doi: 10.1111/j.1420-9101.2009.01838.x
Parent–offspring conflict and selection on egg size in turtles
F. J. JANZEN & D. A. WARNER
Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, USA
Keywords:
Abstract
Apalone mutica;
Chelydra serpentina;
Chrysemys picta;
life-history evolution;
offspring size ⁄ number trade-off;
optimal egg size;
optimality theory.
The trade-off between offspring size and number can present a conflict
between parents and their offspring. Because egg size is constrained by clutch
size, the optimal egg size for offspring fitness may not always be equivalent to
that which maximizes parental fitness. We evaluated selection on egg size in
three turtle species (Apalone mutica, Chelydra serpentina and Chrysemys picta) to
determine if optimal egg sizes differ between offspring and their mothers.
Although hatching success was generally greater for larger eggs, the strength
and form of selection varied. In most cases, the egg size that maximized
offspring fitness was greater than that which maximized maternal fitness.
Consistent with optimality theory, mean egg sizes in the populations were
more similar to the egg sizes that maximized maternal fitness, rather than
offspring fitness. These results provide evidence that selection has maximized
maternal fitness to achieve an optimal balance between egg size and number.
Introduction
Offspring size and number are critical components of an
organism’s life history. An individual’s size greatly
influences its performance, growth and survivorship, as
well as the fitness of its parents (Gadgil & Bossert, 1970;
Pianka, 1976; Arnold, 1983; Sinervo, 1990; Wilson et al.,
2005). The offspring size that maximizes offspring fitness,
however, may not be equivalent to that which maximizes parental fitness, because the number of young
produced is also an important component of parental
fitness. Thus, this key trade-off between the amount of
resources devoted to each offspring and the number of
offspring produced has generated considerable theoretical and empirical study (Smith & Fretwell, 1974;
Charnov & Downhower, 1995; Roff, 2002; Uller et al.,
2009). Early models of optimal egg size and clutch size
relationships (referred to hereafter as ‘optimality models’) suggest that parental fitness is maximized by
producing offspring of a uniform size, given a fixed
amount of energy committed to reproduction (Smith &
Fretwell, 1974; Brockelman, 1975; Schaffer & Gadgil,
Correspondence: Fredric J. Janzen, Department of Ecology, Evolution and
Organismal Biology, Iowa State University, Ames, IA 50011, USA.
Tel.: 515 294 4230; fax: 515 294 1337; e-mail: fjanzen@iastate.edu
2222
1975; Wilbur, 1977). As investment per offspring
increases, the number of young that can be produced
decreases, providing some intermediate optimum offspring size generated via stabilizing selection.
Despite the predictions of theoretical models that
offspring size for a given population should be optimized
and therefore remain relatively invariant, considerable
variation in size of young is common in both plants and
animals (reviewed by McGinley et al., 1987). Potential
reasons for this variation include parent–offspring
conflict (Trivers, 1974), intra-family genetic variation
(Temme, 1986; Fischer et al., 2006), competition (Parker
& Begon, 1986), weaker overall selection in variable than
in stable environments (McGinley et al., 1987), paternal
effects (Simmons & Garcı́a-González, 2007) and developmental ⁄ physiological constraints (Congdon & Gibbons,
1987; Bowden et al., 2004; Ji et al., 2006, 2009; Rollinson
& Brooks, 2007). These observations and hypotheses
concerning variation in offspring size require explanation
and experimental evaluation in the light of the fundamental ecological and evolutionary importance of
optimality theory.
Turtles are excellent organisms for investigating the
explanatory power of optimality theory for numerous
reasons (Elgar & Heaphy, 1989; Congdon & Gibbons,
1990). First, investment in offspring is almost completely
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represented by the material deposited in eggs (Packard &
Packard, 1988; but see Iverson, 1990). Second, mass
(hereafter, size) of turtle eggs varies greatly at oviposition
within populations (e.g. Iverson & Smith, 1993). Third,
large eggs produce large hatchlings, which usually have
increased performance (Froese & Burghardt, 1974; Miller
et al., 1987; Janzen et al., 2007) and survivorship (Swingland & Coe, 1979; Janzen, 1993a; Janzen et al., 2000).
