HERPETOLOGICA

VOL. 68 SEPTEMBER 2012 NO. 3

Herpetologica, 68(3), 2012, 289–298

Ó 2012 by The Herpetologists’ League, Inc.

MANIPULATIVE MOTHERS AND SELECTIVE FORCES:

THE EFFECTS OF REPRODUCTION
ON THERMOREGULATION IN REPTILES
RICHARD SHINE1
School of Biological Sciences A08, University of Sydney, NSW 2006, Australia

ABSTRACT: In many taxa of squamate reptiles, thermal conditions during incubation affect fitness-relevant
phenotypic traits of the offspring. Therefore, a gravid female can enhance the fitness of her offspring by
selecting appropriate thermal regimes. The maternal manipulation hypothesis (MMH) attributes
phylogenetic shifts in a broad array of maternal traits (such as nest-site selection, prolonged uterine
retention of eggs, and shivering thermogenesis) to selective advantages driven by embryonic developmental
plasticity: mothers enhance the viability of their offspring by providing ‘‘better’’ incubation conditions. In
Herpetologica 68:147-159, Schwarzkopf and Andrews (2012) pointed out an alternative possibility: that
reproduction-induced shifts in maternal thermoregulatory tactics have evolved because they enhance
maternal, not offspring, fitness. Although possible on logical grounds, this alternative hypothesis is
inconsistent with available evidence on squamate biology, especially with the diversity of thermoregulatory
modifications induced by reproduction. Most reproduction-associated shifts in maternal thermoregulation
likely reflect benefits to offspring (as posited by the MMH), or are nonadaptive consequences of ecological
shifts that are enforced by reproduction.
Key words: Adaptation; Developmental plasticity; Life history; Maternal effects; Reproduction

A FEMALE ’ S fitness depends upon her have invited me to respond to Schwarzkopf

lifetime reproductive output, not just the
fitness arising from progeny in her current
clutch (e.g., Marshall and Uller, 2007). As a
result, females sometimes increase their
lifetime reproductive success by adopting
tactics that reduce the fitness of their current
progeny. Cannibalism of offspring is the most
extreme example of such behavior (Lourdais
et al., 2005). Schwarzkopf and Andrews (2012)
recently applied this argument to hypotheses
about the selective processes that have driven
evolutionary shifts in the behavioral traits of
reptiles. Their primary focus was the ‘‘mater-
nal manipulation hypothesis’’ (MMH). I
proposed this idea (Shine, 1995), and (with
several coauthors) have since published ex-
tensively on the topic. Therefore, the editors
1
CORRESPONDENCE: e-mail, rick.shine@sydney.edu.au
and Andrews’ (2012) arguments. I agree with
some of Schwarzkopf and Andrews’ (2012)
points, but disagree with others, as I explain in
this paper.
Schwarzkopf and Andrews (2012) focused
on one aspect of the MMH: the effects of
reproduction on the thermoregulatory tactics
of female reptiles. In many squamate species,
females that are carrying eggs or offspring
exhibit body temperatures that differ from
those of nonreproductive females or other
members of the population (e.g., see review
by Shine, 2006, and by Schwarzkopf and
Andrews, 2012). Why does this happen? The
core idea of the MMH is that abiotic
conditions during incubation can affect off-
spring viability; therefore, selection should
favor maternal traits that enable offspring to
develop under more favorable conditions than

289
290 HERPETOLOGICA
would otherwise be the case (Shine, 1995;
Wapstra et al., 2010). A change in maternal
thermoregulatory tactics is only one of several
ways that reproducing females might influ-
ence the incubation conditions of their
offspring (Shine, 2004a). As Schwarzkopf
and Andrews (2012) noted, mothers also can
affect incubation regimes of their offspring via
traits such as nest-site selection, prolonging
uterine retention of developing eggs (leading
to viviparity), and shivering thermogenesis
during brooding (Shine et al., 1997a,b). Thus,
the MMH is broader than the specific focus of
Schwarzkopf and Andrews’ (2012) arguments,
because it seeks to explain the evolution of a
wide range of maternal traits and life-history
variables (e.g., the evolution of environmental
sex determination, as well as viviparity:
Wapstra et al., 2004; Warner and Shine,
2005, 2008). The MMH includes the effects
of variances as well as means of abiotic
conditions (Shine, 2004b; Shine et al., 2005),
and the effects of hydric as well as thermal
factors (Brown and Shine, 2004a, 2005, 2006).
