Seasonal reproduction and delayed sexual maturity in mound-building mice Mus spicilegus
Patrick Gouat A B , Christophe Féron A and Simone Demouron A
+ Author Affiliations
- Author Affiliations
A Laboratoire d’Ethologie Expérimentale et Comparée, Université de Paris Nord, FRE CNRS 2413, 93430 Villetaneuse, France.
B To whom correspondence should be addressed. email: patrick.gouat@leec.univ-paris13.fr
Reproduction, Fertility and Development 15(3) 187-195 https://doi.org/10.1071/RD02105
Submitted: 18 December 2002 Accepted: 22 May 2003 Published: 22 May 2003
Abstract
In the mound-building mouse, Mus spicilegus, which is found from Central to Eastern Europe, reproduction is seasonal and limited to spring and summer. In autumn, the mice build voluminous mounds composed of vegetable matter covered with earth, where juvenile animals (autumnal individuals) over-winter in groups without reproducing. Autumnal animals delay reproduction until the next spring when they are 6 months old. The influence and interactions of environmental (short light period and cold temperature (C conditions) compared with long light period and temperate temperature (T conditions)) and social factors (lack of odours from breeding adults (NB conditions) compared with presence of odours from breeding adults (B conditions)) on reproduction and sexual maturation were studied. Forty groups of three autumnal individuals (two males and a female or two females and a male) were placed in four experimental conditions (CB, CNB, TB and TNB), corresponding to interactions between environmental and social factors (n = 10 groups for each condition). Of the 40 groups only one initiated reproduction during the 18 weeks of cohabitation. Subsequently, animals were separated and isolated for 1 month and then paired with unfamiliar partners. Reproduction was monitored for an additional month, and 24 out of 39 females reproduced. In addition, of eight reproducing pairs placed in C conditions and 10 reproducing pairs maintained in T conditions, all but one pair continued reproduction. It was concluded that the delay in reproduction observed in autumnal individuals was the result of the social effects of living in groups as opposed to the environmental conditions of winter.
Acknowledgments
We thank Claude Baudoin and Nicolas Busquet for their critical reading of the manuscript, and Lavinia Bruneau for revision of the English version of the manuscript.
References
Ambid, L. and Berges, R. (1986). Testicular activity and hibernation in a seasonal hibernating animal, the ground squirrel (Citellus tridecemlineatus). In
Barnett, S. A. , and Dickson, R. G. (1989). Wild mice in the cold: some findings on adaptation Biol. Rev. 64, 317–40.
| PubMed |
Bonhomme, F. (1992). Genetic diversity and evolution in the genus Mus. In
Bonhomme, F. , Catalan, J. , Gerasimov, S. , Orsini, P. , and Thaler, L. (1983). Le complexe d’espéces du genre Mus en Europe Centrale et Orientale. I. Génétique Z. Säugetierkd. 48, 78–85.(English abstract.)
Boursot, P. , Auffray, J.-C. , Britton-Davidian, J. , and Bonhomme, F. (1993). The evolution of house mice Annu. Rev. Ecol. Syst. 24, 119–152.
| Crossref | GoogleScholarGoogle Scholar |
Bronson, F. H. (1979). The reproductive ecology of the house mouse Q. Rev. Biol. 54, 265–99.
| PubMed |
Bronson, F. H., and Heideman, P. D. (1994). Seasonal regulation of reproduction in mammals.
Bronson, F. H. , and Marsteller, F. A. (1985). Effect of short-term food deprivation on reproduction in female mice Biol. Reprod. 33, 660–7.
| PubMed |
Carlsen, M. (1993). Migrations of Mus musculus musculus in Danish farmland Z. Säugetierkd. 58, 172–80.
Cassaing, J. (1984). Interactions intra- et interspécifiques chez les souris sauvages du Midi de la France, Mus musculus domesticus et Mus spretus: conséquences sur la compétition entre les deux espèces Biol. Behav. 9, 281–93.(English abstract.)
Cassaing, J. , and Croset, H. (1985). Organisation spatiale, compétition et dynamique des populations sauvages de souris (Mus spretus Lataste et Mus musculus domesticus Rutty) du midi de la France Z. Säugetierkd. 5, 271–84.(English abstract.)
