The limits of the energetical perspective: life-history decisions in lizard growth

Abstract

The study of energy allocation is essential in understanding the regulation of major life history traits. It is often assumed automatically that the limitation of an energy budget or higher allocation to a single trait affect all life history traits. This assumption was inherently included in influential models of ontogenetic growth. We aim to challenge this perspective by focusing on growth in lizards. Summarizing the results of a series of long-term manipulative experiments in the Madagascar ground gecko (Paroedura picta), we show that although growth is generally assumed to be highly plastic in reptiles and other ectothermic vertebrates, it is at least in this species largely canalized and does not seem to be affected by energy limitations under several experimental conditions. Diet restriction, resulting in lower allocation to fat storage and reproduction, and the allocation to energetically demanding traits such as reproduction in both sexes and tail regeneration had little if any effect on structural growth. We document that sexual size dimorphism does not emerge in the ontogeny of the studied species directly due to differential allocation to structural growth in males and females. Instead, sex-specific growth trajectories are driven by a signaling of ovarian hormones as the key proximate mechanism shaping sex-specific allocation decisions during ontogeny. We suggest that the large degree of canalization of the structural growth can reflect hierarchy in energy allocation with the structural growth being prioritized to investment in other traits. The prioritized allocation to structural growth can reflect selective advantage of reaching a final, optimal size for a given sex as fast as possible.

Full text

Vol.:(0123456789)
Evolutionary Ecology (2020) 34:469–481
https://doi.org/10.1007/s10682-020-10054-0
1 3
IDEAS & PERSPECTIVES
The limits oftheenergetical perspective: life-history
decisions inlizard growth
BrandonMeter1· ZuzanaStarostová1 · LukášKubička2· LukášKratochvíl2
Received: 30 March 2020 / Revised: 12 May 2020 / Accepted: 14 May 2020 / Published online: 25 May 2020
© Springer Nature Switzerland AG 2020
Abstract
The study of energy allocation is essential in understanding the regulation of major life
history traits. It is often assumed automatically that the limitation of an energy budget or
higher allocation to a single trait affect all life history traits. This assumption was inher-
ently included in influential models of ontogenetic growth. We aim to challenge this per-
spective by focusing on growth in lizards. Summarizing the results of a series of long-term
manipulative experiments in the Madagascar ground gecko (Paroedura picta), we show
that although growth is generally assumed to be highly plastic in reptiles and other ecto-
thermic vertebrates, it is at least in this species largely canalized and does not seem to
be affected by energy limitations under several experimental conditions. Diet restriction,
resulting in lower allocation to fat storage and reproduction, and the allocation to energeti-
cally demanding traits such as reproduction in both sexes and tail regeneration had little if
any effect on structural growth. We document that sexual size dimorphism does not emerge
in the ontogeny of the studied species directly due to differential allocation to structural
growth in males and females. Instead, sex-specific growth trajectories are driven by a sign-
aling of ovarian hormones as the key proximate mechanism shaping sex-specific allocation
decisions during ontogeny. We suggest that the large degree of canalization of the struc-
tural growth can reflect hierarchy in energy allocation with the structural growth being
prioritized to investment in other traits. The prioritized allocation to structural growth
can reflect selective advantage of reaching a final, optimal size for a given sex as fast as
possible.
Keywords Growth· Energy· Trade-offs· Gonadal hormones· Sexual size dimorphism·
Reptiles
* Zuzana Starostová
zuzana.starostova@natur.cuni.cz
1 Department ofZoology, Faculty ofScience, Charles University, Viničná 7, 12844Prague,
CzechRepublic
2 Department ofEcology, Faculty ofScience, Charles University, Viničná 7, 12844Prague,
CzechRepublic

470
Evolutionary Ecology (2020) 34:469–481
1 3
Direct split ofenergy: anuntested assumption ofgrowth models
The study of energy in living organisms is essential for understanding the regulation of major
life history traits such as growth and reproduction. All living organisms have a limited amount
of allocable energy, which force them to optimize allocation to energetically demanding life-
history traits such as growth, maintenance and reproduction (Stearns 2000; West etal. 2001;
Taborsky 2017). The concept of such energy allocation trade-offs is widespread in evolution-
ary ecology (Angilletta etal. 2003) and we can hardly imagine an alternative to it. Neverthe-
less, it is often assumed automatically that the limitation of an energy budget or higher alloca-
tion to a single trait affects all other life history traits. Several models that tried to describe the
ontogenetic growth trajectories from the energetical perspective are based on this rarely tested
assumption (von Bertalanffy 1957; West etal. 2001; Martin etal. 2019; Sibly and Brown
2020). In other words, these growth models assumed that ontogenetic growth is very pheno-
typically plastic and that changes in growth are directly affected by allocation to other traits,
mainly to reproduction. For example, the general model by West etal. (2001) suggests that
acquired energy related to metabolic rate is split into three components: to the maintenance
of existing tissue, the replacement of cells and the formation of new tissue. According to this
model, a substantial portion of energy is later in ontogeny allocated to reproduction, which is
accompanied directly due to energy limitations with a reduction in growth (West etal. 2001).
Similar logic was also applied to explain the ontogeny of sexual size dimorphism (SSD), i.e.
differences in size between the sexes. The so called “reproductive cost” hypothesis states that
allocation to growth should be smaller in the sex with higher reproductive cost (Cox 2006),
i.e. that the amount of energy allocated to reproduction is directly traded-off with the alloca-
tion to growth.
The idea that ontogenetic growth is plastic with respect to the total energy budget or to
the amount of energy allocated to reproduction and other energetically demanding traits is so
appealing that it is in fact rarely tested. It has straightforward predictions: growth and hence
final body size should correlate with the total amount of available energy and with the allo-
cation to other energetically demanding processes such as reproduction and tissue regenera-
tion. Nevertheless, we realized in the series of growth experiments in the model lizard species
Madagascar ground gecko, Paroedura picta (Peters, 1854), that these intuitive predictions are
not followed. Here, we summarized the observed effect of manipulations with diet, allocation
to reproduction and tissue regeneration on structural growth, i.e. increase in snout-vent length
(SVL) reflecting skeleton dimensions, in this species. As typical reptile with “indeterminate
growth”, P. picta mature at a size representing a small fraction of its final body size (males
can mature at the body mass of c. 3 g and continue to final body mass of 35–40 g, females
mature at about 4 g and their final mass is around 15–19 g; own data). An enormous fraction
of postembryonic growth in this species thus proceeds after the start of reproduction, which is
convenient for the manipulative growth experiments focused on energy allocation. We provide
insights into the proximate control of sex-specific growth trajectories and suggests an explana-
tion at the ultimate level, why the predictions based on direct differential allocation were not
followed.

