1932

Abstract

Talpid moles and spotted hyenas have become the paradigms of anatomical and behavioral female masculinization. Females of many mole species develop ovotestes that produce testosterone, show external genitalia that resemble that of males, and close their vaginal orifice after every estrus, and female spotted hyenas lack an external vaginal orifice and develop a pseudoscrotum and a large pseudopenis through which they urinate, mate, and give birth. We review current knowledge about several significant aspects of the biology and evolution of these females, including () their specific study methods; () their unique anatomical features, and how these peculiarities influence certain physiological functions; and () the role that steroid hormones as well as genetic and environmental factors may have in urogenital system development, aggressive behavior, and social dominance. Nevertheless, both mole and hyena females are exceptionally efficient mothers, so their peculiar genitalia should not call into question their femininity.

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2023-02-15
2024-04-15
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Literature Cited

  1. 1.
    Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL et al. 1990. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346:6281240–44
    [Google Scholar]
  2. 2.
    Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. 1991. Male development of chromosomally female mice transgenic for Sry. Nature 351:6322117–21
    [Google Scholar]
  3. 3.
    Jost PA. 1948. Le controle cormonal de la différenciation du sexe. Biol. Rev. 23:2201–36
    [Google Scholar]
  4. 4.
    Jost A, Price D, Edwards RG, Harris GW, Edwards RG. 1970. Hormonal factors in the sex differentiation of the mammalian foetus. Philos. Trans. R. Soc. Lond. B 259:828119–31
    [Google Scholar]
  5. 5.
    Jost A, Vigier B, Prépin J, Perchellet JP. 1973. Studies on sex differentiation in mammals. The Gregory Pincus Memorial Lecture. Proceedings of the 1972 Laurentian Hormone Conference, Vol. 29 RO Greep 1–41 Boston: Academic
    [Google Scholar]
  6. 6.
    Bashamboo A, McElreavey K. 2015. Human sex-determination and disorders of sex-development (DSD). Semin. Cell Dev. Biol. 45:77–83
    [Google Scholar]
  7. 7.
    Jiménez R, Barrionuevo FJ, Burgos M. 2013. Natural exceptions to normal gonad development in mammals. Sex. Dev. 7:1–3147–62
    [Google Scholar]
  8. 8.
    Wislocki GB. 1936. The external genitalia of the simian primates. Hum. Biol. 8:3309–47
    [Google Scholar]
  9. 9.
    Hawkins CE, Dallas JF, Fowler PA, Woodroffe R, Racey PA. 2002. Transient masculinization in the fossa, Cryptoprocta ferox (Carnivora, Viverridae). Biol. Reprod. 66:3610–15
    [Google Scholar]
  10. 10.
    Glickman SE, Short RV, Renfree MB. 2005. Sexual differentiation in three unconventional mammals: spotted hyenas, elephants and tammar wallabies. Horm. Behav. 48:4403–17
    [Google Scholar]
  11. 11.
    Campbell CJ. 2017. Hypertrophied clitoris. The International Encyclopedia of Primatology Hoboken, NJ: John Wiley & Sons
    [Google Scholar]
  12. 12.
    Carosi M, Spani F, Ulland AE, Scalici M, Suomi SJ. 2020. Clitoral length in immature and mature captive tufted capuchin (Sapajus spp.) females: a cross-sectional study. Am. J. Primatol. 82:11e23135
    [Google Scholar]
  13. 13.
    Hill WO. 1958. External genitalia. Primatologia 3:1630–704
    [Google Scholar]
  14. 14.
    Wilson DE, Reeder DM. 2005. Mammal Species of the World: A Taxonomic and Geographic Reference Baltimore: Johns Hopkins Univ. Press
  15. 15.
    Westbury MV, Le Duc D, Duchêne DA, Krishnan A, Prost S et al. 2021. Ecological specialization and evolutionary reticulation in extant hyaenidae. Mol. Biol. Evol. 38:93884–97
    [Google Scholar]
  16. 16.
    Foley NM, Springer MS, Teeling EC. 2016. Mammal madness: Is the mammal tree of life not yet resolved?. Philos. Trans. R. Soc. B 371:169920150140
    [Google Scholar]
  17. 17.
