Download Body Size, Performance and Fitness in Galapagos Marine Iguanas1

INTEGR. COMP. BIOL., 43:376–386 (2003)
Body Size, Performance and Fitness in Galapagos Marine Iguanas1
MARTIN WIKELSKI2,*
AND
L. MICHAEL ROMERO†
*Department of Ecology and Evolutionary Biology, Guyot Hall 303, Princeton University, Princeton, New Jersey 08540
†Department of Biology, Tufts University, Medford, Massachusetts 02155
SYNOPSIS. Complex organismal traits such as body size are influenced by innumerable selective pressures,
making the prediction of evolutionary trajectories for those traits difficult. A potentially powerful way to
predict fitness in natural systems is to study the composite response of individuals in terms of performance
measures, such as foraging or reproductive performance. Once key performance measures are identified in
this top-down approach, we can determine the underlying physiological mechanisms and gain predictive
power over long-term evolutionary processes. Here we use marine iguanas as a model system where body
size differs by more than one order of magnitude between island populations. We identified foraging efficiency as the main performance measure that constrains body size. Mechanistically, foraging performance
is determined by food pasture height and the thermal environment, influencing intake and digestion. Stress
hormones may be a flexible way of influencing an individual’s response to low-food situations that may be
caused by high population density, famines, or anthropogenic disturbances like oil spills. Reproductive performance, on the other hand, increases with body size and is mediated by higher survival of larger hatchlings
from larger females and increased mating success of larger males. Reproductive performance of males may
be adjusted via plastic hormonal feedback mechanisms that allow individuals to assess their social rank
annually within the current population size structure. When integrated, these data suggest that reproductive
performance favors increased body size (influenced by reproductive hormones), with an overall limit imposed
by foraging performance (influenced by stress hormones). Based on our mechanistic understanding of individual performances we predicted an evolutionary increase in maximum body size caused by global warming trends. We support this prediction using specimens collected during 1905. We also show in a commongarden experiment that body size may have a genetic component in iguanids. This ‘performance paradigm’
allows predictions about adaptive evolution in natural populations.
INTRODUCTION
it is difficult to determine how body size might evolve
(Schmidt-Nielsen, 1984).
One of the big challenges in integrative organismal
biology is to explain—and ideally predict—the evolution of complex animal traits in nature (Darwin,
1883; Bonner, 1984; West-Eberhard, 2003). A prime
example for an integrative trait is body size (Peters,
1983; Schmidt-Nielsen, 1984; Reiss, 1989; McKinney,
1990; Perrin, 1998). We know for many animals that
body size is highly heritable, with heritability coefficients (narrow-sense) ranging from 0.3 to 0.9 (Peters,
1983). Body size has also been suggested to be consistently influenced by natural selection in the wild:
Mammals on islands generally decrease in body size
towards small sizes (Brown and Maurer, 1989), while
body sizes in all endotherms appear to increase towards higher latitudes (Bergmann’s rule, e.g., Meiri
and Dayan, 2003). At the same time it remains unresolved for many animal species why they attain a specific size in a specific habitat (Dobson and Headrick,
1995). The reason why we have so little power in predicting what body size animals ought to have under
specific circumstances is that many environmental and
internal factors potentially influence body size. Thus
Performance measures integrate selective processes
Arnold (1983) suggested a simple yet powerful
method to help resolve the multitude of selective processes influencing complex traits. By studying the
performance of individuals at the organismal level we
can simultaneously integrate and quantify a large
number of potential selective agents (e.g., Tsuji et al.,
1989). One example is locomotor performance. Sprint
performance, for example, can have a direct impact
on fitness (i.e., escaping from predators), yet is the
net result of many processes, including limb morphology, muscle fiber composition, neuronal (signal
processing) capabilities and the natural environment
(e.g., altitude, ambient temperature, humidity; Huey
and Hertz, 1982; Waldschmidt and Tracy, 1983; Sinervo et al., 1991; Sorci et al., 1994; Bauwens et al.,
1995; Farley, 1997). An obvious drawback of such
composite performance measures is that the exact
mechanistic base for selection on traits may remain
unclear (Garland et al., 1991). However, we can determine which performance measures most critically
influence fitness (Sorci et al., 1994). Subsequently we
can exclude less important performances (e.g., walking performance) or factors (e.g., limb morphology)
based on the ranking of their influence on fitness
(Swoap et al., 1993). Extending Arnold’s (1983) approach, we could then start to analyze the physiolog-
1 From the Symposium Selection and Evolution of Performance
in Nature presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto,
Canada.