471
Evolutionary Ecology (2020) 34:469–481
1 3
Sexual dimorphism ingrowth isnotdirectly related toallocation
toreproduction
One field where an energetical perspective on the control of growth became prevalent is the
ontogeny of SSD. SSD in body size is widespread in animals including reptiles and male-
or female-biased SSD can be found across taxa, sometimes even closely related species
being at the opposite side of the spectrum (Cox etal. 2007). For instance, our model spe-
cies P. picta experiences male-biased SSD while the closely related species P. vazimba and
P. androyensis are female larger (Starostová etal. 2010). The “reproductive cost” hypoth-
esis based on an energetical perspective states that a trade-off between reproduction and
growth due to the high energetical cost of reproduction is at the core of SSD development.
This hypothesis was tested mostly in reptiles with male-biased SSD (Cox 2006), but it can
also be relevant for species with female-biased dimorphism since the cost of reproduction
has been found for both sexes across taxa (Hayward and Gillooly 2011).
In male-larger species, the “reproductive cost” hypothesis was traditionally tested by
removing female allocation to reproduction by ovariectomy, which should remove the
energetical cost of reproduction and therefore lead to higher allocation to growth. Higher
growth rate and/or larger structural body in females comparable to male-typical pattern
was indeed observed in ovariectomized females in the Yarrow’s spiny lizard, Scelopo-
rus jarrovii (Cox 2006), brown anole, Anolis sagrei (Cox and Calsbeek 2010; Cox etal.
2014) and the Madagascar ground gecko P. picta (Starostová etal. 2013; Kubička etal.
2017; schematically depicted in Fig.1), which could be taken (and often was) as support
for the “reproductive cost” hypothesis (Cox 2006; Cox and Calsbeek 2010). As charac-
teristic for geckos, P. picta lay maximally two eggs per clutch, but the clutches are very
frequent in this species leading to enormous reproductive effort (Kubička and Kratochvíl
2009; Kubička etal. 2012; Starostová etal. 2012). The idea that non-reproducing females
allocate saved energy to growth is thus seemingly supported.
However, Starostová et al. (2013) also used social isolation as another way of block-
ing energy allocation to egg production next to ovariectomy in P. picta as females of this
species do not produce eggs if they do not have access to sperm. Surprisingly, females in
reproductive isolation did not differ in growth trajectory in SVL and in final SVL from
regularly reproducing females (Fig.1), which suggests that the female reproductive cost is
not responsible for the ontogeny of SSD in this species.
These authors suggested that ovariectomy removed not only reproductive cost but also
production of ovarian hormones, which can drive females to female-typical growth trajec-
tory leading to decreased final SVL directly, not via allocation to reproduction. A follow
up study by Kubička etal. (2017) extended the test of the “reproductive cost” and “ovar-
ian hormone” hypotheses. They found that contrary to the predictions of the “reproductive
cost” hypothesis, unilaterally ovariectomized females that produced around half of eggs
in comparison to sham operated females while maintaining normal hormonal cycling,
reached a comparable final size in terms of SVL via the same growth trajectory as control
sham operated females (Fig.1). Moreover, ovariectomized females of P. picta receiving
exogenous estradiol reached a smaller size, which suggests that female growth can be sup-
pressed by gonadal estrogens (Kubička etal. 2017).
Manipulations in males also found little support for the “reproductive cost” hypoth-
esis. Sperm production is energetically demanding and can be restricted by metabolic
rate and total available energy (Hayward and Gillooly 2011). Removal of allocation
to gonads in growing males should thus lead to higher allocation to structural growth.