For the present paper, however, I will focus
on the same subset of the MMH’s domain as
examined by Schwarzkopf and Andrews
(2012). Schwarzkopf and Andrews (2012)
operationally defined MMH as the idea that
‘‘females alter the mean and/or variance of
their own body temperature (Tb) while gravid
to manipulate the phenotypes of their off-
spring, so that the latter are more fit than they
would have been if females had not altered
their ‘normal’ or nongravid thermal behavior.’’
Schwarzkopf and Andrews suggested an
alternative hypothesis: that shifts in maternal
thermoregulatory tactics during reproduction
have evolved to benefit the female herself (the
‘‘selfish mother’’ hypothesis, henceforth SMH)
rather than to benefit her progeny in the
current clutch (as per the MMH). This is a
logical alternative hypothesis because (as noted
above) selection works on lifetime reproduc-
tive success. The important distinction be-
tween immediate and long-term reproductive
success has often been overlooked when
framing evolutionary arguments (and indeed,
was overlooked by Charles Darwin himself on
at least one occasion; Shine, 1988). Just
because the SMH is logical does not, however,
mean that it is correct. Whether or not benefits
[Vol. 68, No. 3
to female lifetime reproductive success out-
weigh immediate benefits to the viability of
progeny is a question that can be resolved
empirically, and the answer to that question
will differ among study systems. For the SMH
to offer a better explanation than the MMH,
maternal thermoregulatory modifications need
to enhance maternal lifetime reproductive
success more than they enhance offspring
viability. I doubt that this is the case. The
evidence on reproduction-associated shifts in
thermoregulatory tactics by female squamate
reptiles (reviewed below) suggests that bene-
fits to current progeny (as per the MMH) have
been more important than have benefits to
maternal survival or growth (as per the SMH).
ALTERNATIVE PATHWAYS FOR THE EVOLUTION OF
MATERNAL THERMOREGULATORY MODIFICATIONS
The MMH and the SMH offer competing
(although some mutually compatible) expla-
nations for the same phenomenon. There is
also a third possibility, largely ignored to date:
that these shifts in maternal thermoregulation
are nonadaptive consequences of reproduc-
tion. These three explanations make different
predictions about the consequences of chang-
es to maternal thermoregulation. That is, do
these changes (1) enhance offspring viability
(MMH), (2) enhance maternal fitness (SMH),
or (3) have no effect on the fitness of either
mothers or offspring (nonadaptive)? All three
of these explanations are logically possible, but
they differ in plausibility and importance.
Maternal Manipulation Hypothesis
Many studies have shown that traits likely to
predict offspring fitness are enhanced by
incubation at the temperatures provided by
reproducing females. Schwarzkopf and An-
drews reviewed this evidence for female
thermoregulation (also see Beuchat, 1986,
1988; Arnold and Peterson, 2002), and other
studies have supported this prediction for
aspects of the MMH such as criteria for
maternal nest-site selection (Elphick and
Shine, 1998, 1999; Downes and Shine, 1999;
Shine and Downes, 1999; Brown and Shine,
2004a; Du and Shine, 2010; Löwenborg et al.,
2010, 2011) and the evolution of viviparity
(Shine, 1995; Qualls and Shine, 1996; Shine,
2002; Shine and Thompson, 2006). The
September 2012] HERPETOLOGICA
quality of evidence varies considerably, and
actual measures of offspring fitness are rare.
Nonetheless, there is strong support for the
idea that offspring can benefit substantially
from the thermal regimes provided by their
mothers, both in oviparous and viviparous
species, and in the tropics as well as the
temperate zone (Shine, 1995; Shine and
Harlow, 1996; Webb et al., 2006). The
widespread sensitivity of embryogenesis to
incubation temperatures means that in many
(but undoubtedly not all) squamate popula-
tions, embryos can benefit if mothers slightly
change either the mean or the variance of
their usual body temperatures.