2 E-mail: [email protected]
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MARINE IGUANAS
377
ical mechanisms underlying specific critical performances (Klukowski et al., 1998).
MARINE IGUANAS AS MODEL SYSTEM
EVOLUTION OF BODY SIZE
FOR THE
To understand the complex trait body size, we selected the Galapagos marine iguana as a model system:
Island populations differ by more than one order of
magnitude in body mass. The maximum body mass on
Genovesa island in the NE of the Galapagos archipelago is ;1,000 g while the largest animals in SW Isabela island reach .12,000 grams (Wikelski et al.,
1997). At the same time two confounding factors that
often influence body size in unpredictable ways, predation and competition, are largely absent for adult
iguanas (Curio, 1965). There are no major predators
to adult marine iguanas except the Galapagos hawks
(Buteo galapagoensis) that kill a minor percentage of
females during the nesting periods on some islands,
independent of their body size (unpublished data, M.
Wikelski). Competition with other vertebrates is similarly unimportant for marine iguanas, which gather all
of their food in the intertidal algae flats that are exposed at low tide, or by diving for submerged algae
pastures (Wikelski and Trillmich, 1994). Marine iguanas possess specialized hindgut fermenting microbes
that help them to digest algae cell walls (Mackie et
al., 2003). Furthermore, intraspecific competition is
minimal since marine iguanas forage on red and green
algae in scramble competition, i.e., can not exclude
each other from foraging sites but simply try to maximize individual intake during the time-constrained
foraging hours (Trillmich and Trillmich, 1986). Most
individuals of each population (;95%) forage approximately every second day in the intertidal areas as soon
as high tides recede, while only the largest individuals
(mostly males, ;5% of each population) also go diving for food (Hobson, 1965; Wikelski and Hau, 1995).
Diving animals emerge from underwater foraging
bouts during the hottest time of the day and thus maximize their re-warming rate (Buttemer and Dawson,
1993).
The key natural history observation in marine iguanas that allowed for an evolutionary analysis of body
size is that the largest animals of each island die first
during adverse environmental condition such as El
Niño periods (Fig. 1, upper panel; Laurie, 1989, 1990;
Laurie and Brown, 1990a, b). During El Niños, sea
surface water temperature can rise from as low as 118C
to as high as 328C when the upwelling of cool, nutrient-rich water ceases. Post-mortem analysis suggested
that death occurred as a result of starvation induced
by a lack of food in the intertidal areas (Cooper and
Laurie, 1987). Indeed, the largest animals per island
were unable to reach high body condition values, suggesting that food supply limits body size in some way
(Fig. 1, lower panel; Wikelski and Trillmich, 1997).
FIG. 1. Body size in Galapagos marine iguanas on Santa Fe Island
influences annual survival rate (top) and maximum condition
reached per mm snout-to-vent length (SVL; bottom). Top panel: Annual survival rates between February 1991 and March 1992 for
males (open circles) and females (filled circles). Note the decrease
in survival with size, in particular in males. Lower panel: Maximum
condition calculated as residuals of a linear regression of log mass
versus log body length (Krebs and Singleton, 1993, symbols as
above). Diagonal lines indicate linear regression lines for females
(left) and males (right), each starting at the inflection point of decreasing maximum condition (redrawn after Wikelski and Trillmich,
1997).
Performance measures that are not important in
marine iguanas
Initially we predicted that locomotor performance
should be of great importance for marine iguanas as
they forage actively by grazing in the intertidal zone.