472
Evolutionary Ecology (2020) 34:469–481
1 3
However, growth rate and final SVL in males of P. picta was not affected by castra-
tion both under constant temperature (Starostová etal. 2013) and in a thermal gradient
(Kubička etal. 2015) (Fig.1). These results also suggest that male gonadal androgens
are not responsible for the increased growth in males in comparison to females and by
extension for the ontogeny of SSD in P. picta. Control of male growth by male gonadal
androgens was suggested as a major mechanism of evolutionary changes in SSD in
squamate reptiles (Cox etal. 2005, 2009). The evidence for masculinized growth by
the application of exogenous androgens in females was initially taken as a support for
the control of SSD ontogeny by male gonadal androgens (Cox etal. 2009). However,
this assumption has been challenged as it is not consistent with the lack of the effect
of castration on growth in males P. picta (Kubička etal. 2015) and other lizard spe-
cies (Kubička etal. 2013; Bauerová etal. 2020). Equally as ovariectomy, application of
exogenous androgens likely causes defeminization, i.e. the suppression of the develop-
ment of female-typical morphology via interference with normal ovarian hormonal pro-
duction, not masculinization of female growth trajectory (Starostová etal. 2013). The
agreement of various, mutually complementary experimental data (schematically pre-
sented in Figs.1 and 2) implies that SSD in P. picta is caused by suppressed growth in
females, which cannot be attributed to their high allocation to reproduction but is likely
driven by ovarian hormones as the key proximate mechanism switching between sex-
specific growth trajectories.
Fig. 1 Schematic depiction of postembryonic structural growth trajectories in accordance to sex and treat-
ment in Paroedura picta. Only ovariectomy affects female growth and final snout-vent length likely causing
defeminization in absence of hormones produced by ovaries. All other experimental treatments depicted
fail to affect the growth of experimental animals. Arrow indicates the start of experimental manipulations.
Schematic growth depiction for experimental groups (from above): control males, castrated males, ovariec-
tomized females, control reproducing females, unilaterally ovariectomized reproducing females, females in
social isolation

473
Evolutionary Ecology (2020) 34:469–481
1 3
Fig. 2 Summary of the results from case studies in Paroedura picta that show that growth does not seem to be
influenced by variations in allocable energy. a The “reproductive cost” hypothesis predicts that removal of the
costs of reproduction should lead to higher allocation to growth in both sexes. However, castrated males attained
the same size as non-castrated control males (Starostová etal. 2013). Socially isolated non-reproducing females
and females with highly decreased allocation to reproduction due to unilateral ovariectomy maintained similar
body size (SVL) and growth rate as control regularly egg-laying females (Kubička etal. 2017). Only full ovariec-
tomy led to higher allocation to structural growth in females, which indicates that ovarian hormones, not directly
allocable energy, controls ontogeny of sexual size dimorphism via negative effect on growth in females (Kubička
etal. 2017). b In the case of food restriction, we expected that restricted diet would lead to reduced allocation
to reproduction, growth and fat storage. However, structural growth was not affected by food limitations, which
reduced only allocation to reproduction and fat storage (Kubička and Kratochvíl 2009). c The simple energy allo-
cation trade-off predicts that growth should be decreased in the lizards during tail regeneration. Nevertheless,
geckos with and without growth regeneration had similar growth rates and reached similar structural body size
(Starostová etal. 2017). Silhouette images were taken and modified from: https ://pixab ay.com/

474
Evolutionary Ecology (2020) 34:469–481
1 3
Food restriction: limited reproduction andfat storage,
butnotstructural growth
Energy allocation to growth and reproduction was studied in females of P. picta also
through restriction of allocable energy via manipulation with food quantity (Kubička
and Kratochvíl 2009). Two balanced groups of young, still growing females kept at dif-
ferent food levels were followed for six months until cessation of growth. The expec-
tation based on direct differential allocation was that the limited energy intake would
impair growth rate and possibly final structural body size represented by final SVL
(Fig.2). Nevertheless, females on a restricted diet maintained growth rate and attained
the same final SVL as females with higher food intake (Kubička and Kratochvíl 2009).
They did however compromise on their reproduction. Females on the restricted diet
laid smaller eggs in longer intervals. Diet restriction also led to the lower body mass
and thus fat reserves when compared to females with higher food intake. A trade-off
between growth and reproduction does not seem to occur in its simplest form here with
an expected allocation compromise between these processes. In this case study, the allo-
cation to structural growth was clearly more canalized than allocation to reproduction.
Little eect ofenergy limitation throughtail autotomy onstructural
growth
Another factor that should affect the allocable energy to life history traits is tail autot-
omy, a widespread defence strategy of a vast number of lizard species, which is com-
monly followed by tail regeneration (Arnold 1988; Bateman and Fleming 2009). By
shedding a tail lizards can lose a substantial proportion of body mass (Jagnandan and
Higham 2018) and possibly also an energy reserve since tails are an important organ
for fat storage (Pond 1978; Paz etal. 2019). Tails also need to be regenerated since they
are important for locomotion and balance (Gillis etal. 2009; Gillis and Higham 2016;
Jagnandan and Higham 2018) as well as social interaction (Fox etal. 1990; Martín
and Salvador 1993). The energetical cost of tail regeneration can come to the expense
of growth (Ballinger and Tinkle 1979; Niewiarowski etal. 1997; Lynn etal. 2013) or
reproduction (Dial and Fitzpatrick 1981; Wilson and Booth 1998; Chapple etal. 2002),
but the support is ambiguous (e.g.,Fox and McCoy 2000; Goodman 2006; Webb 2006).
In a study on P. picta, the cost of tail regeneration in growing juvenile males was evalu-
ated (Starostová etal. 2017). Tail autotomy was induced in juvenile, approximately four
months old males still in the phase of rapid growth and their growth was followed and
compared to intact control group for more than five months. The prediction based on a
simple direct differential energy allocation was that the growth rate and final SVL of
the juveniles that suffered tail autotomy would be hindered compared to intact juveniles
(Fig.2). However, tail autotomy and its subsequent regeneration did not affect structural
growth and resulted in a similar SVL. Furthermore, mass-corrected metabolic rate was
not significantly affected by tail loss and allocation to regeneration. It seems that fast
growing juveniles can compensate tail autotomy at least under unrestricted food condi-
tions without a notable change in mass-specific metabolic rate. Future studies should
test whether the same pattern would be observed also under food limitation.

