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Mothers determine sexual preference

Authors:

Abstract

The extent to which behaviour is determined by `nurture' as opposed to `nature' in mammals is controversial, although most recent interest has focused on genetic determinants. Here we investigate maternal influences on behavioural development by using the approach of cross-fostering between sheep and goats, which, like ourselves, form close individual attachment bonds with their offspring. We show that the emotional bond between a mother and her male offspring, rather than other social or genetic factors, may irreversibly determine these species' social and sexual preferences. Maternal influences on female offspring are weaker and totally reversible. In both sexes, visual cues from the face are important for determining attraction.
Nature © Macmillan Publishers Ltd 1998
8
T
he extent to which behaviour is deter-
mined by ‘nurture’ as opposed to
‘nature’ in mammals is controversial,
although most recent interest has focused
on genetic determinants. Here we investi-
gate maternal influences on behavioural
development by using the approach of
cross-fostering between sheep and goats,
which, like ourselves, form close individual
attachment bonds with their offspring. We
show that the emotional bond between a
mother and her male offspring, rather than
other social or genetic factors, may irre-
versibly determine these species’ social and
sexual preferences. Maternal influences on
female offspring are weaker and totally
reversible. In both sexes, visual cues from
the face are important for determining
attraction.
Studies of birds
1–3
have shown that nur-
ture can alter the development of social and
sexual preferences through parental influ-
ences, as individuals of one species cross-
fostered onto another develop a preference
for individuals of their cross-fostered
maternal rather than genetic species. This
has been called ‘sexual imprinting
1
. How-
ever, unlike mammals, these avian species
also classically imprint on the first salient
animate or inanimate visual object they see,
suggesting a high degree of preprogrammed
inflexibility in their development of social
preferences.
An important question, therefore, is
whether maternal influences on social
mammals that form strong attachment
bonds with their offspring are similar even
though such mammals exhibit increased
behavioural flexibility. Maternal influences
have been suggested to affect sociosexual
preferences in humans, particularly males,
but this has been difficult to prove. One
study of three macaque monkeys cross-fos-
tered at birth onto mothers of another
macaque species showed that one monkey
preferred pictures of members of its mater-
nal rather than its genetic species, but the
study made no direct assessments of social
and sexual preferences
4
.
We reciprocally cross-fostered offspring
between sheep (eight male and five female
offspring) and goats (four male and four
female offspring) at birth
5
. We tested the
relative importance of the maternal bond
compared with other social relationships by
allowing fostered offspring social contact
with members of their genetic species at all
times during development. As juveniles,
their play and grooming behaviour resem-
bled that of their maternal rather than their
genetic species, but species-specific patterns
of aggression, climbing, feeding and vocal-
ization were unaffected.
During formal choice tests using adult
animals, cross-fostered males strongly pre-
ferred to socialize (mean
5s.e.m.
89.158.3% of time) and mate (Fig. 1a)
with females of their maternal species. This
preference was not altered even after living
exclusively with their genetic species for 3
years (Fig. 1a).
In contrast, cross-fostering effects on
female social (68.7512.7% time with
maternal species females,
P*0.001 versus
cross-fostered males; U-test) and sexual
(Fig. 1b) preferences were significantly
weaker and reversible within 1 to 2 years.
All normally reared animals preferred social
contact (males, 95.750.96% of time;
females, 9451.1% of time) and chose to
mate exclusively with their genetic species.
NATURE
|
VOL 395
|
17 SEPTEMBER 1998 229
Mothers determine sexual preferences
scientific correspondence
FFiigguurree 11
Maternal influence
on mating choices. a, Per-
centage mating choices
(mean5s.e.m.) made by
cross-fostered male sheep
and goats between tethered
ewes and nanny goats dur-
ing 5-minute tests (30–60
tests per year). b, Percent-
age mating choices made
by cross-fostered oestrus
females between rams and
billy goats. Normally reared
sheep (9 males and 6
females) and goats (8 males
and 10 females) mated
exclusively with members of
their genetic species. In tests
in years 2, 3 and 4, animals
had lived with their genetic
species only after year 1.
Asterisks indicate
P
*0.01
versus normally reared ani-
mals; crosses indicate
P
*0.01 different choices ver-
sus cross-fostered females
(two-tailed Student’s
t
-test).