Marine iguanas have to run towards the intertidal areas
between huge breaking waves, need to sprint to crevices or behind rocks to avoid being swept away, and
have to grip the intertidal rocks as strongly as possible
to resist wave drag. We therefore first measured—as
do many lizard researchers—sprint performance, as
well as the iguana’s force of gripping wire mesh (Wikelski and Trillmich, 1994). Small animals had higher
sprint speeds compared to large individuals at high
body temperatures (358C), but not at lower body temperatures (258C; see also Bartholomew and Lasiewski,
1965; Bartholomew, 1966; White, 1973). We suggest
the ultimate reason for high sprint speeds in small
iguanas may be predation by hawks, or the need to run
from huge waves that could wash them out into the
ocean. Small animals could not grab a wire mesh as
forcefully as large animals (2 N versus 25 N). Those
data initially encouraged us to predict that sprint speed
and grabbing force would strongly influence foraging
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M. WIKELSKI
AND
performance. However, when we observed foraging
durations of animals of all sizes we found that there
was no difference in average daily foraging time according to body size: All individuals on Santa Fe island foraged for about 30 minutes in the intertidal areas (Wikelski and Trillmich, 1984). Thus although
sprint speed and grabbing force are likely important
per se, they appear to be unrelated to foraging performance (Wikelski and Trillmich, 1997).
Based on the scramble competition in the foraging
areas we then tested whether the timing of arrival in
the foraging areas significantly contributed to differential survival of large and small animals. We found
that early arrival at intertidal foraging areas was associated with improved survival during El Niño conditions (Wikelski and Hau, 1995). However, the differences in arrival time only explained survival differences within each size class of animals, not the large
differences in survival between small and large animals during El Niños. Although the discovery of presumably endogenous circatidal foraging rhythms in a
terrestrial vertebrate was interesting (Woodley et al.,
2003), it did not contribute significantly to the understanding of the evolution of body size.
Critical performance measures in marine iguanas: I)
Foraging performance
Because some of the performance measures that often explain lizard fitness turned out to be relatively
unimportant in marine iguanas, we concentrated on
foraging performances that could potentially be related
to survival (Illius and Gordon, 1992). We measured
and marked individual iguanas and observed them
continuously during their daily foraging trips, counting
every bite they made when they foraged in the intertidal or while diving. We then captured those individuals immediately after their daily foraging periods and
flushed their stomachs by lavage (Wikelski et al.,
1997). Because marine iguanas graze on pastures with
very short algae sward lengths, we are confident that
stomach washing represented all food gathered by individuals during a daily foraging trip. Subsequently we
determined the energy content of the lavaged food (30
kJ/dry mass) and the digestive efficiency of the animals (70%; Wikelski et al., 1993; Rubenstein and Wikelski, 2003). Neither algae quality nor digestive efficiency changed with body size, but total intake of
algae dry mass was higher in larger animals. However,
when we compared food intake with energy expenditure of marine iguanas of specific sizes, we found that
large animals could barely gather enough food to sustain their body size while small animals had a surplus
of energy beyond maintenance needs (Fig. 2; Drent et
al., 1999; Wikelski et al., 1997). Field metabolic rates
were measured on Fernandina Island (Nagy and Shoemaker, 1984) as well as on Santa Fe and Genovesa
islands (Drent et al., 1999) via the doubly labeled water technique. Large animals in each population were
presumably at their energetic limits, while small animals could support tissue growth or fattening with the
L. M. ROMERO
FIG. 2. The food intake (dashed and solid lines) of marine iguanas
from two islands (Genovesa, Santa Fe) differs dramatically, both
between islands and between seasons. Food intake is lower during
El Niño periods (solid line; 1991/92) compared to a ‘normal’ year
(dashed line, 1992/93). Iguanas on Santa Fe have much higher food
intakes than Genovesa iguanas. The regression lines from food intake cross the regression line from energy expenditure (field metabolic rate, FMR) at much lower body sizes in Genovesa compared
to Santa Fe. The predicted maximum body mass is much lower on
Genovesa than on Santa Fe, and lower during El Niños than during
normal years.
excess energy they had available. Interestingly, the absolute body sizes at which energy intake equaled energy expenditure were different between populations.
On Genovesa Island, where animals only reach a maximum body mass of ;1,000 grams, the energy intake
line crossed the energy expenditure line at a much
lower body size than on Santa Fe Island, where marine
iguanas reach a maximum body mass of 4,500 grams.
This result suggests that foraging performance was key
to the differences in body size between island populations (see also Illius and Gordon, 1992; Naganuma
and Roughgarden, 1990; Carbone et al., 1999). We
suggest that restrictions on foraging time do not influence metabolizable energy intake because the small
Genovesa iguanas had slightly longer foraging times
compared to the large Santa Fe iguanas (M. Wikelski,
unpublished data).