    Racey PA, Skinner JD. 1979. Endocrine aspects of sexual mimicry in spotted hyaenas Crocuta crocuta. J. Zool. 187:3315–26
    [Google Scholar]
  18. 18.
    Lindeque M, Skinner JD. 1982. Fetal androgens and sexual mimicry in spotted hyaenas (Crocuta crocuta). Reproduction 65:2405–10
    [Google Scholar]
  19. 19.
    Lindeque M, Skinner JD, Millar RP. 1986. Adrenal and gonadal contribution to circulating androgens in spotted hyaenas (Crocuta crocuta) as revealed by LHRH, hCG and ACTH stimulation. Reproduction 78:1211–17
    [Google Scholar]
  20. 20.
    van Jaarsveld AS, Skinner JD. 1991. Plasma androgens in spotted hyaenas (Crocuta crocuta): influence of social and reproductive development. Reproduction 93:1195–201
    [Google Scholar]
  21. 21.
    Dloniak SM, French JA, Holekamp KE. 2006. Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas. Nature 440:70881190–93
    [Google Scholar]
  22. 22.
    Watts HE, Tanner JB, Lundrigan BL, Holekamp KE. 2009. Post-weaning maternal effects and the evolution of female dominance in the spotted hyena. Proc. Biol. Sci. 276:16652291–98
    [Google Scholar]
  23. 23.
    McCormick SK, Holekamp KE. 2022. Aggressiveness and submissiveness in spotted hyaenas: One trait or two?. Anim. Behav. 186:179–90
    [Google Scholar]
  24. 24.
    Ilany A, Holekamp KE, Akçay E. 2021. Rank-dependent social inheritance determines social network structure in spotted hyenas. Science 373:6552348–52
    [Google Scholar]
  25. 25.
    Glickman SE, Frank LG, Davidson JM, Smith ER, Siiteri PK. 1987. Androstenedione may organize or activate sex-reversed traits in female spotted hyenas. PNAS 84:103444–47
    [Google Scholar]
  26. 26.
    Glickman SE, Frank LG, Pavgi S, Licht P. 1992. Hormonal correlates of “masculinization” in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity. Reproduction 95:2451–62
    [Google Scholar]
  27. 27.
    Frank LG, Glickman SE, Licht P. 1991. Fatal sibling aggression, precocial development, and androgens in neonatal spotted hyenas. Science 252:5006702–4
    [Google Scholar]
  28. 28.
    Licht P, Frank LG, Pavgi S, Yalcinkaya TM, Siiteri PK, Glickman SE. 1992. Hormonal correlates of “masculinization” in female spotted hyaenas (Crocuta crocuta). 2. Maternal and fetal steroids. Reproduction 95:2463–74
    [Google Scholar]
  29. 29.
    Licht P, Hayes T, Tsai P, Cunha G, Kim H et al. 1998. Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 1. Urogenital morphology and placental androgen production during fetal life. Reproduction 113:1105–16
    [Google Scholar]
  30. 30.
    Yalcinkaya TM, Siiteri PK, Vigne J-L, Licht P, Pavgi S et al. 1993. A mechanism for virilization of female spotted hyenas in utero. Science 260:51161929–31
    [Google Scholar]
  31. 31.
    Browne P, Place NJ, Vidal JD, Moore IT, Cunha GR et al. 2006. Endocrine differentiation of fetal ovaries and testes of the spotted hyena (Crocuta crocuta): timing of androgen-independent versus androgen-driven genital development. Reproduction 132:4649–59
    [Google Scholar]
  32. 32.
    Conley AJ, Corbin CJ, Browne P, Mapes SM, Place NJ et al. 2007. Placental expression and molecular characterization of aromatase cytochrome P450 in the spotted hyena (Crocuta crocuta). Placenta 28:7668–75
    [Google Scholar]
  33. 33.
    Henning WL. 1952. Method for keeping the eastern mole in captivity. J. Mammal. 33:3392–95
    [Google Scholar]
  34. 34.
    Skoczeń S. 1961. A new keeping arrangement for the mole Talpa europaea Linnaeus 1758, in captivity; Nowy sposób trzymania kreta, Talpa europaea Linnaeus 1758 w niewoli. Acta Theriol. 5:20287–89
    [Google Scholar]
  35. 35.