Initial choice
Time < 1.5m from face
Normal
Cross fostered
Male goats
Female goats
Male sheep Female sheep
Initial choice
100
50
0
100
50
0
100
50
0
100
50
0
Nanny
Ewe
Nanny
Ewe
Nanny Ewe
Nanny
Ewe
Nanny Ewe
Nanny
Ewe
Nanny Ewe
Nanny
Ewe
75
50
0
75
50
0
75
50
0
75
50
0
25
25
25
25
Time <1.5m from face (s)
*
*
*
*
*
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
FFiigguurree 22
Mean5s.e.m. percentage initial choice of nanny goat or ewe faces made by normal and cross-
fostered male and female sheep and goats (
n
45 normal and
n
44 cross-fostered animals for each species
and sex) and durations spent within 1.5 metres of the faces during 120-second tests. Asterisks indicate
P
*0.05 versus normally raised animals; crosses indicate
P
*0.05 compared with proportion of choice/dura-
tion of time of nanny versus ewe face in females (two-tailed Student’s
t
-test).
Raised with twin
of genetic species
Raised alone or with twin
of maternal species
100
75
50
25
0
100
75
50
25
0
100
75
50
25
0
100
75
50
25
0
Mating choice (%)
Year
Year
Year
Year
1
23
4
1
23
4
1
2
3
412
34
Male goats
Female goats
Male sheep Female sheep
1
23
4
1
234
Ewe Nanny
1
2
34
Ram Billy
12
3
4
+
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
*
*
*
*
*
*
*
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
+
*
a
b
Nature © Macmillan Publishers Ltd 1998
8
scientific correspondence
230 NATURE
|
VOL 395
|
17 SEPTEMBER 1998
find that the assumption is not correct.
This finding has obvious implications for
our understanding of limb development
and evolution.
The prevailing view of limb patterning,
based on experiments in chick and mouse,
involves three distinct signalling centres,
each controlling the differentiation of struc-
tures along one of the anatomical axes of
the limb bud: proximodistal, anteropos-
terior and dorsoventral
3
. By using various
reagents we found that the proximodistal
and anteroposterior systems in Xenopus
appear similar to the amniote species,
whereas the dorsoventral system appears to
be different (Fig. 1).
The model for dorsoventral patterning
3
involves activation of the transcription fac-
tor En-1 in the ventral ectoderm at an early
stage. Expression of En-1 represses the
expression of two signalling molecules,
Wnt-7A and Radical fringe (Rfng), which
are therefore made only in the dorsal ecto-
derm. The Wnt-7A signal causes the dorsal
mesenchyme to form dorsal structures. The
Rfng signal participates in the induction of
the apical ectodermal ridge (AER), proba-
bly by potentiating the action of another
signal, Serrate, on its receptor Notch-1 (refs
4, 5). We have examined the expression of
the genes en-1, Wnt-7A, Rfng and Notch-1
in Xenopus limb buds. Of these, only en-1 is
expressed in the expected position, the
ventral epidermis. The other three do not
show the expected regionalization, but are
expressed in a diffuse manner through-
out the limb bud in both ectoderm and
mesenchyme. We have confirmed that they
really are expressed, and that the diffuse
staining is not just nonspecific background,
by RNase protections (Fig. 2).
The proximodistal pattern of amniote
limbs arises from the sequential formation
of structures from a mesenchymal progress
zone, the developmental lability of which is
maintained by fibroblast growth factors
(FGFs) secreted by the AER
3
. In Xenopus
there is an apical band of expression of
FGF-8, which presumably functions as the
AER. There is also expression of the tran-
scription factor Msx-1 in the underlying
progress zone. The anteroposterior pattern
arises in response to the secretion of Sonic
hedgehog (Shh) from the zone of polarizing
activity on the posterior side of the mes-
enchyme
6
. Xenopus has a similar localized
expression of Shh, and a similar expression
of Bmp-2, in both the zone of polarizing
FFiigguurree 11
In situ
hybridization in
Xenopus
limb buds at stage 50/51 (a, ch) or stage 53 (b) for the eight
genes studied.
We also determined whether sibling
bonds might reduce the impact of the
maternal bond, as lambs and kids form
close bonds with a twin. However, cross-
fostering opposite-sex twins of the same
genetic species (kids, n=10; lambs, n=8) did
not prevent the maternal influence on pref-
erences from occurring (Fig. 1a, b).
