’Ryan C. Genetic signatures for enhanced olfaction in the African mole-rats. PLoS ONE. 2014;9:e93336. doi: 10.1371/journal.pone.0093336. PubMed DOI PMC

Heth G, Todrank J, Burda H. Individual odor similarities within colonies and across species of Cryptomys mole rats. J. Mammal. 2002;83:569–575. doi: 10.1644/1545-1542(2002)083<0569:IOSWCA>2.0.CO;2. 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

Bappert M, Burda H. Forgotten siblings or how the long memory of the eusocial giant mole-rat Cryptomys mechowi (Rodentia: Bathyergidae) serves to maintain incest avoidance. Mammal. Biol. 2005;70(Suppl.):5.

Heth G, Todrank J, Begall S, Wegner RE, Burda H. Genetic relatedness discrimination in eusocial Cryptomys anselli mole-rats, Bathyergidae, Rodentia. Folia Zool. 2004;53:269–278.

Leedale AE, Thorley J, Clutton-Brock T. Odour-based social recognition in Damaraland mole-rats, Fukomys damarensis. Anim. Behav. 2021;179:83–96. doi: 10.1016/j.anbehav.2021.06.019. DOI

Macholán M, Scharff A, Burda H, Zima J, Grütjen O. The karyotype and taxonomic status of Cryptomys amatus (Wroughton, 1907) from Zambia (Rodentia, Bathyergidae) Zeitschrift für Säugetierkunde. 1998;63:186–190.

Begall S, Burda H, Caspar KR. Fukomys anselli (Rodentia: Bathyergidae) Mamm. Species. 2021;53:160–173. doi: 10.1093/mspecies/seab015. DOI

de Graaff, G. A systematic revision of the Bathyergidae (Rodentia) of Southern Africa. Ph.D. dissertation, University of Pretoria, Pretoria, South Africa (1964).

Peters W. Über die von Herrn Major v. Mechow von seiner letzten Expedition nach Westafrika mitgebrachten Säugetiere. Sitzungsberichte der Gesellschaft naturforschender Freunde zu Berlin. 1881;1881:131–134.

Van Daele PAAG, Blonde P, Stjernstedt R, Adriaens D. A new species of African mole-rat (Fukomys, Bathyergidae, Rodentia) from the Zaire-Zambezi watershed. Zootaxa. 2013;3636:171–189. doi: 10.11646/zootaxa.3636.1.7. PubMed DOI

Fagir DM, Bennett NC, Ueckermann EA, Howard A, Hart DW. Ectoparasitic community of the Mahali mole-rat, Cryptomys hottentotus mahali: Potential host for vectors of medical importance in South Africa. Parasit. Vectors. 2021;14:1–9. doi: 10.1186/s13071-020-04537-w. PubMed DOI PMC

Quay WB. Comparative survey of the sebaceous and sudoriferous glands of the oral lips and angle in rodents. J. Mammal. 1965;46:23–37. doi: 10.2307/1377813. DOI

Sokolov VE. Mammal Skin. University of California Press; 1982.

Brady KM, Armitage KB. Scent-marking in the yellow-bellied marmot (Marmota flaviventris) Ethol. Ecol. Evol. 1999;11:35–47. doi: 10.1080/08927014.1999.9522840. DOI

Kimani, J. M. Comparative skin morphology and wound healing in Kenyan African mole rat (Tachyoryctes ibeanus) and naked mole rat (Heterocephalus glaber). Diploma thesis, University of Nairobi, Nairobi, Kenya (2013).