Beyond these putative advantages attributed to the
production of large hatchlings, a direct benefit of
producing large eggs has been demonstrated. For example, large eggs of painted turtles (Chrysemys picta) exhibit
greater hatching success than small eggs across a wide
range of incubation environments (Gutzke & Packard,
1985; Packard et al., 1989).
The objective of this study was to investigate how
selection has optimized egg size in natural populations of
three species of broadly-sympatric, but distantly-related,
North American turtles (Apalone mutica, Chelydra serpentina, C. picta). Egg size vs. number trade-offs have been
documented in C. picta (Rowe, 1994) and C. serpentina
(Iverson et al., 1997), and egg size has previously been
shown to impact offspring size, and hence fitness in some
of these and related turtle species (Janzen, 1993a; Janzen
et al., 2000; Paitz et al., 2007; but see Congdon et al.,
1999). Thus, these species provide excellent models for
addressing optimality theory. We specifically address the
following questions: (1) What is the form and strength of
selection on egg size and what is the opportunity for
selection to act on egg size? (2) Is egg size optimized and,
if so, does this optimum vary between mothers and
offspring? (3) How do optimal egg sizes for mothers vs.
offspring differ from actual population mean egg sizes?
Materials and methods
Collection and incubation of eggs
Over 2 years, eggs from three turtle species (A. mutica,
C. serpentina and C. picta) were removed from fresh nests
at geographically proximate collection sites in the upper
Mississippi River drainage in early summer and brought
to the laboratory for incubation (Table 1). All eggs were
weighed upon collection; only fertile eggs were placed in
incubators. Fertile eggs develop a white spot, indicating
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initial formation of extraembryonic membranes (Yntema,
1981). Eggs were assigned to containers with moist
vermiculite at a water potential of )150 kPa. Containers
were rehydrated twice weekly to replace absorbed or
evaporated water and were rotated daily within incubators to mitigate the potential effects of undetected thermal
gradients. Although eggs were incubated under a standardized laboratory environment for other experiments
(Janzen, 1992, 1993b, 1995; Brodie & Janzen, 1996;
Janzen & Morjan, 2002; F.J. Janzen, unpublished), we
used several incubation temperatures (Table 1) that
reflect conditions experienced in natural nests in these
populations (Weisrock & Janzen, 1999; St. Juliana et al.,
2004). Thus, our laboratory incubation introduced some
of the environmental variation that would occur in
natural nests, but these controlled conditions minimized
potentially confounding variables that occur in nature.
Selection on egg size
For each year and species, data on egg size and hatching
success were pooled across incubation temperatures,
because there was no significant effect of incubation
temperature on survivorship (G-test of heterogeneity,
P > 0.05 in all instances). We evaluated fitness as
hatching success of eggs because this measure provides
indices for individual survival (for offspring fitness) and
for the relative level of parental investment that was
successful (for maternal fitness) during a critical lifehistory stage (i.e. embryogenesis). Egg fitness was scored
binarily with unhatched eggs receiving 0 and surviving
eggs being assigned 1. Selection on individual egg size
was determined with logistic regression. Egg survival
(0 or 1) was the dependent variable and egg mass was the
independent variable; prior to analysis, egg mass was
standardized to a mean of zero and unit variance. Logistic
regression coefficients were transformed to obtain selection gradients (Janzen & Stern, 1998). This method
provides selection coefficients (bavggrad) that are interpreted similar to those obtained from linear regression for
analysing directional selection (b) (Lande & Arnold,
1983). Additionally, stabilizing and disruptive selection
(c) on individual egg mass were evaluated with the same
logistic regression technique but using the square of
standardized egg mass as the independent variable.
Table 1 Descriptive information for the turtle clutches used in this study.
