ELSEVIER Behavioural Brain Research 62 (1994) 119-125
BEHAVIOURAL
BRAIN
RESEARCH
Research Report
Males located caudally in the uterus affect sexual behavior of male rats in
adulthood
E.J. Houtsmuller a'*, J. Juranek b, C.E. Gebauer b, A.K. Slob a, D.L. Rowland b
a Department o! Endocrinology and Reproduction, Facultyof Medicine and Health Sciences, Erasmus Universi O" Rotterdam, PO Box 1738, 3000 DR
Rotterdam, The Netherlands b Department of Psycholog3'. Valparaiso Universio'. Valparaiso, IN 46383. USA
Received 26 February 1993: revised 19 November 1993; accepted 5 January 1994
Abstract
It has been suggested that the sexual differentiation of female rats is affected by androgens from male fetuses in the uterine horn
(intra-uterine position phenomenon). Effects of adjacent males, as well as of males located caudally in the uterus have been reported.
The present study investigated whether male rats, like females, are affected by the presence of either caudal or adjacent male litter-
mates. When tested in adulthood for sexual behavior, males that had male fetuses located caudally in the uterine horn showed shorter
latencies to the first mount or intromission and shorter latencies to ejaculation, and exhibited more mounts and intromissions per minute
than males that lacked caudal male siblings in the uterus. The presence of adjacent males did not significantly affect the parameters
studied in this experiment.
Key word~v Intra-uterine position; Sexual behavior; Ejaculation latency; Sexual differentiation; Caudal; Prenatal environment; Male
rat
1. Introduction
As a result of exposure to higher levels of testosterone
perinatally, male rats show more masculine sexual behav-
ior (mounts, intromissions and ejaculations) in adulthood
than females [2]. Testosterone secretion in male rat fe-
tuses starts around day 14 of gestation, and peaks on days
18 and 19 [3,22,28]. This testosterone not only affects
males" own sexual differentiation, but supposedly affects
female fetuses in the same uterine horn as well [9,19,26].
The manner in which androgens from males reach fe-
male fetuses remains uncertain. It has been reported that
females thai develop in utero between two males are more
masculinized behaviorally (i.e., show more mounting be-
havior) and somatically (i.e., have larger anogenital dis-
tances at birth) than females located between two females.
This finding prompted the hypothesis that androgens from
males reach females by diffusion through the amniotic
membrane {"adjacent male hypothesis") [9,26]. Support
for this hypothesis has most often been provided in studies
* Corresponding author. Present address: Dept. of Biological Sciences.
University of Notre Dame, Notre Dame, 1N 46556, USA. Fax: (1)(219)
631-7413. E-mail: Elisabcth J. Houtsmuller @nd.edu
0166-4328,94 $7.110 © 1994 Elsevier Science B.V. All rights reserved
SSDI 01 66-4328(94)00025- B
using mice and gerbils (e.g. [8,25,29,30]), although non-
supportive findings in mice and rats have been reported as
well [ 16,17,19]. In view of their disparate findings, Meisel
and Ward [19] proposed the alternative hypothesis that
androgens from males reach females through the blood
supply, which supposedly flows from the cervix in a ros-
tral direction [ 12]. This hypothesis was derived from the
observation that female rats that have males located cau-
dally (i.e. females that are located "upstream" from males
with regard to bloodflow) in the uterus are somatically and
behaviorally more masculinized than females without such
males. Several, though not all (e.g [3,4]), studies have
provided subsequent support for this hypothesis in rats
[17,20], hamsters [24] and ferrets [18].
In studies addressing this ~'intrauterine position
phenomenon", effects of male fetuses on females have
been described extensively in a variety of species. Only
recently it was reported that males, like females, may also
be affected by hormones secreted by littermates in the
same uterine horn. Specifically, male mice located between
two females had higher levels of estradiol prenatally and
showed, surprisingly, more mounting behavior and less
aggression in adulthood than other males [27]. Male ger-
bils that developed in utero between two males were found