Sheep, like primates, can recognize indi-
viduals using facial cues
6,7
. In choice tests
using pictures of sheep and goat faces, we
found that these alone could elicit prefer-
ence for females of the maternal species and
that effects were again stronger in males
(Fig. 2). Thus the face appears to be an
important source of attraction.
This strong maternal influence on social
and sexual preferences may function to pre-
vent cross-species matings. However, it has
been argued for avian species that sexual
imprinting may also ensure an optimal out-
breeding strategy, as cross-fostered individ-
uals prefer mates that differ only slightly in
appearance from their mothers
8
. The fact
that male offspring are affected more than
females, and apparently for life, is evidence
that they are indeed more potently influ-
enced by their mothers. This indirectly sup-
ports Freud’s concept of the Oedipus
complex and suggests that males may also
be less able than females to adapt to altered
social priorities.
Keith M. Kendrick, Michael R. Hinton,
Khia Atkins
Laboratory of Cognitive and Developmental
Neuroscience, The Babraham Institute,
Babraham, Cambridge CB2 4AT, UK
e-mail: keith.kendrick@bbsrc.ac.uk.
Martin A. Haupt, John D. Skinner
Mammal Research Institute,
University of Pretoria,
Pretoria 0002, South Africa
1. Lorenz, K. J. Ornithol. 83, 137–213 & 289–413 (1935).
2. Immelmann, K. Z. Tierpsychol. 26, 677–691 (1969).
3. ten Cate, C. in Perspectives in Ethology Vol. 8 (eds Bateson,
P. P. G. & Klopfer, P. H.) 243–269 (Cambridge Univ. Press, New
York, 1989).
4 Fujita, K. Primates 34, 141–150 (1993).
5. Kendrick, K. M., da Costa, A. P., Hinton, M. R. & Keverne, E. B.
Appl. Anim. Behav. Sci. 34, 345–357 (1992).
6. Kendrick, K. M., Atkins, K., Hinton, M. R., Heavens, P. &
Keverne, E. B. Behav. Proc. 38, 19–35 (1996).
7. Kendrick, K. M. & Baldwin, B. A. Science 236, 448–450 (1987).
8. Bateson, P. Nature 273, 659–660 (1978).
All limbs are not
the same
Recent papers published in Nature have
assumed that the mechanism of limb
development in all vertebrates is the same
1, 2
.
But if mechanisms were conserved in all
tetrapods, we should expect to find them
in amphibians as well as in amniotes. We
have examined the expression of eight
important signalling and regulatory mol-
ecules in Xenopus limb development and
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Japanese and rhesus monkeys aged between 9 months old and 5 yrs old pressed a lever to see a variety of pictures of seven macaque species. These monkeys had various restricted social experience: namely, either reared by humans with conspecific or heterospecific peers, or cross-fostered between these two species. Rhesus monkeys tended to prefer seeing rhesus monkeys best among the pictures of the seven species without regard to their age or social experience. Japanese monkeys having restricted experience also liked to see rhesus monkeys better than Japanese monkeys, but not the best among the seven species. In a previous study, mother-reared infants of Japanese monkeys preferred seeing pictures of their own species over those of rhesus monkeys. These results suggest a dissociation of the determinants of this basic social preference: rhesus monkeys prefer to see their own species by nature while Japanese monkeys may learn to prefer their own species.
Article
WHEN Konrad Lorenz showed that early experiences can have a dramatic influence on the mating preferences of birds, he proposed that `sexual imprinting', as the process came to be known in English, enables adults to recognise their own species1. Subsequent experimental work2,3 has, however, suggested that, although early experiences can indeed have long-lasting effects, a bird may also show a preference for members of its own species in the absence of experience with any of them except itself. The implication is that a bird may have a predisposing bias for its own species and sexual imprinting merely refines this bias in natural conditions. If birds are able to identify and mate with their own species without prior experience (and seeing or hearing themselves is irrelevant) what is the biological function of sexual imprinting? One possible answer is that sexual imprinting is required for recognition of close kin so that, by selecting mates that are slightly different, the animal is able to strike an optimal balance between inbreeding and outbreeding4. The prediction is that the strongest mating preference of a bird should be for something a little different (but not too different) from the object with which it had been imprinted. I report here that male Japanese quail (Coturnix coturnix japonica) mate with slightly unfamiliar females in preference to females to which they were exposed in early life, and that both types of female are preferred to those with a grossly unfamiliar type of plumage.
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