475
Evolutionary Ecology (2020) 34:469–481
1 3
Structural growth isstill plastic withrespect totemperature
The above discussed findings suggested that structural growth represented by change in
SVL during the postembryonic ontogeny in P. picta is less phenotypically plastic than
generally assumed under manipulation with energetically demanding processes. But, is
it plastic with respect to other factors than energy allocation? Considering ectotherms,
i.e. animals that rely on external sources for body heat, a clearly essential factor influ-
encing structural growth is environmental temperature. The Temperature size rule states
that ectotherms develop faster but mature at smaller body sizes at higher temperatures
whereas ectotherms maintained at low temperatures grow more slowly, but attain a
larger final body size (Atkinson 1994; Zuo etal. 2012). Temperature has indeed a strong
influence on growth in P. picta (Starostová etal. 2010). Animals incubated and reared
until cessation of growth under three different environmental temperatures did not fol-
low the Temperature size rule, but body size in terms of SVL was higher especially
in males at the intermediate temperature (Starostová etal. 2010). The effect of tem-
perature at least in P. picta does not operate via changes in number of trunk vertebrae
(Kratochvíl etal. 2018), but partially via influence on cell size at least in some tissues
(Czarnoleski etal. 2017). The influence of temperature on growth and final body size
in animals was considered as an energy allocation problem (Zuo etal. 2012); however,
this hypothesis deserves further attention and seems less likely taking into account that
growth responses of P. picta to manipulation with energetically demanding processes
are rather limited.
Why isgrowth highly canalized whenfacing energy limitations?
Being indoctrinated by the simple energy allocation perspective before we conducted
these growth studies introducing both decreased and increased demands of other ener-
getically demanding processes, we did not expect that growth would be so canalized
with respect to manipulations affecting energy and were ever surprised by the results.
The growth experiments challenged the idea of simple direct allocation of growth versus
other energetically demanding processes (summarized in Fig.2). Growth was affected
neither by reduced energy uptake through food restriction (Kubička and Kratochvíl
2009) nor by hindering the energy balance during growth through tail autotomy and
regeneration (Starostová etal. 2017). By extension, simple trade-offs in energy alloca-
tion between growth and reproduction was not supported by studies in P. picta (Kubička
and Kratochvíl 2009; Starostová etal. 2013; Kubička etal. 2017).
The inherent insignificant role of simple energy allocation in the case of growth in
P. picta is even more evident when comparing the role of energy in another life history
trait, reproduction. Reproduction was found to be more sensitive to allocable energy in
the study on food restriction (Kubička and Kratochvíl 2009). This difference in varia-
tion between growth and reproduction is also highlighted through a substantial differ-
ence in environmental plasticity. Reproduction in P. picta is also heavily influenced by
temperature (Starostová etal. 2012). Overall, females at higher temperatures produced
smaller eggs which is consistent with the pattern found in ectotherms (e.g.,Blancken-
horn 2000; Oufiero etal. 2007), and rate of reproduction (amount of energy allocated
to reproduction per unit of time) was smaller for females at the lowest of the tested

