Behavior and Neurology of Lizards 
N. Greenberg and P. D. MacLean, eds. 
NIMH, 1978. 
Integration of Internal and External Stimuli in the Regulation 
of Lizard Reproduction 
David Crews 
Department of Biology 
Department of Psychology and Social Relations 
and 
Museum of Comparative Zoology 
Harvard University 
SUMMARY. Environment, hormones, and behavior interact to regulate vertebrate reproduc- 
tion. However, the integration of these factors can be fully appreciated only in an ecological con- 
text where the adaptive significance of such interaction becomes apparent. 
Experiments with the lizard, Anolis carolinensis, indicate that internal and external factors 
interact to regulate different phases of the female reproductive cycle. Following female emergence 
from winter dormancy, environmentally induced androgen-dependent male behavior acts along 
with climatic aspects of the environment to modulate ovarian recrudescence; male courtship 
insures normal gonadotropin (GT) secretion in the female; the absence of courtship results in 
subnormal GT secretion, while aggression between males inhibits GT secretion. During the 
breeding season, females undergo cycles of sexual receptivity which depend upon hormonal con- 
ditions normally arising during follicular maturation and are restricted to the time immediately 
preceding ovulation. If the female mates during this period, further receptivity within that fol- 
licular cycle is inhibited. At the end of the breeding season, females are insensitive to both en- 
vironmental and hormonal stimuli that would otherwise facilitate ovarian growth; this re- 
fractoriness is maintained by the atretic follicle. 
These and related findings demonstrate that principles originally elaborated with inbred labora- 
tory species can be generalized to animals in the field and shown to have clear adaptive value in 
the animal’s natural history. 
INTRODUCTION 
. . . the sexual posturing of the male 
produces exteroceptive stimuli which 
act upon the anterior pituitary of the 
female through the hypothalamus, and 
so affects the necessary synchronization 
between the sexual processes of the male 
and female . . . (F.H.A. Marshall, 1936, 
p. 445) 
The integration of behavioral, endocrino- 
logical, and environmental factors in the 
regulation of vertebrate reproduction has 
been the subject of intensive investigation 
in recent years. Perhaps most notable has 
been the research of Robert A. Hinde and 
the late Daniel S, Lehrman. Due largely to 
their work on the canary (Hinde, 1965) and 
the ring dove (Lehrman, 1965), many of 
the fine details of the synchronization about 
which Marshall speculated 40 years ago have 
been confirmed; we can now say with some 
assurance that the environmentally induced 
endocrine-dependent courtship behavior of 
the male, acting along with climatic and 
physical aspects of the environment, stimu- 
lates pituitary gonadotropin secretion and 
consequent ovarian development, steroid pro- 
duction, and reproductive behavior in the 
conspecific female (Bermant and Davidson, 
1974) (see Fig. 1). Changes in the female’s 
behavior, in turn, feed back ultimately to 
influence the physiology and behavior of 
the male (Cheng, 1975). This concept of a 
reciprocal interaction between the animal 
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