lactin, and estrogen all affect reproductive activity (Bron-
son and Whitten 1968; Bronson and Stetson 1973; Bronson
1975; Bronson and Maruniak 1976).
In mice, urine that accelerates puberty also synchronizes
estrus among grouped adults (known as the Lee-Boot and
Whitten effects; Drickamer 1992, unpublished data). Many
aspects of the synchronization phenomenon are similar
to the acceleration of puberty. These aspects include the
seasonality, testosterone-dependency, and small dosages
needed for effect. The chemical nature of the compound
involved appears to be the same as for puberty acceleration
(Novotny et al. 1998, 1999a, 1999b)
The following is known about these acceleration and
synchronization of estrous cycle effects in other rodents.
For prairie voles (Microtus ochrogaster), activation of re-
production in young virgin females and in adult females
is stimulated by a male chemosignal (Batzli et al. 1977;
Carter et al. 1980, 1987; Gavish et al. 1983). There may
be some intraspecific variation in this phenomenon in that
prairie voles from Kansas were more responsive than those
from Illinois (Roberts et al. 1998). Among voles, accelera-
tion or activation of reproduction has also been recorded
for meadow voles (M. pennsylvanicus;Baddaloo and Clu-
low 1981) and pine voles (M. pinetorum;Lepri and Van-
denbergh 1986; Solomon et al. 1996), but not for Califor-
nia voles (M. californicus;Rissman and Johnston 1985).
For deer mice, only a few studies have been conducted
to explore acceleration of female sexual maturation or syn-
chronization of estrus in adults. For prairie deer mice (Per-
omyscus maniculatus bairdii), exposure to a male or male
urine synchronizes estrus in females caged in groups (Whit-
ten effect; Bronson and Marsden 1964; Marsden and Bron-
son 1964, 1965b; Bronson and Dezell 1968). Terman (1984)
reported just the opposite finding; females reared in the
presence of a male or male urine had smaller ovaries and
fewer corpora lutea than females treated with water. There
apparently have not been any studies that reported acceler-
ation of puberty or induction of estrus in adult female deer
mice following exposure to male urine. At this time, con-
siderable work remains to be done to obtain a better picture
of acceleration of reproduction in Peromyscus. The limited
results to date provide some contradictions, and no consis-
tent picture has emerged with regard to possible male ac-
celeration of female puberty.
Delaying effects
Two related phenomena that characterize a delay in repro-
duction in rodents are that grouping among females tends
to keep them in anestrus and that groups of females or urine
from grouped females delays puberty in young females. I
prefer the term “delay” for both of these phenomena rather
than the widely used “inhibition” and “suppression,” be-
cause the latter imply an absence of estrus or puberty.
Rather, this grouping or urine from grouped females tends
to slow the timing of reproduction to varying degrees, but
females still exhibit estrous cycles and young females attain
a first vaginal estrus and puberty. The same list of reviews,
cited in the previous section on acceleration effects, con-
tains summaries of many aspects of these reproduction-
delaying processes.
The disruption of estrous patterns in adult females that
are grouped was first discovered by Whitten (1959) and
later attributed to a urinary chemosignal (Whitten et al.
1968; McClintock 1983). The delay in sexual maturation
in young mice was first reported for young females housed
in groups (Vandenbergh et al. 1972) and was investigated
in a series of studies exploring various facets of this phe-
nomenon (Drickamer 1974b, 1977a, 1984a, 1984e, 1986b,
1986c; Drickamer and Assmann 1981; Coppola and Van-
denbergh 1985). Based on laboratory studies, the urinary
delay substance is produced by females housed in groups, is
effective in very small doses, is received by the vomeronasal
organ of prepubertal females, elicits the same response
in females independent of the relatedness of the male, and
is released by grouped females only after several weeks of
caging at high density. When young females are exposed to
both male urine and urine from grouped females, the lat-
ter takes precedence, except when the relative proportions
involve considerably more urine from males than from
grouped females (Drickamer 1982, 1988).
Limited work has been done on urinary chemosignal ef-
fects producing delays in puberty or induction of estrus in
Microtus. For meadow voles, females housed in groups
have lighter-weight ovaries and uteri than females housed
alone (Pasley and McKinney 1973), suggesting that group-
ing delays or inhibits sexual maturation. Delay of sexual
maturation for grouped females has been reported for prai-
rie voles and California voles but not for meadow voles
(Batzli et al. 1977). In contrast, Wolff et al. (2001) found no
delays or inhibition of reproduction in young female
meadow voles or prairie voles raised in the presence versus
the absence of their mothers.
Conflicting results have been reported forPeromyscusre-
garding the effects of a urinary chemosignal on attainment
of puberty. Terman (1984, 1993) reported that young fe-
male white-footed mice (Peromyscus leucopus) caged with
an adult female reproduced at a higher rate than females
caged alone. On the other hand, the presence of an adult
female (Haigh et al. 1988) or soiled bedding from adult fe-
males (Bediz and Whitsett 1979; Haigh 1987; Haigh et al.
1985) delayed reproduction in young female white-footed108 Chapter Nine