Selfish Mother Hypothesis
The SMH suggests that maternal thermo-
regulatory modifications can benefit maternal
lifetime reproductive success in ways other
than by enhancing viability of the current
progeny. How could this benefit occur? If
there were any straightforward and consistent
viability benefits to a female from maintaining
a higher, lower, or more or less constant body
temperature, then we would expect these
thermal tactics to enhance maternal fitness
throughout the female’s life, not simply when
she is carrying eggs or offspring. Therefore,
the shift associated with reproduction cannot
be explained by any general (non-reproduc-
tion-associated) advantage of this type.
As Schwarzkopf and Andrews (2012) noted,
the most plausible advantage to reproduction-
related shifts in thermoregulatory tactics is to
reduce costs that result from reproductive
activities. The physical burden of the clutch
reduces maternal mobility and thus may
increase vulnerability to predation (Shine,
1980; Schwarzkopf and Shine, 1992; Shine et
al., 1996). Presumably as an adaptation to
ameliorate those risks, reproducing females
often cease feeding (see review by Brischoux
et al., 2011) and become sedentary (Shine,
1980; Graves and Duvall, 1993). Modifications
to maternal thermoregulatory tactics that are
adaptive to such shifts in maternal foraging or
spatial ecology could plausibly support the
SMH. I can envision at least four such shifts:
(1) If gravid female reptiles are more vulner-
able to predators because of the physical
burden of the clutch (Shine, 1980;
291
Schwarzkopf and Shine, 1992), then
higher or more constant body tempera-
tures might facilitate their ability to detect
and flee from predation. I am unaware of
any evidence that bears directly upon this
idea, but shifts in antipredator tactics due
to pregnancy (or other factors that reduce
locomotor performance, such as low body
temperatures or a large meal) are wide-
spread (e.g., Shine et al., 2000; Llewelyn
et al., 2010). For example, reproductive
female Keelback Snakes (Tropidonophis
mairii) flee from humans at a greater
distance than do nonreproductive females
(Brown and Shine, 2004b).
(2) Higher maternal temperatures accelerate
embryogenesis, enabling earlier birth,
which might both enhance offspring
viability as envisioned by the MMH
(e.g., Olsson and Shine, 1997, 1998; Shine
and Olsson, 2003; Warner and Shine,
2007) and reduce the duration of female
burdening (as per the SMH).
(3) Anorexia induces many reptiles to select
lower body temperatures, perhaps be-
cause doing so reduces their energy
expenditure (Cogger, 1974; Gregory et
al., 1999). If gravid females do not feed,
then their shift to lower temperatures
might be adaptive in dealing with anorex-
ia.
(4) More generally, a gravid female that
reduced her body temperature (perhaps
because of reduced need to move around)
would thereby reduce her energy expen-
diture (Gregory et al., 1999).
There is a fundamental difficulty with these
ideas: they all make unidirectional predictions.
Hypotheses 1 and 2 predict that reproducing
females should elevate their temperatures,
whereas hypotheses 3 and 4 suggest that they
should reduce them. Therefore, unlike the
MMH, no single mechanistic pathway could
explain the observed pattern (i.e., that females
of some species adopt lower temperatures
when reproductive, whereas females of other
species adopt higher temperatures: Shine,
2006). At best, then, each of these putative
advantages can explain only a subset of cases.
A proponent of these ideas would need to
explain why a specific advantage (e.g., to early
birth, or to reduced maternal energy expen-
292 HERPETOLOGICA
diture) is more important for some species
than others. These ideas also raise an addi-
tional problem for the SMH: any given change
to maternal thermoregulation is as likely to
reduce as it is to enhance a female’s
subsequent reproductive success.