476
Evolutionary Ecology (2020) 34:469–481
1 3
temperatures (Starostová etal. 2012). The plasticity of growth regarding temperature is
clearly less significant than in reproduction indicating the more plastic nature of repro-
duction compared to growth.
Why do the predictions from differential energy allocations fail so much (Fig.2)? The
structural growth rate and final SVL has some capability for phenotypic plasticity as exem-
plified by manipulations with rearing temperature described above. Also, structural growth
trajectories can be shaped in P. picta by hormonal manipulations bringing further evidence
that growth trajectories are not totally fixed. So, why is structural growth to a high extent
canalized with respect to changes in an energy budget, even more so when compared to
reproductive traits? One possible explanation is that selection in geckos and possibly other
lizards is preferring the allocation rules prioritizing structural growth to other traits such
as reproduction, fat storage and regeneration. It is possible that the allocation to particu-
lar traits is not totally mutually plastic as commonly assumed under the intuitive logic of
“higher allocation to reproduction means less allocation to growth”, but that the allocation
of energy followed a hierarchical rule with the priority given to structural growth. This
hypothesis was suggested by Kubička and Kratochvíl (2009) interpreting the results of
their food limitation experiment. They concluded that energy is allocated to reproduction
only after demands of structural growth are fulfilled, and to fat storage only when the maxi-
mal possible allocation to reproduction was achieved.
The degree of phenotypic plasticity, more specifically canalization (e.g., Walzer and
Schausberger 2014), should reflect selective pressures. Canalization—no matter whether
against environmental or genetic perturbations—should evolve when there is a stabiliz-
ing selection on a trait value (Stearns and Kawecki 1994). At the current stage of knowl-
edge, we can only speculate why structural growth should be prioritized in P. picta over
other traits. Body size is a crucial fitness-related trait and as such it should be optimized.
Body size is connected with food intake—in a gape limited predators like geckos body
size determines maximal and minimal prey size (Daza etal. 2009), antipredator strategies
(Roth and Johnson 2004), dealing with competitors (Pafilis etal. 2009) and optimal repro-
ductive performance, e.g. due to positive egg size-body size relationship demonstrated in
geckos (Kratochvíl and Frynta 2006) and other reptiles (e.g. Escalona etal. 2018). Reach-
ing an optimal size as fast as possible for a given ecological niche and keeping it as long
as possible throughout life span might be important. Of course, reptiles including P. picta
start reproduction well before reaching the final/close to asymptotic structural body size.
This hypothesis trying to explain the canalization of allocation to structural growth expects
that the performance, including reproductive performance, should be suboptimal before the
period of the cessation of growth. We welcome tests of this hypothesis in the future.
The optimal size could be sex-specific, e.g. due to sexual selection or other sex-specific
roles (Darwin 1871; Cox etal. 2003; Fairbairn etal. 2007). Males of P. picta are highly
combative (Golinski etal. 2014; Schořálková etal. 2018) and intrasexual selection can
thus be a selective force responsible for male-larger SSD in this species. At the proximate
level, it seems that males in this species are not larger because females do not have enough
energy for growth as they allocate more to reproduction, but because each sex has their
own optimal trajectory of ontogenetic structural growth. Gonadal hormones, particularly
ovarian hormones seem to be the signal to cells in the body which of these trajectories
should be followed during the ontogeny (Starostová etal. 2013; Kubička etal. 2017).

477
Evolutionary Ecology (2020) 34:469–481
1 3
Limits ofour approach
We acknowledge the limits for generalizations brought by focusing on one species. How-
ever, in this review we chose to focus on a well-studied—and hopefully not too special
and exceptional—gecko since we considered it would help to tell a complex story as best
as possible and at the same time to control several potentially confounding issues. While
we have attempted to add arguments from other species, we found such parallels between
species to be harder to establish, as we doubt that there is another species where simi-
lar manipulative long-term growth experiments were performed under so many treatments
under so similar conditions, and partial studies (e.g. only a test of the effect of tail autot-
omy on growth in one species, but of the removal of the allocation to female reproduction
in the other) might be confounded by differences in life-history decisions and other aspects
of species biology. Although we tried to analyze as many parameters as possible in our
growth experiments, we are aware that these studies are not complete. For example, activ-
ity has been found to influence distribution of energy and the expression of life history
traits such as reproduction or immunity (Lailvaux and Husak 2014; Husak and Lailvaux
2017; Husak etal. 2017), but it was mostly not considered in our experiments. We only
found that castrated and control males did not differ in the activity in the open field test
performed in the neutral arena (Kubička etal. 2015), but we lack data for other experi-
ments. As all treatment groups in each of our former experiments were held in the same
environment (the same thermal environment, social isolation, the same size and equipment
of cages) and hence likely possessed similar activity patterns, it is not very likely that the
difference in the activity pattern would explain the notable lack in the response in the struc-
tural growth. In the case of different activity pattern among treatment group, groups would
have to precisely counterbalance the allocation to growth with differences in activity,
which seems unlikely. However, the energetical cost of activity and its influence on other
life history traits such as growth and reproduction should be more explored in the future.
As natural conditions certainly are more demanding for energy intake than conditions in
the laboratory, it will be important to do more energetically focused research on growth
also in the field, which will be especially important to elucidate the evolutionary context of
growth canalization observed by us in the laboratory experiments.
Conclusions andfuture perspectives
Overall, we documented that although structural growth has some potential to be plastic
and it is sexuall dimorphic in P. picta, it is at the same time to a large degree canalized with
respect to an energy budget. This pattern is consistent with the idea that structural growth
is carefully regulated and that allocation to it is prioritized to other life history traits, most
importantly to reproduction. Importantly, this observation challenges the general growth
models based on dynamic energy budgets as they assume that the limitation of an energy
budget or higher allocation to a single trait—mostly to reproduction—affects all other life
history traits (von Bertalanffy 1957; West etal. 2001) and neglect that there might exist a
strict hierarchical rules shaped by selection for priority allocation of metabolized energy
to structural growth (or other traits). The simplified energetical perspective became also
influential in macroecology being claimed responsible for major ecological rules in the
so called “metabolic theory of ecology” aiming to quantify the processes of acquisition