    Rudge AJB. 1966. Catching and keeping live moles. J. Zool. 149:142–45
    [Google Scholar]
  36. 36.
    Rozmus S. 1973. Keeping the mole (Talpa europaea Linnaeus, 1758) in captivity. Acta Theriol. 18:27489–90
    [Google Scholar]
  37. 37.
    Funmilayo O. 1977. Daily food consumption of captive moles. Acta Theriol. 22:389–92
    [Google Scholar]
  38. 38.
    Hickman GC. 1978. A transparent burrow system for the study of fossorial mammals. Acta Theriol. 23:443–45
    [Google Scholar]
  39. 39.
    Redfern R, Mitchell W. 1987. Successful keeping of the European mole (Talpa europaea) in captivity. J. Zool. 212:2369–73
    [Google Scholar]
  40. 40.
    Borroni A, Loy A, Capanna E. 1999. A flexible arrangement for the study of moles in captivity. Acta Theriol. 44:207–14
    [Google Scholar]
  41. 41.
    García-López de Hierro L, Moleón M, Lupiáñez DG, Virgós E, Jiménez R. 2013. Positive and negative unintended human-induced effects on Iberian mole abundance at the edge of its distribution area. Mamm. Biol. 78:4276–82
    [Google Scholar]
  42. 42.
    Jiménez R, Burgos M, Sánchez A, Diaz De La Guardia R. 1990. The reproductive cycle of Talpa occidentalis in the southeastern Iberian Peninsula. Acta Theriol. 35:1–2165–69
    [Google Scholar]
  43. 43.
    Barrionuevo FJ, Zurita F, Burgos M, Jiménez R. 2004. Developmental stages and growth rate of the mole Talpa occidentals (Insectivora, Mammalia). J. Mammal. 85:1120–25
    [Google Scholar]
  44. 44.
    Sterba O. 1977. Prenatal development of central European insectivores. Folia Zool 26:127–44
    [Google Scholar]
  45. 45.
    Godfrey G, Crowcroft P. 1960. The Life of the Mole (Talpa auropaea Linnaeus) London: Museum
    [Google Scholar]
  46. 46.
    Matthews LH. 1935. 24. The œstrous cycle and intersexuality in the female mole (Talpa europaea Linn. Proc. Zool. Soc. Lond. 105:2347–84
    [Google Scholar]
  47. 47.
    Gorman ML, Stone RD. 1990. The Natural History of Moles Ithaca, NY: Comstock Publ. Assoc.
  48. 48.
    Zurita F, Barrionuevo FJ, Berta P, Ortega E, Burgos M, Jiménez R. 2003. Abnormal sex-duct development in female moles: the role of anti-Müllerian hormone and testosterone. Int. J. Dev. Biol. 47:6451–58
    [Google Scholar]
  49. 49.
    MacLeod J. 1880. Contribution a l'étude de la structure de l'ovaire des mammifères. Arch. Biol. 1:241–78
    [Google Scholar]
  50. 50.
    Jiménez R, Burgos M, Sánchez A, Sinclair AH, Alarcón FJ et al. 1993. Fertile females of the mole Talpa occidentalis are phenotypic intersexes with ovotestes. Development 118:41303–11
    [Google Scholar]
  51. 51.
    Carmona FD, Lupiáñez DG, Real FM, Burgos M, Zurita F, Jiménez R. 2009. SOX9 is not required for the cellular events of testicular organogenesis in XX mole ovotestes. J. Exp. Zool. B 312B:7734–48
    [Google Scholar]
  52. 52.
    Barrionuevo FJ, Zurita F, Burgos M, Jiménez R. 2004. Testis-like development of gonads in female moles. New insights on mammalian gonad organogenesis. Dev. Biol. 268:139–52
    [Google Scholar]
  53. 53.
    Lupiáñez DG, Real FM, Dadhich RK, Carmona FD, Burgos M et al. 2012. Pattern and density of vascularization in mammalian testes, ovaries, and ovotestes. J. Exp. Zool. B 318:3170–81
    [Google Scholar]
  54. 54.
    Zurita F, Carmona FD, Lupiáñez DG, Barrionuevo FJ, Guioli S et al. 2007. Meiosis onset is postponed to postnatal stages during ovotestis development in female moles. Sex. Dev. 1:166–76
    [Google Scholar]
  55. 55.