To determine the mechanistic basis for differences
in foraging performance we first analyzed the foraging
efficiency in terms of intake per bite in relation to each
metabolic gram of body mass (field metabolic rate was
found to scale to body mass to the power of ;0.8 in
marine iguanas, Nagy and Shoemaker, 1984; Drent et
al., 1999; see also Butler et al., 2002). Foraging efficiency was much higher in populations where marine
iguanas reached higher body masses (Santa Fe Island)
compared to islands where maximum sizes are smaller
(Genovesa Island; Fig. 3). In addition, we also detected
a generally decreasing trend of foraging efficiency
with body mass, larger animals being overall less efficient in their foraging efforts. However, our analysis
failed to detect a decrease in foraging efficiency
among the largest animals per island, i.e., among those
BODY SIZE
IN
FIG. 3. The foraging efficiency of marine iguanas differs between
islands and generally decreases with body size. Data show means
(n 5 6 for each data point, 6 95% CI) for iguanas of 6 size classes
on Santa Fe (circles) and 7 size classes on Genovesa islands
(squares).
individuals that show the strongest decrease in survival
during adverse environmental conditions (El Niños;
Fig. 3). Thus although differences in foraging efficiency are consistent with between-population differences
in maximum body size, they are not sufficient in predicting differential survival of iguanas within each
population.
We therefore searched for additional environmental
factors that could explain the remaining differences in
survival among the largest animals in each population
(Porter and Tracy, 1983; Huey and Kingsolver, 1989;
Bakken, 1992; Adolph and Porter, 1993; Porter et al.,
2000). Marine iguana body temperature is directly related to ambient temperature that limits the rewarming
intervals between feeding trips, as well as the warming-up phases before and after foraging in the cold
intertidal areas. Sea surface temperatures in Galapagos
can be as low as 118C which can significantly limit
foraging times (Bartholomew, 1966; Wikelski and
Trillmich, 1994). Because we already knew (see
above) that individuals of all body sizes within each
population had similar total daily foraging time, we
investigated the key parameter that might change with
body temperature during foraging trips: bite rate. We
implanted body temperature transmitters in marine
iguanas on several islands and found that the maximum speed of biting depended linearly on body temperature. High body temperatures allow significantly
faster bite rates than low body temperatures (Fig. 4).
At the same time, we also detected a slowing of digestive rate, but not digestive efficiency, at lower body
temperatures, with gut passage time having a Q10 of
about 2.5 (Wikelski et al., 1993; cf., McWilliams et
al., 1997; Secor and Phillips, 1997).
We then combined data for algae intake rates at various environmental temperatures with changes in digestion at different body temperatures in a model attempting to explain maximum body size throughout
the Galapagos archipelago. In short, the model calcu-
MARINE IGUANAS
379
FIG. 4. The maximum bite rate (squares and regression line) increases linearly with body temperature in Santa Fe marine iguanas.
Body temperature was measured via implanted radiotelemetry tags
when animals foraged in the intertidal areas (redrawn from Wikelski
and Trillmich, 1994). The amount of food material that passed
through the gut was related to body temperature with a Q10 of about
2.5, thus a decrease in body temperature by 108C from an average
of 368C slows down digestive processes about 2.5-fold (upper regression line, redrawn from Wikelski et al., 1993).
lates the total number of bites per day for iguanas of
various body sizes and islands under each island’s typical environmental temperatures, using the formula:
B[Tb (t)]dt 5 (4.05/c)(T0 2 Tss )(ect 2 1)
1 (4.02Tss 2 56.82)t,
where B is the total number of bites obtained, t is time,
Tb is body temperature, T0 is the initial body temperature (before entering the cold intertidal), c is an empirically determined negative variable that scales the
rate of heat loss to the water and is dependent on the
body mass of iguanas, and Tss is sea surface temperature. To arrive at total food intake per day, the total
number of bites per day is then multiplied by the
amount of food ingested per bite, which differs depending on the height of the algae pasture in the intertidal. These simple calculations, not yet based on
first-principle heat transfer models (Porter et al.,
2000), suggest that environmental temperatures and algae pasture heights are indeed sufficient to explain
body size differences in marine iguanas (Fig. 5; Wikelski and Carbone, 2003; see also Porter and Tracy,
1983; Zimmermann and Tracy, 1989).