Species
Year
Site
Nests
Eggs
Apalone mutica
Chelydra serpentina
1989
1990
1989
Muscatine Co, IA
Muscatine Co, IA
Whiteside Co, IL
6
14
5
56
122
236
Chrysemys picta
1990
1989
Whiteside Co, IL
Carroll Co, IL
20
13
244
147
Incubation
temperature (C)
Mean clutch
mass (g ± SE)
Mean clutch
size (N ± SE)
Mean egg
mass (g ± SE)
28, 30
28, 30
26, 27.5, 28,
28.5, 30
26, 28, 30
26, 28, 30
89.7 ± 12.6
85.6 ± 4.6
493.8 ± 22.3
14.2 ± 1.9
13.1 ± 0.8
45.2 ± 3.0
6.4 ± 0.1
6.6 ± 0.1
11.0 ± 0.1
535.6 ± 50.2
68.3 ± 4.5
45.5 ± 3.8
11.4 ± 0.7
12.0 ± 0.1
6.0 ± 0.1
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F. J. JANZEN AND D. A. WARNER
Absolute fitness of mothers was calculated as the
proportion of successfully hatched eggs in each clutch.
Relative fitness of mothers then is equivalent to an
individual’s absolute fitness over the average number of
successfully hatched eggs per clutch (x = Wi ⁄ W ). By
using the average egg mass for each clutch, clutch egg
mass was standardized to a mean of zero and unit
variance. This standardization facilitated visualization of
the form of selection on egg size by making the mean
equivalent to zero. Simple and polynomial regressions
subsequently were performed to evaluate the variance in
relative fitness of the mothers attributable to linear (b)
and to nonlinear (c) selection on adjusted egg mass
(Lande & Arnold, 1983).
The opportunity for selection and selection differentials
on egg mass were calculated for each turtle species. The
opportunity for selection, which measures the overall
constraint on evolution of egg size imposed by variance
in fitness (Arnold & Wade, 1984a,b), is equivalent to the
variance in relative fitness (I = x(var)). In this case,
relative fitness for each egg is calculated by dividing the
absolute fitness for each individual egg by the mean
absolute fitness (x = W ⁄ W ). The selection differential,
which measures the direct and indirect forces of selection
combined (Arnold & Wade, 1984a,b), was calculated for
egg size as the product of the selection gradient and the
variance in adjusted egg mass (S = br2). Adjusted egg
mass was calculated as the mean initial egg mass
subtracted from the value for each individual egg. To
be comparable among species and years, however,
selection differentials were computed in units of phenotypic standard deviations, yielding standardized selection
differentials (S¢ = S ⁄ rz). These values consequently can
be discussed in terms of the units in which egg size was
measured (g in this case). Finally, the optimal egg size for
offspring of each species was determined by modifying
eqn 11 in Phillips & Arnold (1989): zo = )[c])1b + z. This
formula is equivalent to taking the derivative of
the regression equation, assuming one maximum or
minimum.
Results
Selection on egg size
The strength and form of selection on egg size differed
among years and species (Fig. 1; Table 2). Overall,
selection favoured larger eggs in most cases, despite
intra- and inter-specific variation. For example, the
strength of selection (S¢) on C. serpentina eggs varied
from 0.168 in 1989 to 0.378 in 1990 (Table 2), indicating
that within-generation selection can favour a substantial
increase in egg mass. Chelydra serpentina eggs were subject
to strong directional selection in both years, but those of
Fig. 1 Fitness of eggs as a function of egg mass for three turtle species (Apalone mutica, Chelydra serpentina and Chrysemys picta). Each plot
is the best fit curve predicted from the polynomial regression analyses in Table 2. Egg mass was standardized to a mean of 0 and unit
variance based on pooled data across years; actual mean egg masses (Table 1) can be substituted for 0 on the abscissa. The top row of graphs
represents egg fitness and the bottom row of graphs represents maternal fitness. The solid grey lines represent the mean egg size of the
population for each species. The dashed line represents the optimal egg size for mothers and the arrow represents the optimal egg size for
eggs. The optimal egg sizes for mothers and for eggs are calculated in Table 3.
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Table 2 Selection analyses on egg size through hatching success (i.e. egg fitness) and maternal reproductive success (i.e. maternal fitness).
Selection on egg size through hatching success of individual eggs was evaluated with logistic regression (Janzen & Stern, 1998), and
selection on egg size through maternal fitness was evaluated with linear or polynomial regression (Lande & Arnold, 1983). b = slope of logistic
or linear regression describing directional selection; c = 2 · coefficient from logistic or polynomial regression, describing stabilizing ()) or
disruptive (+) selection; the strength of selection (S¢ = brz) was calculated using b from the regressions; the opportunity for selection (I)
was calculated as w(var) (see Materials and methods section for more details).
