THE JOURNAL OF EXPERIMENTALZOOLOGY 270:16-27 (1994)
Sex Ratios of Sea Turtles
N. MROSOVSKY
Departments of Zoology, Psychology and Physiology, University of Bronto,
%-onto, Ontario M5S IAl, Canada
ABSTRACT
Estimates of sex ratios of hatchling sea turtles range from approximately 50%
female (Chelonia mydas and Dermochelys coriacea in Suriname) to approximately 90% female
(Caretta caretta in Florida). Seasonal sex production profiles (SSPPs) show how similar overall
sex ratios can be achieved in dissimilar ways. Possible explanations of the data include sampling
error, constraints on evolutionary adjustment of pivotals o r behavior to local thermal conditions,
and violations of assumptions required by classical Fisherian theory. o 1994 Wiley-Liss, Inc.
WHY STUDY NATURAL SEX RATIOS
ma1 changes, such as transplanting eggs (MrosovHaving the direction of sexual differentiation sky and Yntema, '80). Knowledge of natural sex
determined by the environment (ESD) requires ex- ratios would help in estimating the risks of such
planation at two levels: that of proximate mecha- interventions. And if eggs are harvested for connism and that of adaptive value. For temperature servation through utilization-for instance, for
determination of phenotypic sex (TSD) there are reptile ranches-then one needs t o arrange the
several plausible candidates: temperature depen- take in a way that does not detrimentally affect
dent synthesis or activity of enzymes (Standora sex ratios. The same applies t o the selection of
and Spotila, '85; Desvages and Pieau, '921, heat eggs for protection. In Malaysia, the 30% infertilshock proteins (Harry et al., '901, and tempera- ity of eggs of leatherback turtles (Dermochelys
ture sensitive gene expression (Deeming and coriacea) has been attributed to lack of males in
Ferguson, '89). It is not too difficult to imagine the population. This insufficiency has in turn been
mechanisms. However, it is harder t o think up attributed t o having in the past protected eggs
convincing specific proposals for the adaptive mostly from the warmer, female producing months
of the season (Chan, '91). Thus there are applied
value of TSD in reptiles.
as
well as theoretical reasons for wanting to know
When I started working on TSD, it seemed t o
what
animals themselves are doing with TSD in
me that speculations on its adaptive value would
the
wild.
be better founded if one knew what the animals
themselves were doing with this system. If natuSAMPLING PROBLEMS
ral sex ratios were 1:lnear the time when parenIt sounds like such a simple question, but distal investment ends in species whose male and
female offspring are equally costly, then one might covering natural sex ratios is beset with empiritake that as a confirmation of Fisher's ('30) theory cal and interpretational traps. It is not just that
and not search so hard for special functional sig- one needs to sample in a thermally typical year;
nificance. TSD might just be an alternative t o the one also needs t o know that egg laying occurred
more familiar XY-XX or ZZ-ZW chromosomal at a time of year typical for the species. This latmechanism of going about the matter of balanc- ter point is neglected in most studies. In addiing sex ratios. But if ratios were highly skewed, tion, one must sample fairly in space and in time.
It is also necessary to know what are the limits
that might foster different speculations.
A second reason for wanting t o learn about sex of the breeding population, whether the habitat
ratios in nature is the need for some yardstick is natural, and whether the population is in equiagainst which to assess conservation measures. librium. For these reasons tabulating sex ratios
If global warming strikes, it might become neces- from different studies without reference t o the
sary t o manipulate reptile eggs t o avoid produc- sampling problems is questionable. Such metaing all of one sex. But what proportions should analyses that try to extract consensus from a numone aim for? Also, there are a number of cur- ber of inadequate studies are to be viewed with
rent conservation practices that involve ther- suspicion. The sampling problems, as they apply
0 1994 WILEY-LISS, INC.
SEX RATIOS OF SEA TURTLES
17
POSSIBLE EXPLANATIONS OF
SEX RATIOS
Classic sex ratio theory
When one sees how relatively even sex ratios
can be achieved in different regions by various
combinations of nesting seasons, pivotal levels,
and thermal conditions, it might be natural to take
that as evidence of the power of Fisherian principles. That fairly balanced ratios can occur in a
variety of ways in these reptiles could be taken
as a better way of validating classic sex ratio
DATA ON SEA TURTLE SEX RATIOS
theory
than finding even sex ratios in mammals
Estimates of sex ratio have been obtained by
and
birds.