Mechanistic regulation of body size and body mass
As our data suggest that foraging performance predicts body size we attempted to further understand the
physiological mechanisms regulating selection on
body size. The Galapagos archipelago offers a natural
experimental situation for selection studies because recurring El Niño events lead to high mortality selection
(Grant, 1986; Snell, 1987; Wikelski and Trillmich,
1997). We found that the reptile-typical glucocorticoid
stress hormone corticosterone (CORT) is elevated once
body condition drops below a critical threshold level,
determined as a significant change in the slope of a
linear regression model (Fig. 6, and unpublished data;
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M. WIKELSKI
AND
FIG. 5. Two environmental parameters, mean standard operative
temperature and mean algae pasture height, predict the maximum
body mass of marine iguanas in the Galapagos archipelago. Isocline
lines indicate maximum body mass in grams. The grey ovals indicate
the range of average values predicted from the measurement of environmental parameters in the field, while the vertical bars show the
range of maximum body masses found in the wild. Generally there
was strong congruence between predicted and real values, however,
the Seymour population had higher than expected maximum body
masses due to inclusion of additional food from land (from Wikelski
and Wrege, 2000). The black area to the left top of the graph identifies the range of environmental conditions when the digestive system of the iguanas can not cope any more with maximum amount
of ingested food, such as when the environmental temperature falls
too much or when the algae pasture height increases too much.
Fig. 6 shows data for Santa Fe only, but iguanas on
five other islands showed the same trends). Glucocorticoids such as CORT are known to have dramatic influences on behavior and physiological systems in all
vertebrates (Romero and Wikelski, 2002a). In general,
the highest levels of CORT were found in animals that
were almost completely emaciated, many of which
died during the strong El Niño of 1997/98 (Fig. 7).
However, not all iguanas in bad body condition had
high CORT levels and we are presently investigating
FIG. 6. Baseline corticosterone (‘stress hormone’) levels, measured
within 3 min of capture, start to increase once the body condition
of marine iguanas drops below a critical threshold level of ;35.
Body condition is here determined as Weight/SVL3 (after Romero
and Wikelski, 2001). Filled circles show animals in low condition,
open circles animals in medium to high condition.
L. M. ROMERO
FIG. 7. Plasma corticosterone levels measured after 15 min of handling stress allow the population-level prediction of annual survival
probabilities. Each data point shows one island population 61 SE
in each direction if available. Vertical arrows indicate that corticosterone levels of marine iguanas on Santa Fe Island before and after
an oil spill that killed about 60% of the population’s iguanas.
whether CORT levels are indeed causally related to
the animals’ death. Some large individuals survived
long-term El Niño conditions while simultaneously
shrinking in body mass and length (Fig. 8; Wikelski
and Thom, 2000). Individuals that shrank between 21
to 60 mm in body length survived on average for 3
years, while individuals that did not shrink or that
slightly grew only survived on average for one more
year. In general, survival probabilities were higher for
individuals that shrank more in body length. Although
we are only beginning to unravel the mechanistic details of shrinkage in body length (unpublished data, T.
Bromage, I. Smolyar and M. Wikelski), we hypothesize that high CORT levels may contribute to the remodeling of body structure, i.e., reversed growth or
resorption of bones. It is so far unclear whether changes in a leptin-like hormone (unpublished data, R. Londraville and M. Wikelski) and/or growth hormone (cf.,
Gerwien and John-Alder, 1992) could be involved in
body length shrinkage.
The increased secretion of CORT is not restricted
FIG. 8. Changes in body size (SVL) of male marine iguanas on
Santa Fe Island between 1981 and 1999. Subsequent measurements
of individuals are connected by lines and only large males .280
mm SVL are shown. Note that body length decreases in several
males during each major El Niño event (1982/83, 1987/88, 1991/
92) as well as during the high-temperature and high population density period of 1993 to 1998.
BODY SIZE
IN
MARINE IGUANAS
381
to large animals that are stressed by El Niño-induced
food shortages. Marine iguanas of all sizes had high
circulating levels of CORT in their blood after a manmade environmental disaster, an oil spill (Fig. 7; Wikelski et al., 2001a). We assume that CORT is causally
involved in supporting organisms during unpredictable
but potentially disastrous events (Wingfield et al.,
1998) such as oils spills. The population of Santa Fe
iguanas affected by the oil spill dramatically declined,
while an unaffected control population with low
CORT levels had no mortalities (Wikelski et al.,
2002). Thus in this case we could use the secretion of
CORT—presumably intended to help the individual
survive—as an indicator of environmental stress on the
population level.