    Beolchini F, Rebecchi L, Capanna E, Bertolani R. 2000. Female gonad of moles, genus Talpa (Insectivora, Mammalia): Ovary or ovotestis?. J. Exp. Zool. 286:7745–54
    [Google Scholar]
  56. 56.
    Jost A. 1953. Problems of fetal endocrinology: the gonadal and hypophyseal hormones. Recent Prog. Horm. Res. 8:379–418
    [Google Scholar]
  57. 57.
    Watson M. 1877. On the female generative organs of Hyaena crocuta. Proc. Zool. Soc. Lond. 1877:369–79
    [Google Scholar]
  58. 58.
    Neaves WB, Griffin JE, Wilson JD. 1980. Sexual dimorphism of the phallus in spotted hyaena (Crocuta crocuta). J. Reprod. Fertil. 59:2509–13
    [Google Scholar]
  59. 59.
    Matthews LH. 1939. Reproduction in the spotted hyaena, Crocuta crocuta (Erxleben). Philos. Trans. R. Soc. B 230:5651–78
    [Google Scholar]
  60. 60.
    Drea CM, Coscia EM, Glickman SB 1999. Hyenas. Encyclopedia of Reproduction E Knobil, JD Neill 718–24 San Diego: Academic. , 1st ed..
    [Google Scholar]
  61. 61.
    Drea CM, Place NJ, Weldele ML, Coscia EM, Licht P, Glickman SE. 2002. Exposure to naturally circulating androgens during foetal life incurs direct reproductive costs in female spotted hyenas, but is prerequisite for male mating. Proc. R. Soc. Lond. B 269:15041981–87
    [Google Scholar]
  62. 62.
    Frankand LG, Glickman SE. 1994. Giving birth through a penile clitoris: parturition and dystocia in the spotted hyaena (Crocuta crocuta). J. Zool. 234:4659–65
    [Google Scholar]
  63. 63.
    Schneider KM. 1926. Uber hyanenzucht. Die Peltierzucht 2:1–4
    [Google Scholar]
  64. 64.
    Cunha GR, Wang Y, Place NJ, Liu W, Baskin L, Glickman SE. 2003. Urogenital system of the spotted hyena (Crocuta crocuta Erxleben): a functional histological study. J. Morphol. 256:2205–18
    [Google Scholar]
  65. 65.
    Rubenstein NM, Cunha GR, Wang YZ, Campbell KL, Conley AJ et al. 2003. Variation in ovarian morphology in four species of New World moles with a peniform clitoris. Reproduction 126:6713–19
    [Google Scholar]
  66. 66.
    Sinclair AW, Glickman S, Baskin L, Cunha GR. 2016. Anatomy of mole external genitalia: setting the record straight. Anat. Rec. 299:3385–99
    [Google Scholar]
  67. 67.
    Cadet de Vaux AA 1803. De la taupe, de ses moeurs, de ses habitudes et des moyens de la détruire Paris: Jean-Baptiste-Louis Colas
  68. 68.
    Saint-Hilaire EG. 1829. Cours de l'histoire naturelledes mammifères Paris: Pichon et Didier
  69. 69.
    Szykman M, Horn RV, Engh A, Boydston E, Holekamp K. 2007. Courtship and mating in free-living spotted hyenas. Behaviour 144:7815–46
    [Google Scholar]
  70. 70.
    East ML, Hofer H, Wickler W. 1993. The erect “penis” is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behav. Ecol. Sociobiol. 33:6355–70
    [Google Scholar]
  71. 71.
    Schneider KM. 1952. Einige bilder zur paarung der fleckenhyane, Crocutta crocuta. Erxl Deutsche Zool. Gart. 19:135–49
    [Google Scholar]
  72. 72.
    Szykman M. 2001. Sexual behavior and male mate choice in the spotted hyena Crocuta crocuta. PhD thesis, Mich. State Univ., East Lansing
  73. 73.
    East ML, Burke T, Wilhelm K, Greig C, Hofer H. 2003. Sexual conflicts in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure. Proc. R. Soc. Lond. B 270:15211247–54
    [Google Scholar]
  74. 74.