In those cases it can always be argued
combining information about the number of fethat
results
are the inevitable outcome of sex chromales nesting at different times of the season
mosome
mechanics
(but see Wilson, '75).
(nesting distributions) with the sexing of samples
of hatchlings from different times of the season
Sampling error reconsidered
(Fig. 1).These estimates are presented as seasonal
The data from Florida loggerheads put a n
sex production profiles (SSPPs). This method of
presentation shows not only the overall sex ratio abrupt halt to such speculations. Although the
but also when during the season the different Florida data represent only one out of the four
sexes are produced. This makes it easy to assess, SSPPs in Figure 1, they are the hardest to disor even spot, management options. For example, miss as sampling error. They are based on 3 years
incubation of eggs in Styrofoam boxes became sampling for sex and supported by 5 years of tempopular because it was a simple way of protect- perature monitoring (Fig. 2). The Suriname SSPPs
ing eggs and gave high hatch rates. Unfortunately, and beach temperature recordings are for one seabecause such boxes tend t o be cooler than the son, and the study in GA and SC was not designed
sand, horrendous masculinizing biases can be in- for producing sex ratio estimates and had its share
troduced (Morreale et al., '82; Mrosovsky, '82; of sampling imperfections. Some additional points
Dutton et al., '85; Standora and Spotila, '85). Nev- support the belief that loggerheads in the USA
ertheless, from the SSPPs it can be seen that there are producing highly skewed sex ratios. First,
are times of year when mostly males are being about 90% of the loggerhead nesting along the
produced anyway, such as April for Suriname southeast coast takes place in Florida (Murphy
leatherbacks (Fig. 1). At such times Styrofoam and Hopkins, '84). Even if the more northern nests
boxes could still be a useful conservation option. were producing entirely males, there would still be
Another example of the use of SSPPs is to enable a massive female bias (Mrosovsky and Provancha,
collection of eggs for ranches or other purposes to '89). Second, 68% of juvenile loggerheads caught off
be done in a way that reduces the chances of al- Florida in 1984-1986 were female (Wibbels et al.,
tering sex ratios.
'91). These juveniles would have passed through
SSPPs convey more information than overall their thermosensitive period (during incubation of
ratios. It is interesting t o see how similar ratios the egg) a number of years before the Mrosovsky
can be produced in different ways. The overall sex and Provancha study, 1986-1991. Assuming that
ratios are close t o 1:l for green turtles (Chelonia chances of male or female turtles being caught
mydas) in Suriname and for loggerheads (Caretta are similar when they are immature, the USA was
caretta) in Georgia (GA) and South Carolina (SCj, producing many more female than male loggerbut in the first case females are produced at a heads in years before our sampling in Florida.
relatively steady rate and males with a distinct
Why might loggerheads be producing highly
seasonal peak (corresponding t o the rainy cooler skewed ratios and leatherbacks and green turtles
middle of the nesting season in Suriname (Fig. more balanced ratios? Perhaps this diversity
2). In GA and SC, on the other hand, it is the stems from an unlucky choice of an atypical year
males that are produced at a relatively steady for the work in Suriname. I view this possibility
rate, while the females have a more distinct peak as sufficiently plausible to make it important to
(corresponding to summer warming in the middle continue work there or in other tropical areas. On
of the season in the USA) (Fig. 2).
the other hand, when pivotal and beach temperato particular data sets on reptilian sex ratios in
the wild, have been reviewed elsewhere (Mrosovsky and Provancha, '92) in as much detail (not
enough) as editors could be persuaded to allot to
this essential matter. Lacking more space here, I
will concentrate on the data that colleagues and I
have collected on sea turtles. As discussed in the
original publications, these data are not devoid of
sampling problems, and they illustrate some of
the interpretational questions.
18
N. MROSOVSKY
U
54%$2
Green Turtles Suriname
56%9
--
20
h
,I
"
JFEB
A N MAR APR MAY J U N J U L AUG
Loggerheads SC & GA, U.S.A.