Bennett NC. The social structure and reproductive biology of the common mole-rat, Cryptomys h. hottentotus and remarks on the trends in reproduction and sociality in the family Bathyergidae. J. Zool. 1989;219:45–59. doi: 10.1111/j.1469-7998.1989.tb02564.x. DOI

Scharff A, Begall S, Grütjen O, Burda H. Reproductive characteristics and growth of Zambian giant mole-rats, Cryptomys mechowi (Rodentia: Bathyergidae) Mammalia. 1999;63:217–230. doi: 10.1515/mamm.1999.63.2.217. DOI

Burda H. Reproductive biology (behaviour, breeding, and postnatal development) in subterranean mole-rats, Cryptomys hottentotus (Bathyergidae) Zeitschrift für Säugetierkunde. 1989;54:360–376.

de Bruin PR, Viljoen H, Sichilima AM, Bennett NC. Socially induced infertility in Ansell's mole-rat: Are there depressed hormone levels in non-reproductive males and females? J. Zool. 2012;286:15–21. doi: 10.1111/j.1469-7998.2011.00841.x. DOI

Maswanganye KA, Bennett NC, Brinders J, Cooney R. Oligospermia and azoospermia in non-reproductive male Damaraland mole-rats Cryptomys damarensis (Rodentia: Bathyergidae) J. Zool. 1999;248:411–418. doi: 10.1111/j.1469-7998.1999.tb01039.x. DOI

Lövy M, Sklíba 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

Kawalika, M. Rodents of Ndola (Copperbelt Province, Zambia). PhD dissertation. Universität Duisburg-Essen, Essen, Germany (2004).

Caspar KR, Burda H, Begall S. Fukomys mechowii (Rodentia: Bathyergidae) Mamm. Species. 2021;53:145–159. doi: 10.1093/mspecies/seab014. DOI

R Core Team. R: A language and environment for statistical computing. https://www.R-project.org/ (R Foundation for Statistical Computing, 2021).

Garcia Montero A, Burda H, Begall S. Chemical restraint of African mole-rats (Fukomys sp.) with a combination of ketamine and xylazine. Vet. Anaesthesia Analg. 2015;42:187–191. doi: 10.1111/vaa.12180. PubMed DOI

Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods. 2012;9:671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

Ingram CM, Burda H, Honeycutt RL. Molecular phylogenetics and taxonomy of the African mole-rats, genus Cryptomys and the new genus Coetomys Gray, 1864. Mol. Phylogenet. Evol. 2004;31:997–1014. doi: 10.1016/j.ympev.2003.11.004. PubMed DOI

Chubb EC. On mammals from the Upper Zambezi River. Ann. Mag. Nat. Hist. 1909;3:33–36. doi: 10.1080/00222930908692542. DOI

Christensen, R. H. B. Ordinal-regression models for ordinal data. R package version 12-10. https://cran.r-project.org/package=ordinal (Accessed 27 Feb 2022) (2019).

Hagemeyer P, Peuckmann S, Papenfuhs N, Burda H. Chemical communication in blind, subterranean eusocial mole-rats (genus Coetomys): Which odour source codes information for individual recognition? Adv. Ethol. 2004;38:56.

Kott O, Šumbera R, Němec P. Light perception in two strictly subterranean rodents: life in the dark or blue? PLoS One. 2010;5:e11810. doi: 10.1371/journal.pone.0011810. PubMed DOI PMC

Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80. doi: 10.1186/gb-2004-5-10-r80. PubMed DOI PMC

Bolstad, B. preprocessCore: A collection of pre-processing functions. R package version 1.60.1 (2022).

Rohart F, Gautier B, Singh A, Lê Cao K-A. mixOmics: An R package for ‘omics feature selection and multiple data integration. PLoS Comput. Biol. 2017;13:e1005752. doi: 10.1371/journal.pcbi.1005752. PubMed DOI PMC

Pavelka N, Pelizzola M, Vizzardelli C, Capozzoli M, Splendiani A, Granucci F, Ricciardi-Castagnoli P. A power law global error model for the identification of differentially expressed genes in microarray data. BMC Bioinform. 2004;5:203. doi: 10.1186/1471-2105-5-203. PubMed DOI PMC

Kuntova B, Stopkova R, Stopka P. Transcriptomic and proteomic profiling revealed high proportions of odorant binding and antimicrobial defense proteins in olfactory tissues of the house mouse. Front. Genet. 2018;9:26. doi: 10.3389/fgene.2018.00026. PubMed DOI PMC

Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer; 2016.