Logistic or linear regression
(directional selection)
Logistic or polynomial regression
(stabilizing or disruptive selection)
c
SE
P
S¢
I
0.1356
)0.0463
)0.0533
)0.2430
)0.1289
0.0730
)0.0201
0.2174
)0.3206
)0.4026
0.227
0.069
0.043
0.078
0.255
0.021
0.023
0.095
0.064
0.138
0.231
0.290
0.081
0.137
0.100
0.078
0.837
0.267
0.004
0.175
)0.0425
)0.0789
)0.0647
)0.0229
0.1675
0.3780
0.2815
0.2306
0.2155
0.1834
0.0783
0.2096
0.1643
0.0676
0.2497
0.3131
0.2806
0.1936
0.3636
0.1681
Species
Selection via
Year
b
SE
Apalone
mutica
Egg fitness
Egg fitness
Egg fitness
Maternal fitness
Egg fitness
Egg fitness
Egg fitness
Maternal fitness
Egg fitness
Maternal fitness
1989
1990
Total
Total
1989
1990
Total
Total
1989
Total
0.0709
0.0723
0.0671
)0.0251
0.1695
0.1912
0.1734
0.1343
0.1760
0.1501
0.393
0.072
0.063
0.061
0.051
0.028
0.018
0.088
0.039
0.114
Chelydra
serpentina
Chrysemys
picta
C. picta were subject to both directional and stabilizing
selection in 1989; selection on eggs was similar in
magnitude for both species. Although similar in pattern,
selection on eggs of A. mutica was not statistically significant. The opportunity for selection on egg size also
varied considerably among years and species (Table 2). In
particular, A. mutica had lower variance in relative fitness
than did either C. serpentina or C. picta. Indeed, the
opportunity for selection on egg size of A. mutica in
1989 was less than one-third that for egg size of
C. serpentina in the same year.
The form of selection on egg size through reproductive output of mothers varied among species, as did the
strength of selection (Fig. 1, Table 2). Selection on egg
size through maternal reproductive output was not
significant for any species, but plots of egg mass vs.
maternal fitness hint at disruptive selection for C. serpentina and a stabilizing function for C. picta and
A. mutica (Fig. 1). The strength of selection on egg
investment by mothers in C. serpentina and C. picta was
similar in both magnitude and sign to the strength of
selection on eggs (Table 2). The strength of selection on
P
<
<
<
<
0.088
0.110
0.051
0.685
0.001
0.001
0.001
0.140
0.001
0.213
maternal egg investment in A. mutica was very weak.
The opportunity for selection on mothers also varied
among species (Table 2). Variance in relative fitness of
mothers was more than twice as great for C. serpentina
and C. picta than it was for A. mutica. Further, the
opportunity for selection on mothers in these three
species was roughly half as great as it was for eggs
(Table 2).
Optimal egg size
The optimal egg size for hatching success of eggs and for
maternal fitness differed. Additionally, the optimal egg
size varied among species (Table 3; Fig. 1). The optimal
egg size for mothers was lower than it was for eggs
and was invariably closer to the population mean for
A. mutica and C. picta. Indeed, for both these species, the
per cent difference in optimal egg size for mothers
compared to the population mean was < 2%. In contrast,
the per cent difference between the population mean and
the optimal size for egg fitness ranged from 7% in C. picta
to 18% in A. mutica. Because of strong directional
Table 3 Optimal egg size for hatching success for three turtle species (both years combined). Optimal egg size was calculated through egg
fitness and maternal fitness using a modification of eqn 11 in Phillips & Arnold (1989) (zo = )[c])1b + z). In Chelydra serpentina, the optimal
size for eggs was orders of magnitude larger than the mean egg size due to strong directional selection, and the optimal egg size for maternal
fitness was not calculated because stabilizing selection was not evident.
Optimal egg mass for eggs
Optimal egg mass for mothers
Species
Mean egg
mass (g) of
population
Egg
mass (g)
% difference from
population mean
Egg
mass (g)
% difference from
population mean
Apalone mutica
Chelydra serpentina
Chrysemys picta
6.49
11.36
6.03
7.91
–
6.49
17.9
–
7.1
6.59
–
6.14
1.5
–
1.8
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F. J. JANZEN AND D. A. WARNER
selection on egg size in C. serpentina, the optimal size for
individual eggs was orders of magnitude greater than the
population mean. Because we found no evidence of
stabilizing selection on egg size via maternal fitness, we
could not estimate the egg size that optimizes maternal
fitness in C. serpentina.