MAY J U N J U L AUG
2
n
M
W
Ln
aJ
4
m
E
L
49% 9
Leatherbacks Suriname
25.
/-.
20:
w
15:
v
rn
10 :
Q,
I
m
z
5
E
I
0
U
JAN
FEB MAR APR MAY J U N J U L AUG
MAY J U N J U L AUG
Figure 1.
SEX RATIOS OF SEA TURTLES
tures are also considered (Fig. 2>,there is a certain consistency to the data. The pivotal level
is the temperature giving 50% of each sex when
eggs are incubated a t constant temperatures
(Mrosovsky and Pieau, '91). I n Florida, beach
temperatures are well above t h e pivotal for
most of the season. On this basis one would expect some males t o be produced at the beginning of
the season and few or none after that-just what
was found by direct sampling for sex ratio. I n
Suriname, more even sex ratios would be expected
because during the months when nesting is frequent, sand temperatures are sometimes below
and sometimes above pivotal. For hawksbill
turtles in Antigua, heavy female biases would not
be expected because mean temperatures appear
t o be mainly below pivotal. However, it would not
be safe to infer that there must necessarily be a
Fig. 1. Seasonal sex production profiles (SSPPs). The
graphs give estimates for month or half-month periods (laying dates on x axis) of the number of each sex produced at
hatching, expressed as a percentage of the total number of
hatchlings produced in the season. Similar areas covered by
male and female SSPPs imply an even overall sex ratio (values given numerically as 9% female). Data on sex ratios for
green and leatherback turtles come from a single year; data
on relative nesting frequency at different times of the season
are means of 11years. The data, methods of sampling, and n
values are given in Schulz ('75) and in Mrosovsky et al. ('84b).
For leatherbacks, 7.4%of the sample of gonads showed little
sign of differentiation at hatching ("indeterminate" category
in Mrosovsky et al., '84b) and have been counted as males on
basis of lack of germinal epithelium (Dutton et al., '85). For
the green turtles, 1.1%were intersexes and have been included with the males. SSPP estimates for loggerhead turtles
in GA and SC come from nesting distribution data for 6 years;
the sex ratio data come from unsystematic sampling over 3
years for other purposes; some of the nests sampled had been
reburied (Mrosovsky et al., '84a). Data for Florida loggerheads
(Mrosovsky and Provancha, '92) are means of SSPPs calculated separately for each of 3 years; it has been assumed that
the few loggerheads nesting in the first half of May produced
all males and the few after the middle of August all females.
For all populations, data were available for the main nesting
seasons (i.e.. estimates would not be greatly altered by a few
uncounted turtles laying outside the study periods or by lack
of sampling for sex ratio at the ends of the season). In addition, not shown in this figure, there are estimates ranging
from approximately 50-75% female for some other populations of sea turtles. Some of these do not present information
on nesting frequency (Rimblot-Baly et al., '87; Maxwell et
al., '881, and some are based on extrapolations from data from
limited parts of the season, o r depend on assumptions about
pivotal levels and incubation duration-temperature relationships (Standora and Spotila, '85; Spotila et al., '87; see also
Benabib, '84, and comments in Mrosovsky and Provancha,
'89, '92).
19
marked male bias there, though this is a possibility Metabolic warming toward the end of the thermosensitive period or brief excursions above
pivotal level might be enough to produce a number of females (Bull, '85). The top of the egg mass
is subject t o greater thermal variation than the
30 and 60 cm depths measured in this study
(Mrosovsky et al., '92).
The variety of relationships between pivotal and
beach temperatures (Fig. 2) suggests that diversity of sex ratios in different populations should
be expected. Of course, the pivotal levels obtained
might also be subject t o sampling error. These are
no more than estimates of population pivotals,
based on incubation of a few clutches in constant
laboratory conditions. There is evidence t h a t
pivotals vary between clutches (Bull et al., '83;
Mrosovsky, '88). However, a t least for the loggerheads in Florida, it seems unlikely t h a t the
population pivotal temperature was much underestimated; otherwise, males should have
been found in more of t h e large number of
clutches from which samples were collected in
the field (Mrosovsky and Provancha, '92). Thus
there is sufficient internal consistency between data
on pivotal levels, beach temperatures, and the actual samples for sex ratio to make it worth at least
pondering explanations other than sampling error
for the diversity of sex ratios in these studies.