Pleštilová L, Okrouhlík J, Burda H, Sehadová H, Valesky EM, Šumbera R. Functional histology of the skin in the subterranean African giant mole-rat: Thermal windows are determined solely by pelage characteristics. PeerJ. 2020;8:e8883. doi: 10.7717/peerj.8883. PubMed DOI PMC

Hesselmann, F. Vergleich der mikroskopischen Anatomie der Haut und Hautanhangsorgane des Hausmeerschweinchens (Cavia aperea f. porcellus) und des Ansells Kleingraumulls (Fukomys anselli) unter Berücksichtigung ihrer Anpassung an unterschiedliche Lebensräume. Ph.D. dissertation. Tierärztliche Hochschule Hannover, Hanover, Germany (2010).

Jarvis JUM. Reproduction of naked mole-rats. In: Sherman PW, Jarvis JUM, Alexander RD, editors. The Biology of the Naked Mole-rat. Princeton University Press; 1991. pp. 384–425.

Buffenstein R, Park TJ, Holmes M. The Extraordinary Biology of the Naked Mole-Rat. Springer; 2021.

Tullberg T. Ueber das System der Nagethiere: Eine phylogenetische Studie. Akademische Buchdruckerei Uppsala; 1899.

Thody AJ, Shuster S. Control and function of sebaceous glands. Physiol. Rev. 1989;69:383–416. doi: 10.1152/physrev.1989.69.2.383. PubMed DOI

Martan J. Effect of castration and androgen replacement on the supracaudal gland of the male guinea pig. J. Morphol. 1962;110:285–297. doi: 10.1002/jmor.1051100210. PubMed DOI

Garcia Montero A, Vole C, Burda H, Malkemper EP, Holtze S, Morhart M, et al. Non-breeding eusocial mole-rats produce viable sperm—spermiogram and functional testicular morphology of Fukomys anselli. PLoS ONE. 2016;11:e0150112. doi: 10.1371/journal.pone.0150112. PubMed DOI PMC

Burda H. Zambian mole-rats: 33 years on the scene and what we still do not know and how we could learn it. Front. Ecol. Evol. 2022;10:866709. doi: 10.3389/fevo.2022.866709. DOI

Kuprina KV, Smorkatcheva AV. Noninvasive age estimation in rodents by measuring incisors width, with the Zaisan mole vole (Ellobius tancrei) as an example. Mammalia. 2019;83(1):64–69. doi: 10.1515/mammalia-2017-0163. 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. J. Vertebr. Biol. 2012;61:71–83.

Schulte BA, Müller-Schwarze D, Tang R, Webster FX. Beaver (Castor canadensis) responses to major phenolic and neutral compounds in castoreum. J. Chem. Ecol. 1994;20:3063–3081. doi: 10.1007/BF02033711. PubMed DOI

Leclaire S, Nielsen JF, Drea CM. Bacterial communities in meerkat anal scent secretions vary with host sex, age, and group membership. Behav. Ecol. 2014;25:996–1004. doi: 10.1093/beheco/aru074. DOI

Rasmussen LEL, Perrin TE. Physiological correlates of musth: Lipid metabolites and chemical composition of exudates. Physiol. Behav. 1999;67:539–549. doi: 10.1016/S0031-9384(99)00114-6. PubMed DOI

Aldrich JR, Numata H, Borges M, Bin F, Waite GK, Lusby WR. Artifacts and pheromone blends from Nezara spp. and other stink bugs (Heteroptera: Pentatomidae) Zeitschrift für Naturforschung C. 1993;48:73–79. doi: 10.1515/znc-1993-1-214. DOI

Alberti TB, Barbosa WLR, Vieira JLF, Raposo NRB, Dutra RC. (−)-β-caryophyllene, a CB2 receptor-selective phytocannabinoid, suppresses motor paralysis and neuroinflammation in a murine model of multiple sclerosis. Int. J. Mol. Sci. 2017;18:691. doi: 10.3390/ijms18040691. PubMed DOI PMC

Gutiérrez-García AG, Contreras CM, Saldivar-Lara M. An alarm pheromone reduces ventral tegmental area-nucleus accumbens shell responsivity. Neurosci. Lett. 2018;678:16–21. doi: 10.1016/j.neulet.2018.04.054. PubMed DOI