Discussion
Most models that explore the potential for parent–
offspring conflict (e.g. battleground models) or the
outcome of such conflicts (e.g. resolution models) have
focused primarily on mammals, birds or social insects, all
of which provide variable levels of parental care to the
offspring (Godfray, 1995). In these organisms, offspring
are capable of actively communicating their needs to the
parents, which can bias the distribution of investment
towards the optimum of the offspring. However, because
of the general lack of parental care in turtles (and in most
reptiles), these organisms provide particularly interesting
(and less complex) subjects for exploring the potential for
parent–offspring conflict and how it is resolved. In
turtles, offspring have no influence over the outcome
of the conflict, whereas the female parent apparently has
complete control over the levels of investment per egg.
Hence, in reptiles where offspring have no influence over
parental care, theory predicts that parent–offspring conflict should be resolved in favour of the parents, such that
the outcome enhances parental fitness (Trivers, 1974;
Stearns, 1976; Godfray, 1995).
Maternal fitness is maximized by a balance between
the number of eggs produced and the amount of
investment per egg. Because mothers have a fixed
amount of energy to invest into clutch production, this
trade-off between egg size and number presents a
challenge to reproducing females. Consistent with optimal egg size theory, we show that the egg size that
maximizes hatching success is not equivalent to the egg
size that optimizes maternal fitness, thereby presenting a
conflict between parents (primarily the mother) and
offspring (support for battleground models). Because the
egg size that maximizes maternal fitness (where it could
be assessed) was more similar to the mean egg size in the
population, our study provides evidence that egg size has
evolved in response to selection primarily on maternal
fitness, rather than offspring fitness (support for resolution models). The parent–offspring conflict documented
here has been resolved mostly in favour of the mother,
thereby supporting a classical assumption of life-history
theory (Stearns, 1976; Godfray, 1995).
Selection on egg size
Selection on egg size through hatching success of eggs
and through maternal reproductive success generally
favoured production of larger eggs. The strength and
form of selection, however, varied among species and
between years. Interestingly, the selection differentials
found here were smaller than those typically found in
other studies (Endler, 1986; Einum & Flemming, 2000;
Kingsolver et al., 2001). One possible explanation for this
difference is that our study presumably evaluated selection on a single character when, in fact, selection also
could have acted directly on a trait correlated with egg
size (Lande & Arnold, 1983). Such an indirect influence
of selection via an unknown, but correlated, trait may
reduce the strength of selection on the variable of interest
(Lande & Arnold, 1983; Mitchell-Olds & Shaw, 1987).
Although linear selection was most commonly observed,
stabilizing selection on egg size also was suggested in
several cases. Moreover, the shape of selection on egg
size in C. serpentina differed depending on whether
selection was quantified through egg fitness or parental
fitness (Fig. 1): larger egg size enhanced hatching success
of individual eggs, but no single egg size maximized
maternal fitness. In fact, the pattern of disruptive
selection for egg size in C. serpentina suggests that clutches
of intermediate-sized eggs may reduce maternal fitness.
In this species, selection may favour maternal investment
strategies that yield large clutch size with small eggs and
vice versa.
Our measurements of reproductive variance (i.e.
opportunity for selection) were low. As with the strength
of selection, opportunity for selection on egg size in
A. mutica was lower than that for C. serpentina and
C. picta. Maternal values of I were approximately half as
great as those for eggs. These results preclude substantial
evolutionary shifts in egg size because the variance in
relative fitness places an upper bound on the evolution of
egg size. The opportunity for selection, nonetheless, did
not constrain selection in this study because it was
greater than the strength of selection in all cases (i.e.
|S¢| << I; Arnold & Wade, 1984a). Thus, the variance in
egg size in this study likely provided a large enough range
for selection to favour the optimal egg size.