Drickamer, L. C. (1982a). Acceleration and delay of puberty in female mice by urinary chemosignals from other females Dev. Psychobiol. 15, 433–45.
| PubMed |
Drickamer, L. C. (1982b). Acceleration and delay of first vaginal estrus in female mice by urinary chemosignals: dose levels and mixing urine treatment sources Anim. Behav. 30, 456–60.
Drickamer, L. C. (1984). Urinary chemosignals and puberty in female house mice: effects of photoperiod and food deprivation Physiol. Behav. 33, 907–11.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Drickamer, L. C , and Hoover, J. E. (1979). Effect of urine from pregnant and lactating female house mice on sexual maturation of juvenile females Dev. Psychobiol. 12, 545–51.
| PubMed |
Duryadi, D. (1993). Rôle possible du comportement dans 1’évolution de deux souris Mus macedonicus et Mus spicilegus en Europe centrale. PhD Thesis (Université Montpellier II: France.)
Féron, C. , and Gheusi, G. (2003). Social regulation of reproduction in the female mound-builder mouse (Mus spicilegus) Physiol. Behav. 79, 717–22.
| Crossref | GoogleScholarGoogle Scholar |
Fons, R. , and Saint Girons, M. C. (1993). Le cycle sexuel chez le mulot sylvestre, Apodemus sylvaticus (L., 1758) (Muridae) en région méditerranéenne Z. Säugetierkd. 58, 38–47.(English abstract.)
Garza, J. C. , Dallas, J. , Duryadi, D. , Gerasimov, S. , Croset, H. , and Boursot, P. (1997). Social structure of the mound-building mouse Mus spicilegus revealed by genetic analysis with microsatellites Mol. Ecol. 6, 1009–17.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gouat, P. , Katona, K. , and Poteaux, C. (2003). Is the socio–spatial distribution of mound-building mice, Mus spicilegus compatible with a monogamous mating system? Mammalia 67, 15–24.
Guénet, J. L. , and Bonhomme, F. (2003). Wild mice: an ever-increasing contribution to a popular mammalian model Trends Genetics 19, 24–31.
| Crossref | GoogleScholarGoogle Scholar |
Heideman, P. D. (2000). Environmental regulation of reproduction. In
Jemiolo, B. , Harvey, S. , and Novotny, M. (1986). Promotion of the Whitten effect in female mice by the synthetic analogs of male urinary constituents Proc. Natl Acad. Sci. USA 83, 4576–9.
| PubMed |
Jemiolo, B. , Andreolini, F. , Xie, T. M. , Wiesler, D. , and Novotny, M. (1989). Puberty-affecting synthetic analogs of urinary chemosignals in the house mouse, Mus domesticus. Physiol. Behav. 46, 293–8.
| Crossref | GoogleScholarGoogle Scholar |
Landau, I. T. , and Holmes, W. G. (1988). Mating of captive thirteen-lined ground squirrels and the annual timing of estrus Horm. Behav. 22, 474–87.
| PubMed |
Manning, J. M. , and Bronson, F. H. (1990). The effects of low temperature and food intake on ovulation in domestic mice Physiol. Zool. 63, 938–48.
McKinney, T. D. , and Desjardins, C. (1973). Intermale stimuli and testicular function in adult and immature house mice Biol. Reprod. 9, 370–8.
| PubMed |
Meek, L. R. , Lee, T. M , and Gallon, J. F. (1995). Interaction of maternal photoperiod history and food type on growth and reproductive development of laboratory meadow voles (Microtus pennsylvanicus) Physiol. Behav. 57, 905–11.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Milishnikov, A. N. , Rafiev, A. N. , and Muntianu, A. I. (1998). Genotypic variability in populations of moundbuilder mice Mus spicilegus Pet., 1882, at different life-cycle stages Russ. J. Genetics 34, 785–90.
Murariu, D. (1981). La présence de Mus musculus spicilegus Petenyi, 1882 dans le Delta du Danube accompagné de son ‘parasite’ Apodemus agrarius (Pall., 1771) Trav. Mus. Hist. Nat. Grigore Antipa 23, 297–304.(English abstract.)
Naumov, N. P. (1940). Ecology of the mound-builder mouse Mus musculus hortolanus Works Inst. Evol. Morphol. USSR 3, 33–76.(In Russian.)