478
Evolutionary Ecology (2020) 34:469–481
1 3
and use of resources, to explain different biological patterns of life history traits such as
growth (Brown etal. 2004; Martin etal. 2019). However, the recent large-scale comparison
across eukaryotes suggests that metabolism and thus energy income is not necessarily at
the core control of biomass increase (Hatton etal. 2019). Hatton etal. (2019) propose that
instead of a fundamental metabolic control and limitation of growth, metabolism adjusts to
growth (understood there as a maximum population growth rate, i.e. intrinsic growth rate,
multiplied by individual adult body mass) within major groups, which agrees with here
advocated perspective that a simple and intuitive energy allocation rule is not operating
at the individual level and that growth is carefully regulated endogenously. We argue that
this endogenous control reflects past selective pressures shaping the structure of allocation
rules. Future growth models should incorporate these findings and be based on carefully
tested, not only intuitively appealing assumptions on energy allocations.
Next to growth, analogous situation challenging classical views based on simple trade-
offs in energy allocation recently emerged in another key life-history trait, ageing (Lind
etal. 2019). The classical disposable soma theory of ageing states that the limited amount
of energy can be either used for maintenance and repair or growth and reproduction result-
ing in trade-offs, with energy limitations for repair leading to the accumulation of unre-
paired cellular damage with age (Kirkwood etal. 1979; Lind et al. 2019; Maklakov and
Chapman 2019). However, recent evidence suggests that simple energy allocation between
life history traits is not at the heart of variability in ageing. Similar to structural growth,
delayed ageing is highly endogenously controlled, in the case of aging by a conserved insu-
lin/IGF-1 nutrient-sensing signaling pathway (Lind etal. 2019). In the case of ontogenetic
growth, a prominent and well conserved pathway responsible for growth regulation and its
variability and plasticity can be the insulin and insulin-like signalling network (Shingle-
ton 2011; Stearns 2011). The ovarian hormones can be an important sex-specific modifier
of the structural growth pathways. Evidence brought up for structural growth and aging
demonstrates that trade-offs can be mediated at the proximate level by switches in sig-
nalling pathways independently from direct simple energy allocations (Flatt etal. 2011;
Stearns 2011). As evolutionary ecologists, we should stop thinking in the framework of
simple direct differential energy allocation unless based on solid empirical evidence and
we should focus on the question how selective forces shape complex, likely hierarchical
structure of allocation rules and how it is reflected in proximate mechanisms controlling
life-history decisions.
Acknowledgements This project was supported by the Czech Science Foundation (GACR 19-19746S).
B.M. was also supported by the internal Charles University Grant SVV260571/2020. We would like to
thank Jan Červenka for animal care and long-lasting support and to all coauthors of case studies on P. picta
for their contribution and stimulating discussions. We would also like to thank the reviewers for exception-
ally insightful comments.
Compliance with ethical standards
Conict of interest The authors declare no conflicts of interest.
References
Angilletta MJ, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction
norms. Trends Ecol Evol 18:234–240

479
Evolutionary Ecology (2020) 34:469–481
1 3
Arnold EN (1988) Caudal autotomy as a defence. In: Gans C, Huey R (eds) Biology of the Reptilia. Volume
16. Ecology. B. Alan R. Liss, New York, pp 235–273
Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58
Ballinger R, Tinkle D (1979) On the cost of tail regeneration to body growth in lizards. J Herpetol
13:374–375
Bateman PW, Fleming PA (2009) To cut a long tail short: a review of lizard caudal autotomy studies carried
out over the last 20 years. J Zool 277:1–14
Bauerová A, Kratochvíl L, Kubička L (2020) Little if any role of male gonadal androgens in ontogeny of
sexual dimorphism in body size and cranial casque in chameleons. Sci Rep 10:26–73
Blanckenhorn WU (2000) Temperature effects on egg size and their fitness consequences in the yellow dung
fly Scathophaga stercoraria. Evol Ecol 14:627–643
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology.
Ecology 85:1771–1789
Chapple D, Mccoull C, Roy S (2002) Changes in reproductive investment following caudal autotomy in
viviparous skinks (Niveoscincus metallicus): lipid depletion or energetic diversion? J Herpetol
36:480–486
Cox R, Skelly S, John-Alder H (2003) A compatative test of adaptive hypotheses for sexual size dimorphism
in lizards. Evolution 57:1653–1669
Cox RM, Skelly SL, John-Alder HB (2005) Testosterone inhibits growth in juvenile male eastern fence
lizards (Sceloporus undulatus): implications for energy allocation and sexual size dimorphism. Physiol
Biochem Zool 78:531–545
Cox RM (2006) A test of the reproductive cost hypothesis for sexual size dimorphism in Yarrow’s spiny
lizard Sceloporus jarrovii. J Anim Ecol 75:1361–1369
Cox RM, Butler M, John-Alder H (2007) The evolution of sexual size dimorphism in reptiles. In: Fairbairn
DJ, Blanckenhorn WU, Székely T (eds) Sex, size and gender roles: evolutionary studies of sexual size
dimorphism. Oxford University Press, New York, pp 38–49
Cox RM, Stenquist D, Calsbeek R (2009) Testosterone, growth and the evolution of sexual size dimor-
phism. J Evol Biol 22:1586–1598
Cox RM, Calsbeek R (2010) Severe costs of reproduction persist in Anolis lizards despite the evolution of a
single-egg clutch. Evolution 64:1321–1330
Cox RM, Lovern MB, Calsbeek R (2014) Experimentally decoupling reproductive investment from energy
storage to test the functional basis of a life-history trade-off. J Anim Ecol 83:888–898
Czarnoleski M, Labecka AM, Starostová Z, Sikorska A, Bonda-Ostaszewska E, Woch K, Kubička L, Kra-
tochvíl L, Kozlowski J (2017) Not all cells are equal: effects of temperature and sex on the size of dif-
ferent cell types in the Madagascar ground gecko Paroedura picta. Biol Open 6:1149–1154
Darwin C (1871) The descent of man and selection in relation to sex. John Murray, London
Daza J, Herrera A, Richard T, Hector C (2009) Are you what you eat? A geometric morphometric analysis
of gekkotan skull shape. Biol J Linn Soc 97:677–707
Dial BE, Fitzpatrick LC (1981) The energetic costs of tail autotomy to reproduction in the lizard Coleonyx
brevis (Sauria: Gekkonidae). Oecologia 51:310–317
Escalona T, Dean A, Valenzuela N (2018) A lengthy solution to the optimal propagule size problem in the
large-bodied South American freshwater turtle, Podocnemis unifilis. Evol Ecol 32:29–41
Fairbairn D, Blanckenhorn W, Székely T (2007) Sex, size and gender roles: evolutionary studies of sexual
size dimorphism. Oxford University Press, New York
Flatt T, Heyland A, Stearns SC (2011) What mechanistic insights can or cannot contribute to life history
evolution: an exchange between Stearns, Heyland, and Flatt. In: Flatt T, Heyland A (eds) Mechanisms
of life history evolution. Oxford University Press, New York, pp 375–379
Fox SF, Heger NA, Delay LS (1990) Social cost of tail loss in Uta stansburiana: lizard tails as status-signal-
ling badges. Anim Behav 39:549–554
Fox SF, McCoy J (2000) The effects of tail loss on survival, growth, reproduction, and sex ratio of offspring
in the lizard Uta stansburiana in the field. Oecologia 122:327–334
Gillis G, Bonvini LA, Irschick DJ (2009) Losing stability: tail loss and jumping in the arboreal lizard Anolis
carolensis. J Exp Biol 212:604–609
Gillis G, Higham TE (2016) Consequences of lost endings: caudal autotomy as a lens for focusing attention
on tail function during locomotion. J Exp Biol 219:2416–2422
Golinski A, Kubička L, John-Alder H, Kratochvíl L (2014) Elevated testosterone is required for male copu-
latory behavior and aggression in Madagascar ground gecko (Paroedura picta). Gen Comp Endocrinol
205:133–141
Goodman RM (2006) Effects of tail loss on growth and sprint speed of juvenile Eumeces fasciatus (Scinci-
dae). J Herpetol 40:99–102