Selection for larger egg size has important implications
for the evolution of maternal investment strategies, as
well as nesting behaviours. Both of these maternal factors
have substantial influences on egg and offspring size,
which in turn can impact individual fitness (Packard &
Packard, 1988; Sinervo et al., 1992; Kolbe & Janzen,
2001). Indeed, greater investment into eggs often results
in relatively large offspring with high probabilities of
survival in turtles (Janzen, 1993a; Janzen et al., 2000;
Paitz et al., 2007) and in other organisms (e.g. Sinervo
et al., 1992; Pelayo & Clark, 2003; Wilson et al., 2005). In
addition, nest environments (i.e. moisture and temperature) selected by reproducing females can also influence
hatching success, as well as hatchling body size (Packard
& Packard, 1988; Warner & Andrews, 2002). Consequently, the nest site and its incumbent physical characteristics ought to be chosen carefully by mothers, and
there is some evidence to support this argument in a
variety of reptilian species (e.g. Schwarzkopf & Brooks,
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1987; Plummer & Snell, 1988; Janzen & Morjan, 2001;
Doody et al., 2006). Overall, because parental fitness
functions are extremely sensitive to the rate of offspring
survival (Winkler & Wallin, 1987), any parental effects
that influence this variable should also be under strong
selection.
Optimal egg size
Differential requirements of parental investment
between parents and offspring are expected to lead to
conflict (Trivers, 1974). Trivers envisioned discord
between parents and offspring expressed in a mathematical relationship involving the costs and benefits of
additional parental investment per offspring and the
degree of relatedness among siblings. Assuming all
offspring of a given clutch are full-sibs, which is likely
for most clutches at least in C. picta (Pearse et al., 2002),
then each offspring should try to gain as much maternal
investment as possible until the mother’s cost is twice the
benefit to the offspring (see also Parker & MacNair,
1978). If future offspring are half-sibs, the ceiling of
maternal investment that each current offspring should
seek would rise to four times the mother’s cost (see also
MacNair & Parker, 1978). These relationships imply
considerable conflict between parents and offspring in
the quantity of parental investment per offspring. Indeed,
the results of this study illustrate such a conflict, as the
egg size that maximized maternal fitness does not equal
that which maximizes offspring fitness.
Egg sizes that maximize maternal fitness for two of the
three species of turtles (A. mutica and C. picta) were
strikingly similar to the actual population means for these
species. Despite the similarity between mean egg sizes of
the populations vs. those which maximize maternal
fitness, there is still much variation around the population
means (Fig. 1). This variation suggests that the optimal
egg sizes for each species are not constrained and may
shift in response should selection change. Nevertheless,
the results for A. mutica and C. picta suggest that egg size
maximizes parental fitness rather than offspring fitness,
which supports predictions from a classical assumption of
life-history theory (discussed in Trivers, 1974; Stearns,
1976). These patterns are similar to those seen in a snake
(Naja atra) where the optimal balance between clutch and
egg size is close to the population mean (Ji et al., 2009). For
C. serpentina, however, stabilizing selection on egg size was
not evident, thereby hindering our ability to estimate an
optimal egg size. The lack of such selection on egg size is
unclear as there is no evidence for any constraint on
production of larger eggs in C. serpentina. Perhaps additional components of offspring fitness (e.g. hatchling
survivorship, egg incubation environment) may impart
counterbalancing selection pressures on egg size in C. serpentina (Janzen, 1993a, 1995). Indeed, multiple independent studies of C. serpentina reveal that the importance of
egg size and hatchling size on neonate survival during
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post-hatching migrations to water may vary among years
or sites (Janzen, 1993a; Congdon et al., 1999; Kolbe &
Janzen, 2001). These variable patterns suggest that
stabilizing selection on egg size is not particularly strong
or consistent in C. serpentina, which may explain the lack
of an optimal egg size in this species.