Makarov SE, Ćurčić BPM, Tešević VV, Jadranin MB, Vujisić LV, Ćurčić SB, Mandić BM, Sekulić TL, Mitić BM. Defensive secretions in three species of polydesmids (Diplopoda, Polydesmida, Polydesmidae) J. Chem. Ecol. 2010;36:978–982. doi: 10.1007/s10886-010-9847-6. PubMed DOI

Raina S, Singh VK. Asymmetric synthesis of 5-hexadecanolide, pheromone of the queen of the Oriental hornet, Vespa orientalis. Tetrahedron. 1996;52:4479–4484. doi: 10.1016/0040-4020(96)00095-6. DOI

Filipiak W, Sponring A, Baur MM, Filipiak A, Ager C, Wiesenhofer H, Nagl M, Troppmair J, Amann A. Molecular analysis of volatile metabolites released specifically by Staphylococcus aureus and Pseudomonas aeruginosa. BMC Microbiol. 2012;12:113. doi: 10.1186/1471-2180-12-113. PubMed DOI PMC

Pohorecky LA, Blakley GG, Ma EW, Soini HA, Wiesler D, Bruce KE, Novotny MV. Social housing influences the composition of volatile compounds in the preputial glands of male rats. Horm. Behav. 2008;53:536–545. doi: 10.1016/j.yhbeh.2007.12.006. PubMed DOI

Zidat T, Dufour AB, Meiffren G, Gabirot M, Comte G, Allainé D. Anal scent gland secretions inform on sexual maturity, sex and social status in the Alpine marmot, Marmota marmota (Rodentia: Sciuridae): A role in intrasexual competition in cooperative breeders? Biol. J. Lin. Soc. 2018;125:229–239. doi: 10.1093/biolinnean/bly117. DOI

Setchell JM, Vaglio S, Moggi-Cecchi J, Boscaro F, Calamai L, Knapp LA. Chemical composition of scent-gland secretions in an Old World monkey (Mandrillus sphinx): Influence of sex, male status, and individual identity. Chem. Senses. 2010;35:205–220. doi: 10.1093/chemse/bjp105. PubMed DOI

Kean EF, Müller CT, Chadwick EA. Otter scent signals age, sex, and reproductive status. Chem. Senses. 2011;36:555–564. doi: 10.1093/chemse/bjr025. PubMed DOI

Thoss M, Luzynski KC, Enk VM, Razzazi-Fazeli E, Kwak J, Ortner I, Penn DJ. Regulation of volatile and non-volatile pheromone attractants depends upon male social status. Sci. Rep. 2019;9:489. doi: 10.1038/s41598-018-36887-y. PubMed DOI PMC

Dennis JC, Stilwell NK, Smith TD, Park TJ, Bhatnagar KP, Morrison EE. Is the mole rat vomeronasal organ functional? Anat. Rec. 2020;303:318–329. doi: 10.1002/ar.24060. PubMed DOI

Jastrow H, Burda H, Oelschläger HH. Unilateral absence of the terminal nerve and distribution of gonadotropin-releasing hormone immunoreactive neurons in the brain of the common mole-rat (Cryptomys, Rodentia) Brain Res. 1998;813:229–240. doi: 10.1016/S0006-8993(98)00771-9. PubMed DOI

Jiao H, Hong W, Nevo E, Li K, Zhao H. Convergent reduction of V1R genes in subterranean rodents. BMC Evol. Biol. 2019;19:1–9. doi: 10.1186/s12862-019-1502-4. PubMed DOI PMC

Wang Z, Nudelman A, Storm DR. Are pheromones detected through the main olfactory epithelium? Mol. Neurobiol. 2007;35:317–323. doi: 10.1007/s12035-007-0014-1. PubMed DOI

Scordato ES, Dubay G, Drea CM. Chemical composition of scent marks in the ringtailed lemur (Lemur catta): Glandular differences, seasonal variation, and individual signatures. Chem. Senses. 2007;32:493–504. doi: 10.1093/chemse/bjm018. PubMed DOI

Variation in mouse chemical signals is genetically controlled and environmentally modulated