scientific correspondence
Mothers determine sexual preferences
he extent to which behaviour is determined by ‘nurture’ as opposed to
T
‘nature’ in mammals is controversial,
Male goats
a
100
+ +
+
* *
Female goats
b
++
* *
75
*
*
50
50
**
+
*
Mating choice (%)
25
0
1 2 34
Year
+
25
+
*++
*
*
0
*
1 234
123 4
1 2 34
Year
Male sheep
+
*+ + +
+
**
*
*
100
Female sheep
100
*
75
75
*
*
50
50
*
+ +
25
+*
*
0
25
*++
**
0
1 2 34
1 2 34
1 2 34
Year
Ewe
Nanny
Ram
During formal choice tests using adult
animals, cross-fostered males strongly preferred
to
socialize
(mean5s.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
1 2 3 4
Year
Figure 1 Maternal influence
on mating choices. a, Percentage mating choices
(mean5s.e.m.) made by
cross-fostered male sheep
and goats between tethered
ewes and nanny goats during 5-minute tests (30–60
tests per year). b, Percentage 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 animals;
crosses
indicate
P*0.01 different choices versus cross-fostered females
(two-tailed Student’s t-test).
8
100
*
75
Billy
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.
Time < 1.5m from face
Initial choice
Normal
Cross fostered
Male goats
Female goats
+
100
75
*
100
75
+
*
50
50
*
50
+ +
Nanny
Ewe
Nanny
Male sheep
0
0
Ewe
+
*
100
25
25
* *
0
50
*
Nanny
0
Ewe Nanny
Ewe
Female sheep
+
75
75
100
*
*
50
50
*
50
+
*
0
Nanny
25
+
*
Ewe Nanny
*
0
Ewe
50
Time <1.5m from face (s)
*
Initial choice
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.
Studies of birds1–3 have shown that nurture can alter the development of social and
sexual preferences through parental influences, as individuals of one species crossfostered onto another develop a preference
for individuals of their cross-fostered
maternal rather than genetic species. This
has been called ‘sexual imprinting’1. However, 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-fostered at birth onto mothers of another
macaque species showed that one monkey
preferred pictures of members of its maternal rather than its genetic species, but the
study made no direct assessments of social
and sexual preferences4.
We reciprocally cross-fostered offspring
between sheep (eight male and five female
offspring) and goats (four male and four
female offspring) at birth5. 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 resembled that of their maternal rather than their
genetic species, but species-specific patterns
of aggression, climbing, feeding and vocalization were unaffected.
Raised alone or with twin
of maternal species
Raised with twin
of genetic species
25
0
0
Nanny Ewe
Nanny
Ewe
Figure 2 Mean5s.e.m. percentage initial choice of nanny goat or ewe faces made by normal and crossfostered male and female sheep and goats (n45 normal and n44 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/duration of time of nanny versus ewe face in females (two-tailed Student’s t-test).
NATURE | VOL 395| 17 SEPTEMBER 1998
229
Nature © Macmillan Publishers Ltd 1998
scientific correspondence
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, crossfostering opposite-sex twins of the same
genetic species (kids, n=10; lambs, n=8) did
not prevent the maternal influence on preferences from occurring (Fig. 1a, b).
Sheep, like primates, can recognize individuals using facial cues6,7. In choice tests
using pictures of sheep and goat faces, we
found that these alone could elicit preference 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 prevent cross-species matings. However, it has
been argued for avian species that sexual
imprinting may also ensure an optimal outbreeding strategy, as cross-fostered individuals prefer mates that differ only slightly in
appearance from their mothers8. The fact
that male offspring are affected more than
females, and apparently for life, is evidence
that they are indeed more potently influenced by their mothers. This indirectly supports Freud’s concept of the Oedipus
complex and suggests that males may also
be less able than females to adapt to altered
social priorities.
8
Keith M. Kendrick, Michael R. Hinton,
Khia Atkins
Laboratory of Cognitive and Developmental
Neuroscience, The Babraham Institute,
Babraham, Cambridge CB2 4AT, UK
e-mail: [email protected].
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 same1, 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 molecules in Xenopus limb development and
Figure 1 In situ hybridization in Xenopus limb buds at stage 50/51 (a, c–h) or stage 53 (b) for the eight
genes studied.
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 structures along one of the anatomical axes of
the limb bud: proximodistal, anteroposterior and dorsoventral3. 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 patterning3
involves activation of the transcription factor 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 ectoderm. 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), probably 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 throughout 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 AER3. In Xenopus
there is an apical band of expression of
FGF-8, which presumably functions as the
AER. There is also expression of the transcription 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 mesenchyme6. Xenopus has a similar localized
expression of Shh, and a similar expression
of Bmp-2, in both the zone of polarizing
NATURE | VOL 395 | 17 SEPTEMBER 1998
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Nature © Macmillan Publishers Ltd 1998