Non-adaptive Shifts
Changes in maternal thermoregulation may
be simple consequences of reproduction, and
may not confer any particular advantages or
disadvantages either to the progeny or to the
female. For example, a female that moves
about less (because she is not feeding or
remains close to cover to avoid predators:
Bauwens and Thoen, 1981; Graves and
Duvall, 1993) may thereby exhibit a higher
and more stable body temperature (because
she has no other competing activities, and so
can thermoregulate more carefully) or a lower
and more variable temperature (because she
is reluctant to move to patches of sunlight for
basking: Braña, 1993). However, the persis-
tence of such shifts even in ‘‘low-cost’’ captive
environments suggests that maternal thermo-
regulatory shifts are active ‘‘tactics’’ rather
than passive by-products of local conditions. A
similar ‘‘by-product’’ hypothesis would be that
the greater body mass of a gravid animal
increases her thermal inertia, thus tending to
stabilize her body temperature (Grigg et al.,
1979). Empirical and modeling studies would
be needed to estimate the magnitude of any
such thermal-inertia effects.
HOW CAN WE TEST BETWEEN THE MMH
AND SMH?
As Schwarzkopf and Andrews (2012) noted,
it is logistically difficult to test the main
prediction of the SMH, that females enhance
their lifetime reproductive success at the
expense of the fitness of their current off-
spring. Such a test would require long-term
data coupled with experimental manipulations
of maternal thermoregulatory tactics, thus
posing formidable logistical obstacles. In
contrast, the main prediction from the MMH
is easily tested with data from a single
reproductive episode: that is, incubation at
the conditions provided by maternal manipu-
lation (of nest conditions, maternal body
temperatures, etc.) will enhance the viability
[Vol. 68, No. 3
of offspring compared to that of siblings
incubated under the putative ancestral condi-
tions (e.g., without reproduction-induced
modifications of maternal thermoregulatory
tactics). That ease of testing has encouraged
empirical studies, which have largely produced
data compatible with the MMH (see Table 1 of
Schwarzkopf and Andrews, 2012). In particu-
lar, these studies (and others) strongly support
the fundamental assumption underlying the
MMH: that phenotypic traits plausibly linked
to offspring fitness (size, speed, growth rates,
etc.) are influenced by the abiotic conditions
experienced during incubation. Studies con-
tinue to add to the list of phenotypic traits
influenced by incubation temperature: for
example, we have recently shown that hotter-
incubated hatchling lizards are more adept at
learning tasks (Amiel and Shine, 2012).
The widespread dependence of fitness-
relevant hatchling traits on incubation tem-
peratures is clearly established. Therefore, the
challenge for opponents of the MMH is to
suggest why we should not expect selection to
favor maternal tactics that expose the devel-
oping embryos to the most favorable incuba-
tion regimes. The only cases in which this
selective advantage would not apply are those
in which the usual body temperatures of
nonreproductive individuals are already at
the embryonic thermal optimum. The MMH
also might be irrelevant if the ability of
females to modify their thermal tactics is
precluded by constraints (e.g., no spatial
heterogeneity in operative temperatures) or
by costs (i.e., the reduction in longer-term
maternal fitness outweighs the benefits to
current offspring fitness). For the SMH to
offer a plausible explanation for the evolution
of maternal thermoregulatory modifications,
some (as yet unidentified) advantage of those
modifications to maternal lifetime reproduc-
tive success needs to be greater than the
(readily demonstrable) advantages of those
modifications for offspring viability. Phyloge-
netic changes in maternal thermoregulatory
behavior might be driven by the SMH if
species vary more in those (unspecified)
advantages to reproducing females than in
the advantages to developing embryos. In
summary, the SMH relies upon unclear and
unidentified advantages, whereas the MMH
September 2012] HERPETOLOGICA
relies upon straightforward and well-docu-
mented phenomena.
Given the logistical hurdles to testing the
SMH directly, can we identify scenarios in
which predictions from the SMH differ from
those from the MMH? I suggest the following:
(1) Direction and magnitude of thermal
shifts.—The MMH predicts high inter-
specific variation in the form and direc-
tion of maternal thermoregulatory
modifications during reproduction. That
is, we expect females to select warmer
temperatures in some species, cooler
temperatures in others, less variable
temperatures in yet others, and so forth.