Previous work on egg size and clutch size relationships
suggests that unmodified optimality models may be inapplicable to turtles (Congdon & Tinkle, 1982; Congdon
et al., 1983; Congdon & Gibbons, 1987; Roosenburg &
Dunham, 1997). Egg size in small species of turtles may
be constrained by the width of the pelvic opening which,
in turn, is limited by physical forces operative in
locomotion (Congdon & Gibbons, 1987). This constraint
presumably limits attainment of an optimal egg size in
small females (Beck & Beck, 2005; Rollinson & Brooks,
2007). However, such limitations appear to be of little
concern in this study, because C. serpentina and A. mutica
are large-bodied turtles and because this population of
C. picta is larger-bodied than those examined previously
(minimum plastron length of adult female C. picta in this
study = 151 mm vs. maximum plastron length of adult
female C. picta in other studies = 145 mm) (Congdon
et al., 1983; Congdon & Gibbons, 1987). Importantly,
further evidence suggests that the physical constraint of
the pelvic opening does not exist in northern populations
of C. picta (Iverson & Smith, 1993). Additionally, our
selection analyses suggest that the optimal egg size in
C. picta (as well as in A. mutica and C. serpentina) is below
the maximum size obtained, implying that physical
attributes of the turtles do not constrain the optimal
egg sizes in our study populations. A physiological
constraint on egg size, however, has been demonstrated
in our C. picta population, whereby elevated testosterone
levels in eggs of young mothers may constrain egg size
(Bowden et al., 2004). Such a constraint in young
mothers may result in age-related differences in egg sizes
that maximize maternal fitness. A similar constraint in
C. serpentina may explain the pattern of disruptive selection that we observed in this study; perhaps selection has
favoured smaller eggs from young mothers (due to a preexisting constraint), but also favours larger egg size from
large individuals (in which egg size is not constrained to
the same extent).
Conclusions
Support for the explanatory power of optimality theory
in ectothermic vertebrates has been minimal (Wilbur,
1977; Brodie & Ducey, 1989; Ford & Seigel, 1989; Einum
& Flemming, 2000; Ji et al., 2009). Most work that has
explored variation in ovum size attributes this variation
to differences in reproductive allocation tactics, rather
than to constraints imposed by clutch size (Kaplan, 1980;
Crump, 1984; Meffe, 1987). Indeed, other factors may
influence variation in egg size, such as maternal nutrition
(Kaplan, 1987; Ford & Seigel, 1989; Warner et al., 2007),
ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 2222–2230
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F. J. JANZEN AND D. A. WARNER
traits closely linked to fitness that influence egg size
through counterbalancing selection pressures (Sinervo,
1990; Janzen, 1993a), steroid hormones (Bowden et al.,
2004) or genetic variation among siblings. However,
intra-clutch genetic variation is unlikely to affect egg size
in turtles because eggs essentially are fully yolked at the
time of fertilization (Gist & Jones, 1987). In addition, egg
size in many turtles may be constrained by female body
size or physiology, such that optimality theory would be
inapplicable (Congdon & Tinkle, 1982; Congdon et al.,
1983; Congdon & Gibbons, 1987; Bowden et al., 2004).
Nevertheless, due to the high frequency of stabilizing
selection on egg size in our study population, such
constraints on achieving the optimal egg size may be
minimal.
Overall, our results suggest a conflict between
mothers and offspring as to the optimal quantity of
parental investment per egg. Importantly we also
demonstrate that the optimal egg size for mothers was
closest to the actual population mean egg size. These
findings not only imply the existence of an optimal egg
size but also demonstrate that the conflict between
parents and offspring is resolved by maximizing maternal fitness, rather than offspring fitness. These findings
provide support for a classical assumption of life-history
theory.
Acknowledgments
Thanks to R. Goshien and G.L. Paukstis for assistance in
the field; R. and B. Kraciun for temporary housing of
eggs; and S.J. Arnold, E.D. Brodie III and P.C. Phillips for
statistical advice. E.D. Brodie III, G.L. Paukstis, M.J.
Wade and two anonymous reviewers made helpful
suggestions on the manuscript. Eggs were collected
under permits W-9225 and W-2007 from the Illinois
Department of Conservation and SC 00157 01 and SC
00009 01 from the Iowa Department of Natural
Resources. This project was supported by the University
of Chicago Hinds Fund, a Gaige Fund award, an NIH PreDoctoral Training Grant in Genetics and Regulation (GM07197), an NSF Doctoral Dissertation Improvement grant
(BSR-8914686) and an NSF LTREB grant (DEB-0640932)
to F.J. Janzen.
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Received 17 July 2009; revised 11 August 2009; accepted 17 August
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