    Holekamp KE, Smale L, Szykman M. 1996. Rank and reproduction in the female spotted hyaena. Reproduction 108:2229–37
    [Google Scholar]
  75. 75.
    Engh AL, Funk SM, Horn RCV, Scribner KT, Bruford MW et al. 2002. Reproductive skew among males in a female-dominated mammalian society. Behav. Ecol. 13:2193–200
    [Google Scholar]
  76. 76.
    Grassé PP 1955. Order des insectivores. Anatomie et reproduction PP Grassé 1574–711 Traité Zool. Mammif. 17 Paris: Masson & Co.
    [Google Scholar]
  77. 77.
    Stark D. 1965. Embryologie Stuttgart, Ger: Thieme Publ.
  78. 78.
    Vernhout JH. 1894. Über die placenta des maulwurfs. Anat. Hefte 5:1–49
    [Google Scholar]
  79. 79.
    Hofer H, East ML. 2008. Siblicide in Serengeti spotted hyenas: a long-term study of maternal input and cub survival. Behav. Ecol. Sociobiol. 62:3341–51
    [Google Scholar]
  80. 80.
    Wahaj SA, Place NJ, Weldele ML, Glickman SE, Holekamp KE. 2007. Siblicide in the spotted hyena: analysis with ultrasonic examination of wild and captive individuals. Behav. Ecol. 18:6974–84
    [Google Scholar]
  81. 81.
    Wachter B, Höner OP, East ML, Golla W, Hofer H. 2002. Low aggression levels and unbiased sex ratios in a prey-rich environment: No evidence of siblicide in Ngorongoro spotted hyenas (Crocuta crocuta). Behav. Ecol. Sociobiol. 52:4348–56
    [Google Scholar]
  82. 82.
    Cunha GR, Risbridger G, Wang H, Place NJ, Grumbach M et al. 2014. Development of the external genitalia: perspectives from the spotted hyena (Crocuta crocuta). Differentiation 87:14–22
    [Google Scholar]
  83. 83.
    East M, Hofer H, Turk A. 1989. Functions of birth dens in spotted hyaenas (Crocuta crocuta). J. Zool. 219:4690–97
    [Google Scholar]
  84. 84.
    Frank LG, Weldele ML, Glickman SE. 1995. Masculinization costs in hyaenas. Nature 377:6550584–85
    [Google Scholar]
  85. 85.
    Holekamp KE, Dloniak SM. 2010. Intraspecific variation in the behavioral ecology of a tropical carnivore, the spotted hyena. Adv. Study Behav. 42:189–229
    [Google Scholar]
  86. 86.
    East ML, Hofer H. 2002. Conflict and cooperation in a female-dominated society: a reassessment of the “hyperaggressive” image of spotted hyenas. Adv. Study Behav. 31:1–30
    [Google Scholar]
  87. 87.
    Bronson FH. 2009. Climate change and seasonal reproduction in mammals. Philos. Trans. R. Soc. B 364:15343331–40
    [Google Scholar]
  88. 88.
    Lao-Pérez M, Massoud D, Real FM, Hurtado A, Ortega E et al. 2021. Mediterranean pine vole, Microtus duodecimcostatus: a paradigm of an opportunistic breeder. Animals 11:61639
    [Google Scholar]
  89. 89.
    López-Fuster MJ, Gosálvez J, Lluch S. 1988. Characteristics of the reproductive cycle of the mole, Talpa europaea, in the northeast of the Iberian peninsula. Acta Theriol. 33:131–37
    [Google Scholar]
  90. 90.
    Adams L. 1903. A contribution to our knowledge of the mole (Talpa europaea). Mem. Lit. Philos. Soc. Manch. Old Ser. 47:1–39
    [Google Scholar]
  91. 91.
    Dadhich RK, Real FM, Zurita F, Barrionuevo FJ, Burgos M, Jiménez R. 2010. Role of apoptosis and cell proliferation in the testicular dynamics of seasonal breeding mammals: a study in the Iberian mole, Talpa occidentalis. Biol. Reprod. 83:183–91
    [Google Scholar]
  92. 92.
    Dadhich RK, Barrionuevo FJ, Real FM, Lupiañez DG, Ortega E et al. 2013. Identification of live germ-cell desquamation as a major mechanism of seasonal testis regression in mammals: a study in the Iberian mole (Talpa occidentalis). Biol. Reprod. 88:4101
    [Google Scholar]
  93. 93.