480
Evolutionary Ecology (2020) 34:469–481
1 3
Hatton IA, Dobson AP, Storch D, Galbraith ED, Loreau M (2019) Linking scaling laws across eukaryotes.
Proc Natl Acad Sci USA 116:21616–21622
Hayward A, Gillooly JF (2011) The cost of sex: quantifying energetic investment in gamete production by
males and females. PloS ONE 6:e16557
Husak J, Lailvaux S (2017) How do we measure the cost of whole-organism performance traits? Integr
Comp Biol 57:333–343
Husak J, Roy J, Lovern B (2017) Exercise training reveals trade-offs between endurance performance and
immune function, but does not influence growth, in juvenile lizards. J Exp Biol 220:1497–1502
Jagnandan K, Higham TE (2018) Neuromuscular control of locomotion is altered by tail autotomy in
geckos. J Exp Biol 221:jeb179564
Kirkwood TBL, Holliday R, Smith JM, Holliday R (1979) The evolution of ageing and longevity. Proc R
Soc Lond B 205:531–546
Kratochvíl L, Frynta D (2006) Body-size effect on egg size in eublepharid geckos (Squamata: Eublephari-
dae), lizards with invariant clutch size: negative allometry for egg size in ectotherms is not universal.
Biol J Linn Soc 88:527–532
Kratochvíl L, Kubička L, Vohralík M, Starostová Z (2018) Variability in vertebral numbers does not con-
tribute to sexual size dimorphism, interspecific variability, or phenotypic plasticity in body size in
geckos (Squamata: Gekkota: Paroedura). J Exp Zool A 329:185–190
Kubička L, Kratochvíl L (2009) First grow, then breed and finally get fat: hierarchical allocation to life-
history traits in a lizard with invariant clutch size. Funct Ecol 23:595–601
Kubička L, Starostová Z, Kratochvíl L (2012) Temperature-dependent rate of clutch production in a tropical
lizard (Paroedura picta: Gekkonidae): intraspecific test of the metabolic theory of ecology. J Therm
Biol 37:179–184
Kubička L, Golinski A, John-Alder H, Kratochvíl L (2013) Ontogeny of pronounced female-biased sexual
size dimorphism in the Malaysian cat gecko (Aeluroscalabotes felinus: Squamata: Eublepharidae): a
test of the role of testosterone in growth regulation. Gen Comp Endocrinol 188:183–188
Kubička L, Starostová Z, Kratochvíl L (2015) Endogenous control of sexual size dimorphism: gonadal
androgens have neither direct nor indirect effect on male growth in a Madagascar ground gecko (Par-
oedura picta). Gen Comp Endocrinol 224:273–277
Kubička L, Schořálková T, Červenka J, Kratochvíl L (2017) Ovarian control of growth and sexual size
dimorphism in a male-larger gecko. J Exp Biol 220:787–795
Lailvaux S, Husak J (2014) The life history of whole-organism performance. Q Rev Biol 89:285–318
Lind MI, Ravindran S, Sekajova Z, Carlsson H, Hinas A, Maklakov AA (2019) Experimentally reduced
Insulin/IGF-1 signaling in adulthood extends lifespan of parents and improves darwinian fitness of
their offspring. Evol Lett 3:207–216
Lynn S, Borkovic B, Russell B (2013) Relative apportioning of resources to the body and regenerating tail
in juvenile leopard geckos (Eublepharis macularius) maintained on different dietary rations. Physiol
Biochem Zool 86:659–668
Maklakov AA, Chapman T (2019) Evolution of ageing as a tangle of trade-offs: energy versus function.
Proc R Soc Lond B 286:20191604
Martin T, Thorbek P, Ashauer R (2019) Common ground between growth models of rival theories: a useful
illustration for beginners. Ecol Model 407:108712
Martín J, Salvador A (1993) Tail loss reduces mating success in the Iberian rock-lizard, Lacerta monticola.
Behav Ecol Sociobiol 32:185–189
Niewiarowski P, Congdon J, Dunham A, Vitt L, Tinkle DW (1997) Tales of lizard tails: effects of tail
autotomy on subsequent survival and growth of free-ranging hatchling Uta stansburiana. Can J Zool
75:542–548
Pafilis P, Meiri S, Foufopoulos J, Valakos E (2009) Intraspecific competition and high food availability are
associated with insular gigantism in a lizard. Sci Nat 96:1107–1113
Oufiero CE, Smith A, Angilletta MJ (2007) The importance of energetic versus pelvic constraints on repro-
ductive allocation in the eastern fence lizard (Sceloporus undulatus). Biol J Linn Soc 91:513–521
Paz MM, García NE, Semhan RV, Lobo FJ, Abdala CS (2019) Study of lipid reserves in Liolaemus
koslowskyi (Squamata: Liolaemidae): reproductive and ecological implications. J Comp Physiol B
189:595–609
Pond CM (1978) Morphological aspects and the ecological and mechanical consequences of fat deposition
in wild vertebrates. Annu Rev Ecol Syst 9:519–570
Roth ED, Johnson JA (2004) Size-based variation in antipredator behavior within a snake (Agkistrodon pis-
civorus) population. Behav Ecol 15:365–370
Schořálková T, Kratochvíl L, Kubička L (2018) To fight or mate? Hormonal control of sex recognition,
male sexual behavior and aggression in the gecko lizard. Horm Behav 97:18–24