Critical performance measures in marine iguanas:
II) Reproductive performance in females
While foraging performance appears to explain the
limits to maximum body size, it does not predict that
individuals should grow towards large sizes in the first
place. Therefore we hypothesized that reproductive
performance in females increases with body size because large females generally produce larger hatchlings that are better able to survive (Sinervo and Huey,
1990; Sinervo et al., 1992). So far we have not tested
this prediction directly, but obtained supporting circumstantial evidence: First, we found that larger females produced larger clutches with larger eggs (Fig.
9), which in reptiles often produce larger hatchlings
(e.g., Indenbosch, 1998; Angilletta, 1999; Angilletta et
al., 2000). Egg size increases with body size in a stepwise fashion and marine iguana females allocate about
25–30% of their body mass into one clutch every second year (Fig. 9, inset). Females on Genovesa Island
(maximum body mass ;500 grams) produce only one
egg per clutch, while females on Santa Fe produce two
or three eggs per clutch. Large females on Fernandina
Island (;4,000 grams) can produce up to 6 eggs per
clutch (Gus Angermeyer, personal communication).
Second, we found that larger hatchlings survive longer
(Fig. 9, lower panel). An increase in hatchling snoutto-vent length of ;10% increases the average 1st year
survival rate by about 30% (Fig. 9, lower panel). It is
not yet clear whether large male size contributes to
larger sizes of sons or daughters.
Critical performance measures in marine iguanas:
III) Reproductive performance in males
Male marine iguanas have the highest mating success if they can occupy a central display territory (lek)
in a mating aggregation along the shore (Trillmich,
1983; Partecke et al., 2002). However, competition for
such territories is intense and the outcome of fierce
fights is generally determined by body size (Wikelski
et al., 1996). Males therefore have to grow to large
body sizes and only at an age of 12–15 years will they
establish a territory for the first time. Smaller and/or
younger males are relegated to secondary positions in
the lek, or have to roam around territories as satellite
FIG. 9. Clutch mass (top panel) and egg mass (middle panel) increase with female mass, as does clutch size (inset). All females
below 400 grams body mass are from Genovesa Island, the remainder from Santa Fe. The survival of young marine iguanas depends
on their initial size at hatching (lower panel, for Santa Fe iguanas
only). Each data point represents the average survival per mm SVL
for a cohort of 1,285 marine iguanas hatched in 1988 (data courtesy
of T. Dellinger [1991] and F. Trillmich).
males. Even smaller ‘‘sneaker’’ males can mimic female behavior and thus remain within the territories of
larger males, which can not distinguish them from females based on their morphology.
We investigated what aspect of reproductive performance contributes most to mating success in males.
Female marine iguanas choose males based on the persistence of male head-bob display while they patrol
their tiny territories (Wikelski et al., 2001b). The
amount of head-bobbing in turn can be influenced by
the level of circulating testosterone (Fig. 10; Wikelski
et al., 2003). As for foraging performance, we attempted to understand the physiological basis of how individual males adjust their reproductive performance to
the prevailing social environment. Our previous investigations showed that El Niño-related environmental
catastrophes can seriously change the maximum and
average body size within a population of marine iguanas. Some populations may lose as many as 90% of
all males during a strong El Niño event (Romero and
Wikelski, 2002a, b). The remaining small males adjust
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M. WIKELSKI
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L. M. ROMERO
panel). All males that were hormonally forced to
change reproductive performance (sneaker to satellite,
satellite to territorial, territorial to satellite) decreased
their access to females, thus presumably decreased
their fitness (Fig. 10, lower panel). Thus although the
change in reproductive performance was not beneficial
for males in experimental situations, all males nevertheless switched from one phenotype into the other,
consistent with the predictions of Moore (1991) and
colleagues’ (1998) Relative Plasticity Hypothesis. This
implies that hormones are powerful physiological
agents that can constrain behavior pattern of animals
in the wild even when induced socially (Wingfield et
al., 1998).