    Sánchez A, Bullejos M, Burgos M, Hera C, Stamatopoulos C et al. 1996. Females of four mole species of genus Talpa (Insectivora, Mammalia) are true hermaphrodites with ovotestes. Mol. Reprod. Dev. 44:3289–94
    [Google Scholar]
  94. 94.
    Whitworth DJ, Licht P, Racey PA, Glickman SE. 1999. Testis-like steroidogenesis in the ovotestis of the European mole, Talpa europaea. Biol. Reprod. 60:2413–18
    [Google Scholar]
  95. 95.
    Mills MGL. 1990. Kalahari Hyaenas: The Behavioural Ecology of Two Species London: Unwin Hyman
  96. 96.
    Holekamp KE, Szykman M, Boydston EE, Smale L. 1999. Association of seasonal reproductive patterns with changing food availability in an equatorial carnivore, the spotted hyaena (Crocuta crocuta). Reproduction 116:187–93
    [Google Scholar]
  97. 97.
    Barrionuevo FJ, Burgos M, Scherer G, Jiménez R. 2012. Genes promoting and disturbing testis development. Histol. Histopathol. 27:1361–83
    [Google Scholar]
  98. 98.
    Lin Y-T, Capel B. 2015. Cell fate commitment during mammalian sex determination. Curr. Opin. Genet. Dev. 32:144–52
    [Google Scholar]
  99. 99.
    Stévant I, Nef S. 2019. Genetic control of gonadal sex determination and development. Trends Genet. 35:5346–58
    [Google Scholar]
  100. 100.
    Josso N, Cate RL, Picard J-Y, Vigier B, Di Clemente N et al. 1993. Anti-Müllerian hormone: the Jost factor. Recent Prog. Horm. Res. Cambridge, MA: Academic
    [Google Scholar]
  101. 101.
    Behringer RR, Finegold MJ, Cate RL. 1994. Müllerian-inhibiting substance function during mammalian sexual development. Cell 79:3415–25
    [Google Scholar]
  102. 102.
    Hannema SE, Hughes IA. 2007. Regulation of Wölffian duct development. Horm. Res. Paediatr. 67:3142–51
    [Google Scholar]
  103. 103.
    Merchant-Larios H, Taketo T. 1991. Testicular differentiation in mammals under normal and experimental conditions. J. Electron Microsc. Tech. 19:2158–71
    [Google Scholar]
  104. 104.
    Burgoyne P, Palmer S. 1993. Cellular basis of sex determination and sex reversal in mammals. Gonadal Development and Function SG Hillier17–29 New York: Raven
    [Google Scholar]
  105. 105.
    Mossman HW, Duke KL. 1973. Comparative Morphology of the Mammalian Ovary Madison: Univ. Wis. Press
  106. 106.
    Peters H, Levy E, Crone M. 1965. Oogenesis in rabbits. J. Exp. Zool. 158:2169–79
    [Google Scholar]
  107. 107.
    Yao HHC, Matzuk MM, Jorgez CJ, Menke DB, Page DC et al. 2004. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev. Dyn. 230:2210–15
    [Google Scholar]
  108. 108.
    Real FM, Haas SA, Franchini P, Xiong P, Simakov O et al. 2020. The mole genome reveals regulatory rearrangements associated with adaptive intersexuality. Science 370:6513208–14
    [Google Scholar]
  109. 109.
    Bowles J, Feng C-W, Spiller C, Davidson T-L, Jackson A, Koopman P 2010. FGF9 suppresses meiosis and promotes male germ cell fate in mice. Dev. Cell 19:3440–49
    [Google Scholar]
  110. 110.
    Sinclair AW, Glickman S, Catania K, Shinohara A, Baskin L, Cunha GR. 2017. Comparative morphology of the penis and clitoris in four species of moles (Talpidae). J. Exp. Zool. B 328:3275–94
    [Google Scholar]
  111. 111.
    Cunha GR, Place NJ, Baskin L, Conley A, Weldele M et al. 2005. The ontogeny of the urogenital system of the spotted hyena (Crocuta crocuta Erxleben). Biol. Reprod. 73:3554–64
    [Google Scholar]
  112. 112.
