Combined Olfactory Contact with the Parent Colony and Direct Contact with Nonbreeding Animals Does Not Maintain Suppression of Ovulation in Female Naked Mole-Rats (Heterocephalus glaber)

The study investigated the role of odor cues from two naked mole-rat colonies, in conjunction with behavioral cues from nonbreeding colony members, in maintaining suppression of ovulation in subordinate female naked mole-rats isolated from the two parent colonies. Four high ranking nonbreeding female naked mole-rats were removed from their respective parent colonies and singly housed in separate burrow systems. For a 64-day period, the removed females were maintained in daily odor contact with their parent colony by daily rotating soiled bedding material between the parent colony and the burrow systems of removed females. In addition, subsets of nonbreeding animals from the respective parent colony were regularly moved into the burrow systems of removed females for 2-day periods during this 64-day period. Removed females were therefore in continual social contact with subsets of parent colony animals except for the breeding pair. All four removed females exhibited raised levels of urinary progesterone (< 2 ng/mg Cr) indicative of the onset of ovarian function within 3 days of being separated from the parent colony. Removed females exhibited a normal ovulatory cycle with levels of progesterone remaining elevated for 25-35 days (mean concentration of progesterone +/- SEM; 16.2 +/- 2 ng/mg Cr). Initiation of aggression and sexual behavior by removed females increased significantly when they were isolated from the parent colony. The results demonstrated that odor cues from the complete colony in conjunction with behavioral/tactile/vocal cues from the nonbreeding colony members were not the major cues maintaining reproductive suppression in nonbreeding female naked mole-rats. Instead, our results suggest that female reproductive suppression in naked mole-rats is caused by a dominance-related behavioral mechanism requiring direct contact with the breeding female.

[1]  J. Jarvis,et al.  Social suppression of ovarian cyclicity in captive and wild colonies of naked mole-rats, Heterocephalus glaber. , 1990, Journal of reproduction and fertility.

[2]  J. Hoogland,et al.  The Black-Tailed Prairie Dog: Social Life of a Burrowing Mammal , 1995 .

[3]  J. Hodges,et al.  Social status controls LH secretion and ovulation in female marmoset monkeys (Callithrix jacchus). , 1988, The Journal of endocrinology.

[4]  M. O'Riain,et al.  A dispersive morph in the naked mole-rat , 1996, Nature.

[5]  M. Perret,et al.  Chemical signals and reproductive capactiy in a male prosimian primate (Microcebus murinus) , 1987 .

[6]  D. Kleiman,et al.  Endocrine correlates of behavioural oestrus in the female giant panda (Ailuropoda melaneleuca) and associated hormonal changes in the male. , 1982, Journal of reproduction and fertility.

[7]  E. Wilson The Insect Societies , 1974 .

[8]  S. Milligan Pregnancy blocking in the vole, Microtus agrestis. I. Effect of the social environment. , 1976, Journal of reproduction and fertility.

[9]  C. G. Faulkes,et al.  Evidence that primer pheromones do not cause social suppression of reproduction in male and female naked mole-rats (Heterocephalus glaber). , 1993, Journal of reproduction and fertility.

[10]  C. G. Faulkes,et al.  Social control of reproduction in breeding and non-breeding male naked mole-rats (Heterocephalus glaber). , 1991, Journal of reproduction and fertility.

[11]  P. Sherman,et al.  The Biology of the Naked Mole-Rat , 2017 .

[12]  J. Jarvis,et al.  Social suppression of reproduction in male naked mole-rats, Heterocephalus glaber. , 1991, Journal of reproduction and fertility.

[13]  J. Jarvis,et al.  LH responses of female naked mole-rats, Heterocephalus glaber, to single and multiple doses of exogenous GnRH. , 1990, Journal of reproduction and fertility.

[14]  D. Abbott,et al.  Extension of reproductive suppression by pheromonal cues in subordinate female marmoset monkeys, Callithrix jacchus. , 1990, Journal of reproduction and fertility.

[15]  S. Wasser,et al.  Reproductive Suppression Among Female Mammals: Implications for Biomedicine and Sexual Selection Theory , 1983, The Quarterly Review of Biology.

[16]  R. Steiner,et al.  Luteal phase deficiency: abnormal gonadotropin and progesterone secretion patterns. , 1989, The Journal of clinical endocrinology and metabolism.

[17]  M. Perret,et al.  Sexual inhibition in a prosimian primate: a pheromone-like effect. , 1984, The Journal of endocrinology.

[18]  F. Bronson,et al.  Male-induced puberty in female mice: evidence for a synergistic action of social cues. , 1975, Biology of reproduction.

[19]  D. Abbott,et al.  Sensory cues and the suppression of reproduction in subordinate female marmoset monkeys, Callithrix jacchus. , 1993, Journal of reproduction and fertility.

[20]  Dietland Müller-Schwarze,et al.  Chemical Signals in Vertebrates 3 , 1983 .

[21]  Susan W. Margulis,et al.  Behavioral and Hormonal Changes in Female Naked Mole-Rats (Heterocephalus glaber) Following Removal of the Breeding Female from a Colony , 1995, Hormones and Behavior.

[22]  S. Creel,et al.  Behavioural and endocrine mechanisms of reproductive suppression in Serenge dwarf mongooses , 1992, Animal Behaviour.

[23]  Sandra L. Vehrencamp,et al.  A model for the evolution of despotic versus egalitarian societies , 1983, Animal Behaviour.

[24]  Laurent Keller,et al.  Forum The eusociality continuum , 1995 .