This prediction derives from the idea that
it is the disparity between two traits
(maternal body temperatures and embry-
onic thermal optima), which are them-
selves variable, that drives the fitness
benefit to reproduction-induced shifts in
maternal thermoregulation. Body temper-
atures of free-ranging reptiles vary intra-
specifically as well as interspecifically; for
example, they change with season and
with annual weather conditions, and
diverge among populations of wide-rang-
ing species that inhabit different thermal
environments (Huey, 1974; Huey and
Slatkin, 1976). Embryonic thermal optima
are more conservative phylogenetically
(e.g., Du et al., 2011), and sympatric
species of different lineages often differ
substantially in thermal optima for incu-
bation (e.g., Shine, 1999). Therefore, we
expect the disparity between maternal
temperatures and embryonic optima to
vary considerably through space and time,
and both among and within species.
The SMH does not necessarily predict such
variation. If the effects of thermoregulatory
tactics on maternal fitness derive from funda-
mental physiological advantages to the moth-
er, then we might expect the same
combination of means and variances of body
temperatures to optimize a mother’s viability
across a wide range of species. Without
knowing the mechanisms involved, however,
it is difficult to derive specific predictions
from the SMH. The available data show that
(consistent with the MMH), the direction,
293
degree, and nature of thermoregulatory shifts
induced by reproduction vary considerably
among squamate species (see Shine, 2006).
(2) Abiotic influences on offspring and ma-
ternal phenotypes.—The MMH suggests
that offspring phenotypes depend upon
incubation conditions, and hence should
be modified by thermal variation that is
induced by abiotic as well as biotic
(maternal) factors. For example, offspring
that develop in cooler nests, cooler years,
or cooler seasons should exhibit different
phenotypes than conspecifics that develop
in warmer years or warmer seasons.
Extensive studies support this prediction,
not only for eggs in natural nests (espe-
cially for species with temperature-de-
pendent sex determination) but also for
viviparous species (Lourdais et al., 2004;
Wapstra et al., 2009). Although gravid
female vipers and Snow Skinks ameliorate
local weather conditions by changing their
basking behaviors, the offspring born to
these viviparous reptiles after cool years
differ phenotypically from those pro-
duced after warm years (Lourdais et al.,
2004; Wapstra et al., 2009). Under the
SMH, we might expect spatiotemporal
variation in environmental temperatures
to modify maternal, rather than offspring,
traits. Empirical tests of this prediction
would be both straightforward and inter-
esting.
(3) Semelparity vs. iteroparity.—Unlike the
MMH, the SMH should not apply to taxa
in which females produce only a single
clutch or litter during their lifetimes. The
SMH depends upon fitness advantages
that are manifested in subsequent clutch-
es; and if the female never reproduces
again, then she can never reap such
benefits. Therefore, the SMH predicts
that a semelparous female should not shift
her thermoregulatory tactics when she
reproduces, whereas the MMH predicts
that she should. Consistent with the
MMH (but not the SMH), semelparous
female Asps (Vipera aspis) exhibit pro-
found thermoregulatory modifications
when gravid (Bonnet et al., 2002a,b).
Advocates of the SMH could attribute
294 HERPETOLOGICA
those shifts to enhanced maternal survival
through the end of the (sole) pregnancy,
but the fitness payoff to the female clearly
must be via that single current litter, not
through residual benefits to later repro-
ductive events.
(4) Thermal heterogeneity within a female’s
body.—The SMH posits that the advan-
tage of modified body temperature is to
the female herself, whereas the MMH
posits that the advantage accrues to the
offspring. The elongate form of large
snakes can enable substantial thermal
heterogeneity within the body. Therefore,
most versions of the SMH would predict
that the female would warm (or cool, or
keep stable, or allow variation in) the
temperatures of critical parts of her own
body (e.g., brain, locomotor organs, and
stomach), whereas the MMH predicts that
the developing offspring would be the
primary target of modified thermoregula-
tory tactics. Empirical studies to distin-
guish between these two scenarios would
be straightforward; all that would be
needed are temperature measurements
(using implanted thermocouples, or even
infrared thermometers) at a range of
positions along the body of a gravid
female. My own observations of gravid
female reptiles suggest that they adjust
their positions in ways that modify embryo
temperatures rather than general mater-
nal body temperatures; for example, they
position themselves such that the part of
the body containing embryos is exposed to
sunlight. Most notably, gravid pythons
often invert the rear (egg-containing) but
not anterior parts of their bodies when
basking under heat-lamps (see photo-
graph in Ross and Marzec, 1990, p. 70;
Lourdais et al., 2008). That selectivity
supports the idea that the critical benefit
of additional basking is to warm the eggs,
not the rest of the female’s body (consis-
tent with the MMH rather than SMH).