No special function: Conservatism in
pivotals and behavior
Perhaps there is no particular adaptive value
to TSD (Bull, '80; Mrosovsky, '80). It might simply be a device that works adequately as a way of
producing some of each sex. In slowly maturing
species, like sea turtles, imbalances in hatchling
sex ratio in thermally atypical years will be
smoothed out by recruits to the breeding population coming from a number of different years.
Moreover, if genetic sex determines the direction
of sexual differentiation of eggs incubated close
t o the pivotal (Zaborski et al., '88) (see also Figs.
3 , 41, then production of almost all females in
a hot year will sow the seed of a corrective
masculinisation in later years. Many of the females produced in the hot year will be genetically males (ZZ in most turtle species). When
they mate with males (ZZ o r ZW), the genetic
makeup of their offspring will predispose the
embryos t o develop into males in years when
temperatures are closer t o pivotal level.
If there is no particular special value in TSD as
a way of producing some of each sex, then the
N. MROSOVSW
20
variety of relationships between pivotal and beach
temperatures might result from pivotal being a
conservative characteristic in turtles. Perhaps consequent biases in sex ratio cannot always be adequately compensated for by changes in behavior
because of constraints on when and where nesting is possible. There might be little variation in
behavior for natural selection t o work on. Bull et
al. ('88) found that individual female leopard geckoes, Eublepharis macularius, did not consistently
choose warm or cool sites for nesting, but these authors rightly cautioned against extrapolatingfrom laboratory studies to field conditions. Stoneburner and
Richardson ('81) reported that loggerhead turtles
crawled up the beach until the temperature rose
abruptly by approximately 2.O"C. The temperatures measured were those of the surface. As soon
as the turtle is a certain distance past the wet
tide-washed area, surface temperature would tend
t o rise. It remains t o be demonstrated that particular temperatures at nest depth are chosen and
whether there are individual differences in such
a choice. Individual leatherback turtles do not consistently travel particular distances up the beach
from the water mark (Eckert, '87). Individual
green turtles do not consistently choose one zone
(such as near the treeline or near the water) of
the beach for nesting (Bjorndal and Bolten, '92).
Possibly natural selection might be able t o exert pressure on how early or late in the year
sea turtles begin their nesting (Mrosovsky and
Provancha, '92). Extensive studies on variability of nesting behavior and its thermal consequences are needed.
Turning t o pivotal temperatures, it is notable
that those available for sea turtles are clustered
close to 29°C (Table 1).The fractions of a degree
Leatherback 8 Green Turtles Suriname
,*-•/
,*
27P
26
MAR
APR
MAY
JUNE JULY
AUG
Loggerhead Turtles Florida U S A .
32,
MAY
JUNE JULY
AUG
SEPT OCT
Hawksbills Antigua
?c)
3L
n
31 -
0
L
'
a,
30-
27t
~
JULY
AUG
SEPT OCT
NOV
Fig. 2. Relationship of pivotal temperatures (horizontal
lines) t o sand temperatures over the main nesting season for
different sea turtle populations. To enhance comparability, all
temperatures are for 60 cm; at this depth variations due to
measures being taken at different times of day are minimized.
This figure is designed t o show, in terms of general trends,
how the average sex ratio of hatchlings would be expected t o
vary over the season and between different beaches. The two
points above the month labels are temperature means for halfmonth bins and are for typical nesting sites. Of course, sex
ratios of particular clutches will have different ratios because
of variation in ambient temperature and in pivotals. For green
and leatherback turtles, mean of " s a n d and "border" areas
is shown (Mrosovsky et al., '84b); the solid line (L) represents pivotal level for leatherbacks from Rimblot-Baly et al.