    Conley A, Place NJ, Legacki EL, Hammond GL, Cunha GR et al. 2020. Spotted hyaenas and the sexual spectrum: reproductive endocrinology and development. J. Endocrinol. 247:1R27–44
    [Google Scholar]
  113. 113.
    Drea CM, Weldele ML, Forger NG, Coscia EM, Frank LG et al. 1998. Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 2. Effects of prenatal anti-androgens. Reproduction 113:1117–27
    [Google Scholar]
  114. 114.
    Hammond GL. 2016. Plasma steroid-binding proteins: primary gatekeepers of steroid hormone action. J. Endocrinol. 230:1R13–25
    [Google Scholar]
  115. 115.
    Hammond GL, Miguel-Queralt S, Yalcinkaya TM, Underhill C, Place NJ et al. 2012. Phylogenetic comparisons implicate sex hormone-binding globulin in “masculinization” of the female spotted hyena (Crocuta crocuta). Endocrinology 153:31435–43
    [Google Scholar]
  116. 116.
    Jiménez R, Alarcón FJ, Sánchez A, Burgos M, Díaz de la Guardia R 1996. Ovotestis variability in young and adult females of the mole Talpa occidentalis (Insectivora, Mammalia). J. Exp. Zool. 274:2130–37
    [Google Scholar]
  117. 117.
    Dadhich RK, Barrionuevo FJ, Lupiañez DG, Real FM, Burgos M, Jiménez R. 2011. Expression of genes controlling testicular development in adult testis of the seasonally breeding Iberian mole. Sex. Dev. 5:277–88
    [Google Scholar]
  118. 118.
    Carmona FD, Motokawa M, Tokita M, Tsuchiya K, Jiménez R, Sánchez-Villagra MR. 2008. The evolution of female mole ovotestes evidences high plasticity of mammalian gonad development. J. Exp. Zool. B 310B:3259–66
    [Google Scholar]
  119. 119.
    Loy A, Beolchini F, Martullo S, Capanna E. 1994. Territorial behaviour of Talpa romana in an olivegrove habitat in central Italy. Boll. Zool. 61:3207–11
    [Google Scholar]
  120. 120.
    Ishii N. 1982. Reproductive activity of the Japanese shrew-mole, Urotrichus talpoides Temminck. J. Mammal. Soc. Japan 9:25–36
    [Google Scholar]
  121. 121.
    Ishii N. 1993. Size and distribution of home ranges of the Japanese shrew-mole Urotrichus talpoides. J. Mammal. Soc. Japan 18:287–98
    [Google Scholar]
  122. 122.
    Wingfield JC. 1994. Regulation of territorial behavior in the sedentary song sparrow, Melospiza melodia morphna. Horm. Behav. 28:11–15
    [Google Scholar]
  123. 123.
    Wingfield JC. 1994. Control of territorial aggression in a changing environment. Psychoneuroendocrinology 19:5709–21
    [Google Scholar]
  124. 124.
    Wingfield JC. 2005. A continuing saga: the role of testosterone in aggression. Horm. Behav. 48:3253–55
    [Google Scholar]
  125. 125.
    Cunningham RL, Lumia AR, McGinnis MY. 2012. Androgen receptors, sex behavior, and aggression. Neuroendocrinology 96:2131–40
    [Google Scholar]
  126. 126.
    Bhasin S, Woodhouse L, Storer TW. 2003. Androgen effects on body composition. Growth Horm. IGF Res. 13:S63–71
    [Google Scholar]
  127. 127.
    Smale L, Frank LG, Holekamp KE. 1993. Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with adult females and immigrant males. Anim. Behav. 46:3467–77
    [Google Scholar]
  128. 128.
    McCormick SK, Holekamp KE, Smale L, Weldele ML, Glickman SE, Place NJ. 2021. Sex differences in spotted hyenas. Cold Spring Harbor Perspect. Biol. 14:6a039180
    [Google Scholar]
  129. 129.
    Holekamp KE, Swanson EM, Van Meter PE. 2013. Developmental constraints on behavioural flexibility. Philos. Trans. R. Soc. Lond. B 368:161820120350
    [Google Scholar]
  130. 130.