Nelson, R. J. , and Shiber, J. R. (1990). Photoperiod affects reproductive responsiveness to 6-methoxy-2-benzoxazolinone in house mice Biol. Reprod. 43, 586–91.
| PubMed |
Nelson, R. J. , Badura, L. L , and Goldman, B. D. (1990). Mechanisms of seasonal cycles of behavior Annu. Rev. Psychol. 41, 81–108.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Novotny, M. , Xie, T. M. , Harvey, S. , Wiesler, D. , Jemiolo, B. , and Carmack, M. (1995). Stereoselectivity in mammalian chemical communication: male mouse pheromones Experientia 51, 738–43.
| PubMed |
Novotny, M. , Ma, W. , Wiesler, D. , and Zidek, L. (1999). Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein Proc. R. Soc. London 266, 2017–22.
| Crossref | GoogleScholarGoogle Scholar |
Orsini, P. , Bonhomme, F. , Britton-Davidian, J. , Croset, H. , Gerasimov, S. , and Thaler, L. (1983). Le complexe d’epèces du genre Mus en Europe Centrale et Orientale. II. Critères d’identification, répartition et caractéristiques écologiques Z. Säugetierkd. 48, 86–95.(English abstract.)
Pandey, S. C. , and Pandey, S. D. (1990). Photoperiodic influences on pheromonal delay of puberty in young female wild mice Zool. Sci. 7, 547–9.
Patris, B. , and Baudoin, C. (1998). Female sexual preferences differ in Mus spicilegus and Mus musculus domesticus: the role of familiarization and sexual experience Anim. Behav. 56, 1465–70.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Patris, B. , and Baudoin, C. (2000). A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus. Behav. Processes 51, 35–43.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Patris, B. , Gouat, P. , Jacquot, C. , Christophe, N. , and Baudoin, C. (2002). Agonistic and sociable behaviors in the mound-building mice, Mus spicilegus: a comparative study with Mus musculus domesticus. Aggress. Behav. 28, 75–84.
| Crossref | GoogleScholarGoogle Scholar |
Pelikán, J. (1981). Patterns of reproduction in the house mouse Symp. Zool. Soc. London 47, 205–29.
Perrigo, G. , and Bronson, F. H. (1983). Foraging effort, food intake, fat deposition and puberty in female mice Biol. Reprod. 29, 455–63.
| PubMed |
Perrigo, G. , and Bronson, F. H. (1985). Behavioral and physiological responses of female house mice to foraging variation Physiol. Behav. 34, 437–40.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pisareva, M. E. (1947). Contribution to ecology and systematics of the mound-building mouse Works Biol. Fac. Dnieppropetrovsk State Univ. 32, 68–71.(In Russian.)
Prendergast, B. J. , Kriegsfeld, L. J. , and Nelson, R. J. (2001). Photoperiodic polyphenisms in rodents: neuroendocrine mechanisms, costs, and functions Q. Rev. Biol. 76, 293–325.
| PubMed |
Sage, R. D. , Atchley, W. R. , and Capanna, E. (1993). House mice as models in systematic biology Syst. Biol. 42, 523–61.
Sokolov, V. E. , Kotenkova, E. V. , and Michailenko, A. G. (1998). Mus spicilegus. Mamm. Species 592, 1–6.
Suchomelová, E. , Munclinger, P. , and Frynta, D. (1998). New evidence of pseudosexual behaviour and female aggression in mice: neutral cage interactions in Mus spicilegus and Mus spretus (Rodentia: Muridae) Folia Zool. 47, 241–7.
Vandenbergh, J. G. (1971). The influence of the social environment on sexual maturation in male mice J. Reprod. Fertil. 24, 383–90.
| PubMed |
Vandenbergh, J. G. (1994). Pheromones and mammalian reproduction. In
Vandenbergh, J. G. , Whitsett, J. M. , and Lombardi, J. R. (1975). Partial isolation of a pheromone accelerating puberty in female mice J. Reprod. Fertil. 43, 515–23.
| PubMed |
Vandenbergh, J. G. , Finlayson, J. S. , Dobrogosz, W. J. , Dills, S. S. , and Kost, T. A. (1976). Chromatographic separation of puberty accelerating pheromone from male mouse urine Biol. Reprod. 15, 260–5.
| PubMed |
Whitten, W. K. (1956). Modification of the oestrus cycle of the mouse by external stimuli associated with the male J. Endocrinol. 13, 399–404.
| PubMed |
Whitten, W. K. (1966). Pheromones and mammalian reproduction. In