Finally, I consider two potential tests
suggested by Schwarzkopf and Andrews
(2012):
(5) Proximate causes for thermal changes.—
Schwarzkopf and Andrews (2012) sug-
[Vol. 68, No. 3
gested that ‘‘one way to test whether . . .
variations in Tb while gravid are caused
chiefly by encumbrance or by other
factors would be to determine if nongrav-
id females respond to any physical burden
in the same way that gravid females
respond to pregnancy (i.e., by shifting
mean Tb . . .). . . .Experimental support of
this prediction would challenge one
aspect of the MMH.’’ Such a study
(interesting though it would be) would
simply clarify the proximate basis for
shifts in maternal thermoregulation. Fe-
males may well ‘‘know’’ they are gravid
because of the additional mass and
volume of the developing offspring or
eggs; if so, experimentally mimicking that
burden should induce the thermoregula-
tory changes induced by a real pregnancy.
Thus, this experiment would identify the
proximate mechanisms underpinning
thermoregulatory shifts, but say nothing
about the validity of the MMH. It would
also be instructive to examine thermoreg-
ulatory shifts in male reptiles during
spermatogenesis, because males do not
experience the physical encumbrance of a
large clutch, but should nonetheless be
under similar pressures as females (under
the MMH) if processes such as spermato-
genesis and spermiogenesis proceed more
rapidly or effectively at specific tempera-
tures. Again, empirical studies could test
these ideas.
More generally, Schwarzkopf and Andrews’
(2012) ideas suggested the potential for
experimental work to identify the proximate
underpinnings of thermoregulatory responses
to female reproductive condition. Some of
those responses may be under direct physio-
logical (e.g., hormonal) control, whereas
others may be facultative responses to repro-
duction-induced changes in traits such as a
female’s degree of burdening (and hence,
inducible by a large meal as well as by
pregnancy). Commonly, both processes may
interact; for example, prolonged uterine re-
tention of developing eggs in cold climates
results from a mix of adaptation and proximate
response (Telemeco et al., 2010).
(6) Interspecific correlations in thermal
September 2012] HERPETOLOGICA
traits.—Schwarzkopf and Andrews (2012)
suggested that an interspecific correlation
between embryonic thermal optima and
adult body temperatures would challenge
the underpinnings of the MMH. I dis-
agree. Such a correlation almost certainly
exists, because we expect embryonic
norms of reaction to evolve such that
their thermal optimum approaches the
mean body temperature of reproducing
females, at the same time as body
temperatures of reproducing females
evolve to match the embryonic thermal
optima (Arnold and Peterson, 2002).
These ideas provide fertile material for a
review. That correlation is irrelevant to
the validity of the MMH, however, which
simply requires that an evolutionary shift
from ancestral to derived states of mater-
nal thermoregulatory tactics enhances
offspring viability. Correlations between
embryonic thermal optima and adult body
temperatures are irrelevant; all that mat-
ters is the disparity between the two.
Even if maternal body temperatures and
embryo optima were highly correlated
interspecifically, the two numbers could
differ within each of those species.
Imagine, for example, three species with
mean maternal body temperatures of 20,
25, and 308C, and respective embryonic
optima of 25, 30, and 358C. Although the
two sets of numbers are highly correlated,
embryonic viability could be substantially
enhanced (within all three of those
species) if gravid females basked to
further increase their body temperatures.
Therefore, interspecific correlations be-
tween maternal temperatures and embry-
onic optima are irrelevant to the validity
of the MMH.