INTEGRATION
AND
CONCLUSION
Prediction of long-term evolutionary changes in
marine iguana body size
FIG. 10. Natural (shaded bars) and experimental levels (open bars)
of a) testosterone, b) head bob rate, and c) number of females, for
marine iguana males of different reproductive status (sneaker, satellite and territorial). Experimental manipulation included the injection of testosterone (T) in sesame oil (1 ml of 1 mg/ml T) for sneaker
and satellite males, versus the pharmacological blockage of testosterone actions in territorial males (1 ml of sesame oil containing 20
mg/ml aromatase inhibitor 1-4-6 androstatrien-3,17-dione ATD and
16 mg/ml estrogen receptor blocker Flutamide, after Wikelski et al.,
2003). A) Plasma testosterone levels increased after administration
of exogenous hormone in sneakers and satellites, but decreased in
territorial males. B) Sneaker and satellite males started to head-bob
after testosterone injection, while territorial males decreased headbob rate after testosterone blockage. After experimental manipulation, sneaker, satellite and territorial males lost their potential access
to females in their immediate vicinity (females within 1 m radius).
C) Sneaker and satellite males were excluded from access to females
after they started to behave like territorial males. Satellite males
established territories away from mating aggregations. Territorial
males lost their females to neighboring territorial males after T
blockage. Data show mean 6 SE.
their reproductive tactics (Wikelski and Bäurle, 1996)
via social feedback that in turn changes endocrine secretions. Via repeated-measures sampling of the same
individuals we found that males that fight and are defeated increase CORT and decrease testosterone secretions, while males that win fights increase testosterone
levels (Wikelski et al., 2003). In territorial males, testosterone levels then regulate the amount of head-bob
patrolling. If satellite or sneaker males increase testosterone levels, they change their reproductive performances towards the next higher social level, i.e., from
sneaker to satellite or from satellite to territorial male.
We tested the flexibility of behavioral reproductive
phenotypes by implanting either pharmacological testosterone blockers in territorial males, or by administering exogenous testosterone levels (via injection) in
satellite and sneaker males (Fig. 10, upper and middle
Based on our above results we predict that sexual
selection should always push body size towards larger
sizes due to the enhancement of reproductive performance in both males and females (Wikelski et al.,
1997; see also Case, 1976; Case and Schwaner, 1993;
Losos et al., 1997). At the same time, natural selection
should counteract sexual selection on body size due to
a decrease in foraging performance in large individuals
in each population (Arnold and Wade, 1984a, b). Because bite rate is causally dependent upon environmental temperatures in marine iguanas, we predict that
a relaxation of constraints on foraging performance
should result in an overall increase in body size on all
islands. Environmental temperatures have increased
globally and in particular in the Pacific region over the
past century (Parmesan and Yohe, 2003). We therefore
expected that body size of Galapagos marine iguanas
should increase along with global warming trends and
warmer sea surface temperatures. We tested this prediction using specimens collected during the 1905/06
California Academy of Sciences expedition to the Galapagos Islands. We measured the snout-to-vent and
skull lengths of the largest animal per island for extant
populations of marine iguanas and for specimens in
the California Academy of Sciences collection
(VanDenburgh and Slevin, 1913). We assume, based
on notes from the 1905/06 expedition members (personal observation, M. Wikelski), that the collection
contains many of the largest animals found per site.
Similarly, during our population surveys in 2000, we
attempted to capture and measure the largest animal
per site, which is generally a good predictor of the
largest body size per island (Stamps and Andrews,
1992; Gaines and Denny, 1993). The comparison of
body sizes, based on head length measurements (Wikelski and Trillmich, 1997), between 1905/06 and
2000 shows that the maximum body size of marine
iguanas has increased significantly throughout the archipelago (Fig. 11). Although we can not ascertain that
shrinkage in preservation media is completely absent
even for head lengths nor that sampling techniques
BODY SIZE
IN
FIG. 11. Comparison of maximum body sizes of male marine iguanas collected during the California Academy of Sciences expedition
in 1906 (inset picture) and in 1997 (our sampling of the same populations). Each data point indicates the largest animal per sample
for one island. The maximum size in 1997 was significantly larger
than in 1906 as determined by a significant difference in intercept
of the linear regression line from an expected 1:1 line.
were similar during both expeditions, we suggest that
our data are consistent with an environmentally induced increase in maximum size of marine iguanas in
Galapagos over the course of the past century.