481
Evolutionary Ecology (2020) 34:469–481
1 3
Shingleton AW (2011) Evolution and the regulation of growth and body size. In: Flatt T, Heyland A (eds)
Mechanisms of life history evolution. Oxford University Press, New York, pp 43–55
Sibly RM, Brown JH (2020) Toward a physiological explanation of juvenile growth curves. J Zool. https ://
doi.org/10.1111/jzo.12770
Starostová Z, Kubička L, Kratochvíl L (2010) Macroevolutionary pattern of sexual size dimorphism in
geckos corresponds to intraspecific temperature-induced variation. J Evol Biol 23:670–677
Starostová Z, Angilletta MJ, Kubička L, Kratochvíl L (2012) Thermal dependence of reproductive alloca-
tion in a tropical lizard. J Therm Biol 37:159–163
Starostová Z, Kubička L, Golinski A, Kratochvíl A (2013) Neither male gonadal androgens nor female
reproductive costs drive development of sexual size dimorphism in lizards. J Evol Biol 216:1872–1880
Starostová Z, Gvoždík L, Kratochvíl L (2017) An energetic perspective on tissue regeneration: the costs of
tail autotomy in growing geckos. Comp Biochem Physiol A 206:82–86
Stearns SC, Kawecki TJ (1994) Fitness sensitivity and the canalization of life-history traits. Evolution
48:1438–1450
Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften
87:476–486
Stearns SC (2011) Does impressive progress on understanding mechanisms advance life history theory? In:
Flatt T, Heyland A (eds) Mechanisms of life history evolution. Oxford University Press, New York, pp
364–374
Taborsky B (2017) Developmental plasticity: preparing for life in a complex world. In: Naguib M, Podos J,
Simmons LW, Barrett L, Healy SD, Zuk M (eds) Advances in the study of behavior. vol 49, Academic
Press, pp 49–99
von Bertalanffy L (1957) Quantitative laws in metabolism and growth. Q Rev Biol 32:217–231
Walzer A, Schausberger P (2014) Canalization of body size matters for lifetime reproductive success of
male predatory mites (Acari: Phytoseiidae). Biol J Linn Soc 111:889–899
Webb JK (2006) Effects of tail autotomy on survival, growth and territory occupation in free-ranging juve-
nile geckos (Oedura lesueurii). Austral Ecol 31:432–440
West GB, Brown JH, Enquist BJ (2001) A general model for ontogenetic growth. Nature 413:628–631
Zuo W, Moses M, West GB, Hou C, Brown JH (2012) A general model for effects of temperature on ecto-
therm ontogenetic growth and development. Proc R Soc Lond B 279:1840–1846
Wilson RS, Booth DT (1998) Effect of tail loss on reproductive output and its ecological significance in the
skink Eulamprus quoyii. J Herpetol 32:128–131
Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and
institutional affiliations.