    French JA, Mustoe AC, Cavanaugh J, Birnie AK. 2013. The influence of androgenic steroid hormones on female aggression in “atypical” mammals. Philos. Trans. R. Soc. Lond. B 368:163120130084
    [Google Scholar]
  131. 131.
    Baker MG. 1990. Effects of ovariectomy on dyadic aggression and submission in a colony of peri-pubertal spotted hyenas (Crocuta crocuta) Master's Thesis, Univ. Calif. Berkeley:
    [Google Scholar]
  132. 132.
    Gould SJ. 1981. Hyena myths and realities. Nat. Hist. 90:1–16
    [Google Scholar]
  133. 133.
    Gould SJ, Vrba ES. 1982. Exaptation—a missing term in the science of form. Paleobiology 8:14–15
    [Google Scholar]
  134. 134.
    Hamilton WJ III, Tilson RL, Frank LG 1986. Sexual monomorphism in spotted hyenas, Crocuta crocuta. Ethology 71:163–73
    [Google Scholar]
  135. 135.
    Monaghan EP, Glickman SE 1992. Hormones and aggressive behavior. Behavioral Endocrinology JB Becker 261–85 Cambridge, MA: MIT Press
    [Google Scholar]
  136. 136.
    Frank LG. 1997. Evolution of genital masculinization: Why do female hyaenas have such a large “penis”?. Trends Ecol. Evol. 12:258–62
    [Google Scholar]
  137. 137.
    Kruuk H. 1972. The Spotted Hyaena: A Study of Predation and Social Behavior Chicago: Univ. Chicago Press
  138. 138.
    Muller MN, Wrangham R. 2002. Sexual mimicry in hyenas. Q. Rev. Biol. 77:13–16
    [Google Scholar]
  139. 139.
    Holekamp KE. 2006. Spotted hyenas.. Curr. Biol. 16:22R944–45
    [Google Scholar]
  140. 140.
    Smith JE, Holekamp KE 2019. Spotted hyenas. Encyclopedia of Animal Behavior MD Breed, J Moore 190–208 Cambridge, MA: Academic
    [Google Scholar]
  141. 141.
    Curren LJ, Weldele ML, Holekamp KE. 2013. Ejaculate quality in spotted hyenas: intraspecific variation in relation to life-history traits. J. Mammal. 94:190–99
    [Google Scholar]
  142. 142.
    Soulsbury CD. 2010. Genetic patterns of paternity and testes size in mammals. PLOS ONE 5:3e9581
    [Google Scholar]
  143. 143.
    Iossa G, Soulsbury CD, Baker PJ, Harris S 2008. Sperm competition and the evolution of testes size in terrestrial mammalian carnivores. Funct. Ecol. 22:4655–62
    [Google Scholar]
  144. 144.
    Peyre A. 1961. Recherches sur l'intersexualite specifique chez Galemys pyrenaicus G. Arch. Biol. 73:1–174
    [Google Scholar]
  145. 145.
    Sánchez-Villagra MR, Horovitz I, Motokawa M. 2006. A comprehensive morphological analysis of talpid moles (Mammalia) phylogenetic relationships. Cladistics 22:159–88
    [Google Scholar]
  146. 146.
    Cabria MT, Rubines J, Gómez-Moliner B, Zardoya R. 2006. On the phylogenetic position of a rare Iberian endemic mammal, the Pyrenean desman (Galemys pyrenaicus). Gene 375:1–13
    [Google Scholar]
  147. 147.
    Grenyer R, Purvis A. 2003. A composite species-level phylogeny of the “Insectivora” (Mammalia: order Lipotyphla Haeckel, 1866). J. Zool. 260:3245–57
    [Google Scholar]
  148. 148.
    Zhou C, Liu Y, Qiao L, Lan Y, Price M et al. 2020. Genome-wide analyses provide insights into the scavenging lifestyle of the striped hyena (Hyaena hyaena). DNA Cell Biol. 39:101872–85
    [Google Scholar]
  149. 149.
    Shao Y, Wang X-B, Zhang M-L, Liu Y, Wang S et al. 2022. Long-read genome sequencing provides molecular insights into scavenging and societal complexity in spotted hyena Crocuta crocuta. Mol. Biol. Evol. 39:3msac011
    [Google Scholar]
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