Body size in iguanas may have a heritable
component: a common garden experiment in green
iguanas
Unfortunately, we were not allowed to directly conduct a common garden experiment in the Galapagos
because marine iguanas from different populations can
not be brought into captivity at one site. Therefore, we
used the green iguana (Iguana iguana, Burghardt and
Rand, 1992) as a surrogate species in which to test
potential genetic influences on growth rates and body
size (for other iguanids, see Petren and Case, 1997;
Tracy, 1999, 2001). We collected green iguana eggs
from the island of Curacao in the Caribbean, where
green iguanas attain much smaller maximum body size
compared to conspecifics in Panama (Lichtenbelt,
1992, 1993; Lichtenbelt and Albers, 1993; Lichtenbelt
et al., 1993, 1997). We transported the eggs from Curacao to Panama, incubated the eggs in similar environments, and subsequently held Panamanian and Curacao hatchlings under common garden conditions at
the Tupper Research Center of the Smithsonian Tropical Research Institute in Panama City (unpublished
data, M. Wikelski et al.). While Curacao green iguanas
had smaller egg sizes and were smaller than Panama
iguanas at hatch, they caught up with the larger Central
American relatives within 4 months (Fig. 12). However, growth then stalled in Curacao iguanas during
the supposed dry season in Curacao, while Panama
iguanas grew rapidly. After about two years, Panama
iguanas were substantially larger than Curacao iguanas, suggesting that growth and final size has at least
some heritable component when environmental factors
MARINE IGUANAS
383
FIG. 12. Body size in Green iguanas (Iguana iguana) may have a
heritable component, as determined in this common garden experiment using individuals from the Republic of Panama and the Caribbean island of Curacao. We collected eggs at both sites, incubated
them in the same way in Panama, and kept hatchlings under common garden conditions at the Tupper Research Center of the Smithsonian Tropical Research Institute in Panama City for about 2 years.
Data show mean 61 SE for 10 iguanas each. Although the Curacao
iguanas caught up in size with the Panama iguanas by Dec. 2000,
they stopped growing during the expected dry season in Curacao
and only started to grow again in May 2001 (from unpublished data,
Wikelski et al.).
are largely controlled for (Niewiarowski and Roosenburg, 1993; Sugg et al., 1995). However, we do not
yet know whether different populations of green iguanas have different yolk allocations, which could
strongly affect growth rates and final sizes and thus be
part of the mechanism determining body size in each
population. It is interesting to note that green iguana
growth patterns are similar to those found by Tracy,
(1999) in chuckwallas (Sauromalus obesus), although
on a different time scale.
How useful is the ‘‘Performance paradigm’’
We used individual performance tests to identify the
factors that possibly contribute to individual fitness in
the wild, and to exclude factors that are unlikely to be
important for specific traits. We subsequently determined the causal link between the performance factors
and physiological characteristics of individuals, allowing us to tentatively connect the life history characteristics of animals to their mechanistic causation. For
several performance measures we could establish plausible endocrine mechanisms (corticosterone and testosterone secretions) that are possibly linked to the observed individual differences in selective regimens
(Wikelski and Ricklefs, 2001; Ricklefs and Wikelski,
2002). Our data suggest that the performance paradigm
can be expanded to reveal more of the physiological
underpinning of natural selection in the wild. We suggest that measuring morphological, behavioral and in
particular, physiological performance in nature indeed
allows us to predict evolutionary consequences of individual life histories in the wild. We further suggest
384
M. WIKELSKI
AND
that our analysis allows, for example, for the prediction of increased body sizes during the past 100 years
in all Galapagos marine iguana populations. If confirmed by further experimental analysis, such a prediction would lend strong support for the continued
application—and extension into the physiological and
molecular field—of Arnold’s (1983) ‘‘Performance
paradigm.’’
ACKNOWLEDGMENTS
We thank our friends and field assistants for invaluable help. We thank the Galápagos National Park Service, the Charles-Darwin Research Station, Metropolitan touring through the yacht ISABELA II, the Carmabi Foundation and TAME for enabling this work.
E. Ott and S. Layer provided intercontinental communication. Andrew Laurie and Thomas Dellinger
kindly permitted the use of their long-term population
data. Special thanks to Wolfgang Wickler and Ebo
Gwinner, Max-Planck Institute, and Fritz Trillmich for
continuous support. This is contribution no. 771 of the
Charles-Darwin-Foundation and was supported by the
German Science Foundation, the Max Planck Society,
the Humboldt Society, the Smithsonian Tropical Research Institute, the University of Illinois, Tufts University and Princeton University.
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