Rodent Societies: An Ecological & Evolutionary Perspective

and the second involves the Whitten effect, or stimulation
and synchronization of estrus in adult females exposed to
males or male urine (see McClintock 1983; Vandenbergh
1983; Brown 1985a; Drickamer 1986a; and Vandenbergh
and Coppola 1986 for reviews).
For house mice, the acceleration of puberty is a function
of both male presence and the urinary chemosignal (Van-
denbergh 1967, 1969; Drickamer 1974a); puberty is accel-
erated most when both types of cues are present. The male
urinary chemosignal is testosterone dependent, with domi-
nant males producing more potent chemosignals than sub-
ordinate males (Vandenbergh 1969; Drickamer and Mur-
phy 1978). The acceleration effect is seasonal in that male
urine generally does not accelerate estrus or puberty in fe-
male mice during the winter nonreproductive period, but
does so for the remainder of the year including the repro-
ductive season (Drickamer 1987). The chemosignal in male
urine is effective in extremely small (0.0001 cc of urine /day)
doses (Drickamer 1982, 1984a) and is equally effective re-

gardless of whether treatment involves related or unrelated

donors or recipients (Drickamer 1984e). The acceleration

effect is blocked, with delays in puberty occurring, when

young females are treated with urine from both adult males

and grouped females (Drickamer 1982, 1988). Urine from

pregnant and lactating females and females in estrus cause

an acceleration of puberty in young female house mice

(Drickamer 1983, 1986a).

The chemical substance in male urine that is responsible

for acceleration of female puberty appears to be a volatile

compound, but is attached to mouse urinary proteins (Van-

denbergh et al. 1975, 1976; Nishimura et al. 1989; Novotny

et al. 1998, 1999a; Mucignat-Caretta et al. 1995). Con-

nections still need to be made between the role of mouse

urinary proteins and male-male interactions (Hurst et al.

1998, 2001) and the urinary chemosignal from males that

stimulates reproductive activity in female mice. Studies on

the underlying hormonal mechanisms reveal that follicle-

stimulating hormone (FSH), luteinizing hormone (LH), pro-

Acceleration and Delay of Reproduction in Rodents 107

Table 9.1 Summary of three chemosignal-mediated effects on reproduction in rodents

Evidence

Effect Genus For Against Field tests

Acceleration of puberty Mus Vandenbergh 1967, 1969; Drickamer Massey and Vandenbergh 1981; Drickamer
1974 and Mikesic 1990
Microtus Batzli et al. 1977; Carter et al. 1980
Peromyscus Terman 1984
Estrus synchronization Mus Whitten 1958, 1959; Marsden and
Bronson 1964
Microtus Carter et al. 1980; Gavish et al. 1983
Peromyscus Bronson and Marsden 1964; Marsden
and Bronson 1965b
Delay of puberty Mus Vandenbergh et al. 1972; Drickamer Massey and Vandenbergh 1980; Coppola
1974b, 1977a and Vandenbergh 1987; Drickamer and
Mikesic 1990
Microtus Pasley and McKinney 1973; Rodd and Batzli et al. 1977
Boonstra 1988
Peromyscus Haigh 1987; Haigh et al. 1985; Terman Terman 1984; Terman Kaufman and Kaufman 1989; Terman 1993;
1968; Terman and Bradley 1981 1993 Wolff 1992
Anestrus Mus Whitten 1959; Whitten et al. 1968;
Lee and Boot 1955, 1956
Microtus Pasley and McKinney 1973 Batzli et al. 1977
Peromyscus Terman 1965, 1968 Terman 1993; Kaufman and Kaufman 1989
Pregnancy termination Mus Bruce 1959, 1960, 1961; Parkes and Mahady and Wolff 2002;
Bruce 1962; Dominic 1969 Drickamer 1989
Microtus Clulow and Clarke 1968; Stehn and Mallory and Clulow 1977; de la Maza et al. 1999; Mahady and Wolff
Richmond 1975; Jannett 1980; Stehn de la Maza et al. 1999; 2002; Wolff 2003
and Jannett 198 Mahady and Wolff 2002
Peromyscus Bronson and Eleftheriou 1963;
Kennedy et al. 1977; Haigh 1988

NOTES: References are provided by genus for papers describing evidence for, against, and under field conditions for these three effects. All citations for and against are from lab-
oratory studies.