(W),the dashed line (Gj pivotal for green turtles from
Mrosovsky et al. ('84b). For loggerhead turtles, data collected
over 5 years are shown for "mid-beach sites (Mrosovsky and
Provancha, '92). Data for hawksbills are for 2 years for
"shaded sites. Loggerheads and hawksbills do not typically
nest as deep as 60 cm, but values for 30 cm were usually
within approximately 0.5"C of the 60 cm values (Mrosovsky
and Provancha, '92; Mrosovsky et al., '92). Generally similar
data on 60 cm depth temperatures in French Guiana are in
Rimblot-Baly et al. ('87).
21
SEX RATIOS OF SEA TURTLES
-TRT-
Im
If
Fig. 3. Diagram of transitional range of temperature (TRT) and pivotal temperatures
(vertical dashed lines) for a turtle species with ZZ males and ZW females. P1, P2, and P3
represent the pivotals that might be expected from WW, ZW, and ZZ samples; l,, shows the
limit below which 100%of the embryos are masculinized, lf the limit above which 100% of
the embryos are feminized (from Mrosovsky and Pieau, '91).
in Table 1 should not be taken too seriously in
comparing studies using different conditions and
ways of measuring temperature. For instance, the
greater temperature variation in some studies
(e.g., Limpus et al., '85) might have resulted in
more females being produced. For freshwater
turtles, Bull ('85) has shown that even when mean
temperature is the same, increased variation
around this mean increases the number of females; the effect may arise because more developmental time occurs when thermal excursions are
above rather than below the mean, and therefore
there is more development at female producing temperatures, even though the mean temperature may
be at pivotal (Pieau, '82). We are at the limits of
affordable current technology for specifying pivotals. Inevitably there is some thermal variation
within incubators, and it is not feasible to record
the temperature of each egg. But the results are
sufficient to show that pivotals do not vary greatly
among sea turtles.
If a particular sex ratio were an evolutionarily
stable strategy (ESS), then one would expect pivotal and beach temperatures t o be related in a
way that would produce similar sex ratios for
populations of turtles nesting in thermally different places or times (cf. Blackmore and Charnov,
'89). It was partly to look for such adaptive relationships that the study of hawksbill turtles,
Eretmochelys imbricata, was undertaken. Hawksbills commonly nest high on the beach in the
shade, and it had been thought that they might
have a low pivotal temperature. This proved not
t o be the case, even though beach temperatures
were lower than those of other populations shown
in Figure 2. In studies in which pivotal levels from
different parts of the range of a reptilian species
have been compared, little difference has been
found (review in Mrosovsky, '88; Ewert and
Nelson, '91; but see Ewert et al., this issue, for
some new data).
The closest indication of some modification in
the pivotal temperature in sea turtles is perhaps the somewhat higher value for leatherbacks (29.5"C) in the Guianas compared with
that of green turtles (28.8'C) nesting on the
same beach. Since relatively more leatherbacks
nest when it has begun t o warm up after the
rainy season, their higher pivotal makes their
overall sex ratio more similar t o that of green
turtles than it would have been if both species
had the same pivotal. However, although a n estimate of green turtle pivotal for Suriname was
obtained, unfortunately data delimiting the full
transitional range of temperature were lacking.
Sex ratios are not dependent just on pivotal,
but on the shape of curve within the range of
where temperature exerts effects on sex (transitional range of temperature = TRT, Fig. 3) and
on how rapidly the curves approach the 100%
female and 100% male asymptotes at either end
of this range. The effects of a lower pivotal in
greens might be counteracted by slowness t o
asymptote to 0% female at the lower end of the
N. MROSOVSKY
had in mind was the nutritional condition of the
mother of an ungulate. If the mother was well
nourished, her offspring would be large. This
might benefit a male more because by fighting off
other males he would be able to mate with more
females. If the mother was in poor condition, capable only of producing a small, weak calf, then
it might be better t o allocate her resources to a
female which might produce at least some offspring, while a weak male might be excluded from
breeding
altogether. The critical points are that
0
maternal condition predicts the condition and later
25
.;
28.0 28.5 29.0 29.5 30.0 30.5
reproductive success of the offspring and that maternal
condition has differential effects on male
EGG INCUBATION TEMPERATURE OC
and female fitness (Fig. 5).
