Species Differences in the Regulation of Tyrosine
Hydroxylase in Cnemidophorus Whiptail Lizards
Sarah C. Woolley,* David Crews
Section of Integrative Biology, Patterson 141, 2400 Speedway, University of Texas at Austin, Austin,
Texas 78712
Received 30 July 2003; accepted 5 January 2004
ABSTRACT: Evolution of behavioral phenotype
involves changes in the underlying neural substrates.
Cnemidophorus whiptail lizards enable the study of be-
havioral and neural evolution because ancestral species
involved in producing unisexual, hybrid species still ex-
ist. Catecholaminergic systems modulate the expression
of social behaviors in a number of vertebrates, including
whiptails, and therefore we investigated how changes in
catecholamine production correlated with evolutionary
changes in behavioral phenotype by measuring the size
and number of catecholamine producing (tyrosine hy-
droxylase-immunoreactive, or TH-ir) cells across the
reproductive cycle in females from two related whiptail
species. Cnemidophorus uniparens is a triploid, parthe-
nogenetic species that arose from hybridization events
involving the diploid, sexual species C. inornatus. Prior
to ovulation, females from both species display female-
like receptive behaviors. However, after ovulation, only
parthenogenetic individuals display malelike mounting
behavior. In all nuclei measured, we found larger TH-ir
cells in the parthenogen, a difference consistent with
species differences in ploidy. In contrast, species differ-
ences in the number of TH-ir cells were nucleus specific.
In the preoptic area and anterior hypothalamus, parthe-
nogens had fewer TH-ir cells than females of the sexual
species. Reproductive state only affected TH-ir cell num-
ber in the substantia nigra pars compacta (SNpc), and C.
uniparens individuals had more TH-ir cells after ovula-
tion than when previtellogenic. Thus, species differences
over the reproductive cycle in the SNpc are correlated
with species differences in behavior, and it appears that
the process of speciation may have produced a novel
neural and behavioral phenotype in the parthenogen.
© 2004 Wiley Periodicals, Inc. J Neurobiol 60: 360 –368, 2004
Keywords: dopamine; lizard; ploidy; reproduction; ty-
rosine hydroxylase; parthenogenetic
INTRODUCTION
Neural and behavioral evolution are often difficult to
study because ancestral species no longer exist. Cne-
midophorus lizards enable the study of evolutionary
processes because new species arise through multiple
hybridizations. Cnemidophorus uniparens, for exam-
ple, is a triploid parthenogen that arose through two
hybridization events, both involving the diploid, sex-
ual species C. inornatus (Wright, 1993). Though fe-
males of both species show identical patterns of ste-
roid hormone secretion across the reproductive cycle,
there are considerable behavioral differences between
the two. Females of both species display female-like
receptive behaviors during vitellogenesis when estro-
gen levels are rising. However, following ovulation
when there is a surge of progesterone, females of the
ancestral, sexual species become sexually unreceptive
while the parthenogens display male-like copulatory
behaviors (Moore and Crews, 1986; Moore et al.,
1985a,b; reviewed in Crews and Sakata, 2000). By
investigating the neural correlates of this behavioral
* Present address: WM Keck Center for Integrative Neuro-
science, 513 Parnassus, Box 0444, University of California, San
Francisco, San Francisco, CA 94143-0444.
Correspondence to: S. C. Woolley (scwoolley@phy.ucsf.edu).
Contract grant sponsor: NIMH; contract grant numbers: T32
18837 (S.C.W.) and 41770 (D.C.).
© 2004 Wiley Periodicals, Inc.
Published online 15 June 2004 in Wiley InterScience (www.
interscience.wiley.com).
DOI 10.1002/neu.20044
360