CONCLUSIONS
Under the axiom that natural selection acts
to maximize an individual’s lifetime reproduc-
tive success, we expect organisms to adopt
tactics that enhance their own future repro-
ductive output, even at the cost of reducing
the fitness returns from a current clutch or
litter. Therefore, whether or not a given
maternal effect is adaptive depends upon
295
potential impacts both on the current litter
and on the parent’s future reproductive
output (Marshall and Uller, 2007). This does
not, however, mean that fitness returns over
both of these timescales have equally impor-
tant effects on the evolution of specific life-
history tactics.
Many of the behaviors by which a mother
can enhance the fitness of her current litter
may have negligible effects on her future
fitness. Maternal thermoregulatory modifica-
tions in squamate reptiles are a case in point.
By changing the temperatures she selects
while carrying offspring, a female can mas-
sively influence the viability of those offspring,
with minimal (if any) consequences to her
own future rates of survival and growth.
Additionally, any effects of thermal modifica-
tions on a female’s subsequent fitness are
likely to be compromised by conflicts; for
example, higher temperatures during preg-
nancy shorten the duration of her burdening,
but also increase her rate of metabolic
expenditure. These conflicts will reduce any
overall net effect of maternal thermoregula-
tory modifications on maternal fitness. As a
result, the evolution of maternal thermoregu-
latory tactics likely has been driven by
immediate fitness benefits (to current proge-
ny), rather than by any longer-term conse-
quences (to maternal fitness).
The available data back up these conclu-
sions. Schwarzkopf and Andrews (2012) sug-
gested that ‘‘The MMH is supported by
evidence that current offspring fitness was
enhanced by maternal thermoregulatory be-
havior during reproduction, while female
fitness was either unaffected or reduced.’’
This is exactly what the evidence shows, as
summarized in Schwarzkopf and Andrews’
(2012) table 1. There are many cases in which
offspring viability is enhanced by the maternal
behavior in question (supporting the MMH),
but no cases that reveal maternal benefits
from that behavior (the critical prediction of
the SMH). Cases in which maternal variables
(body condition, etc.) are unaffected by
reproduction do not constitute evidence that
thermoregulatory modifications benefit ma-
ternal viability (contra Schwarzkopf and An-
drews, 2012), but instead are consistent with
296 HERPETOLOGICA
the MMH (note the quote from Schwarzkopf
and Andrews, 2012, above).
Although I doubt the importance of the
SMH, Schwarzkopf and Andrews (2012) have
made a valuable contribution by pointing out a
logically plausible alternative explanation for
the influence of reproduction on thermoreg-
ulation. Future work should look for tractable
model systems in which to measure the long-
term effects of thermal manipulations on the
subsequent reproductive output of the female
(the critical test of the SMH). Importantly,
Schwarzkopf and Andrews’ (2012) ideas have
suggested a range of novel experiments: for
example, to look at effects of physical
burdening on thermoregulation, to look at
the influence of spermatogenesis on male
thermoregulation, and to measure spatial
heterogeneity in selected temperatures along
the body of gravid snakes. One of the primary
benefits of comparing simplistic models such
as the MMH and the SMH is to suggest such
studies. Also, Schwarzkopf and Andrews’
(2012) discussion drew attention to a third
hypothesis—neither MMH nor SMH—that
may well explain some of the distinctive
thermal tactics of reproducing reptiles. This
is the idea that some of those thermal
modifications are simple consequences of
shifts in other traits (notably a cessation of
feeding and a reduction in movements) that
accompany reproduction in many squamates.
Despite my unbridled enthusiasm for the
MMH, it would not surprise me if some of
the thermal modifications seen in gravid
squamates do not affect the fitness either of
embryos or of their mothers. Hence, although
I dispute most of Schwarzkopf and Andrews’
(2012) conclusions, I applaud their innovative
contribution to this fascinating topic.
Acknowledgments.—I thank Lin Schwarzkopf and
Robin Andrews for their provocative paper, the editors
for inviting this response, and the many colleagues and
students who have helped me to develop my ideas about
this topic. I thank my main funding body, the Australian
Research Council, for their courage in supporting my
long-term research on a topic as abstruse and ‘‘non-
applied’’ as the thermoregulatory tactics of reproducing
reptiles.
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Accepted: 16 May 2012
Associate Editor: Stephen Mullin