This argument has been extended by Charnov
and Bull ('77) t o explain environmental effects occurring after the mother is out of the picture. Provided that the environment affects male and
female fitness differentially, then selective pressures arise for controI of sex ratio. By implication, and stated explicitly later, ESD may be
favoured "because it enables the embryo t o control its sex in response t o the environment" (Bull,
'81j. Trivers and Willard ('73) also envisaged that
the control of sex ratio was postponed until after
the combination of XX and XY chromosomes at
conception. This type of condition-dependent se' 48 50 52 54 ' 56 ' 58 ' 60 ' 62
lective pressure may therefore be called Triversian
49 51 53 55 57 59
61 63
for
short, t o contrast it t o the more familiar
INCUBATION DURATION (DAYS)
Fisherian frequency-dependent selective pressures
Fig. 4. Sex ratio of two clutches (F and G) of loggerhead (frequency of the two sexes in the population),
turtle eggs incubated in alternate positions in the same incuCould such Triversian selection apply to TSD
bators (Mrosovsky, '88). Data are plotted as a function of inin
turtles? It is not necessary that temperature
cubation temperature (top) and duration (bottom). Numbers
beside points are n values; some turtles in the top graph did itself directly influence survival of male and fenot hatch but were sexed as embryos. Temperatures are those male embryos differently, so long as incubation
of incubators. Because sex ratio is extremely sensitive to tem- temperature is correlated with different fitness for
perature in this range, it should be asked whether some un- males and females later on. Conceivably, incubaknown factor, such as different eggshell thickness affecting
the amount of evaporative cooling, could have led to differ- tion temperature correlates with subsequent
ent temperatures within the eggs of one clutch. Incubation growth which in turn correlates with adult size
duration is an index of temperature. At each incubator tem- and fitness (Ferguson and Joanen, '82; Deeming
perature the mean incubation durations of the two clutches and Ferguson, '89). It should be noted that if such
were <1day apart. Moreover, even for given durations, the types of differential growth are important, they
two clutches had different sex ratios, suggesting a genetic
would provide plausible explanations not only of
component to pivotals.
TSD, but also of skewed sex ratios (should those
be substantiated). This is because with a situaTRT. Therefore, further study of this case is tion such as that diagrammed in Figure 5, the
needed.
average fitness of one of the sexes is higher than
the average fitness of the other sex. Since both
Condition-dependentfactors
sexes contribute equally to the next generation,
Trivers and Willard ('73j realized that selective for the average fitness to differ between the sexes
pressures to produce more of one sex might arise there must be different numbers of the two sexes.
if the environment affected the fitness of males The sex with the lower average fitness (i.e., the
and females differentially The environment they sex that is produced in the poorer condition) must
1
I
I
1
23
SEX RATIOS OF SEA TURTLES
TABLE 1. Pivotal temperatures o f sea turtles'
Species (country)
Leatherback
Suriname
Green
Suriname
Costa Rica
Hawksbill
Antigua
Olive ridley
Costa Rica
Loggerhead
USA
USA
Australia
S. Africa
Pivotal ("C)
Reference
Rimblot-Baly et al. ('87)
29.5
Mrosovsky et al. ('84b)
Standora and Spotila ('85)
28.8
28.0-30.32
Mrosovsky et al. ('92)
29.2
approximately 303
McCoy et al. ('83)
approximately 304
29.0~
28.6
29.'i5
Yntema and Mrosovsky ('82)
Mrosovsky ('88)
Limpus et al. ('85)
Maxwell ('87)
'Methods of measuring temperature, constancy of incubators, moisture, and number of temperatures tested (i.e., resolution) vaned
between studies.
'Estimated from field studies.
3Sexing by gross morphology, not validated against histology (for comments see Whitmore et al., '851.
4The earlier estimate of a 30°C pivotal for USA loggerheads has been revised down to 29"C, partly because of better resolution in temperature and partly because of introducing a 0.5"C correction factor to reflect the finding that the eggs in a moist substrate tend to be cooler than
the incubator.
'This is higher than the 27.0-293°C estimated from field studies for this population (Maxwell et al., '88).
be more abundant (Frank and Swingland, ,881.
Nevertheless, the existence of extreme sex ratio
biases would remain a problem because conditiondependent selection does not operate in isolation
from frequency-dependent selection (Fig. 5 ) . The
more extreme the skew, the stronger will be the
counteracting Fisherian pressures, and therefore,
it has been argued, large imbalances would be unlikely t o be stable (Bull and Charnov, '88).
However, there is another factor that should affect sex ratios: the abundance of various kinds of
conditions (environments/patches). If environments in which one sex is fitter are more common, then there will be a tendency for sex ratios
t o be skewed in that direction. If the environment
in which one sex is fitter is not only very common, but also is one in which fitness for both sexes
is very low, then large biases could develop and
be stable. Most of the offspring from the poor environments might never reproduce, and those that
were able t o might owe this to being the fitter
sex in that environment. Quantitative treatment
is provided by Bull ('81). Therefore, it is possible
in theory that combinations of Triversian pressures and patch frequency could result in highly
skewed sex ratios being stable.
The problem with this conjecture is that when
one moves from the armchair t o the field, these
factors are not obvious. Powerful condition-dependent factors for turtles remain t o be demonstrated.
For slowly maturing species it is hard t o see how
Male
m
m
cu
c
%
Lr.
A
allocation switch point
between female and male
Condition
e.g., nutrition
? temperature
Fig. 5 . Diagram showing gender-different changes in fitness (solid lines) as the condition of the offspring changes (after Bull, '81). For reptiles, incubation temperature or some
correlate might be the relevant condition, but how temperature has such gender-specific effects is not understood. When
the fitness of one sex exceeds that of the other, the allocation
of resources for reproduction should switch between these sexes
(a). For reptiles, the switch point should approximate the pivotal temperature. Density-dependent Fisherian factors still operate; therefore, the switch point should shift to b if males
become abundant, because the fitness of males will be lowered
(dashed line). The shapes of the fitness functions influence the
extent of such shifts. For example, if the fitness of males increases steeply at low temperatures, surplus males in the population should not shift the switch point as much as if the fitness
of males increases gradually.
24
N. MROSOVSKY
temperature during a short period in the middle
of incubation would correlate with some factor
that years later made one sex fitter than another,
especially considering the variety of patterns in
different reptiles relating sex ratio t o temperature
(Ewert and Nelson, '91). In sexually dimorphic
species, being large presumably benefits one sex
more. However, the correlation between the presence of TSD and sexual dimorphism in reptiles is
not compelling; and whether high temperatures
produce males or females does not seem to be
linked t o which sex is the larger as an adult
(Janzen and Paukstis, '91b; see also Ewert et al.,
this issue). Even within crocodilians, data are not
consistent on what kind of start in life is associated with different incubation temperatures. In
Crocody Zus johnstoni, warm temperature incubation results in hatchlings that are lighter but have
more yolk (Whitehead et al., ,901, whereas in AZZigutor mississippiensis, lighter hatchlings come from
intermediate temperatures (Joanen et al., '87).
be relegated to poorer patches to move into the
better ones. When the population is abundant,
then good patches will be fully occupied, and other
turtles will have to adopt the best of a bad situation tactic (BBS) (see Gross, '84). When population levels fall, tendencies to occupy the better
patches will be able t o express themselves in more
individuals. If the species had a TSD mechanism,
perhaps t o accommodate some condition-dependent factor, then its sex ratio could become skewed
in the disequilibrium state, even if the Triversian
factors were not very powerful in themselves.
In a world so much altered by people, there is a
real possibility that populations under study are
not in equilibrium. Harvesting, alteration of the
relative frequency of different patch types, and
the beginning of global warming-near t o pivotal
levels even a fraction of a degree C could alter
sex ratios-are potential causes of disequilibrium.
All this makes it extremely hard to bring data on
sex ratios t o bear on sex ratio theory When a
skewed ratio is found, is that a temporary deparOther Fisherian assumptions not met
ture from a Fisherian situation or a manifestation
Absence of differential condition-dependent ef- of an ESS under some other set of circumstances?
fects on fitness of the sexes is just one of a numEVALUATION AND SUMlMARY
ber of assumptions underlying Fisherian theory
The main conclusion is that we are far from firm
(Bull and Charnov, '88). For instance, if siblings
influence each other's fitness either by competing conclusions in this field, or should one say bog.
for mates or by helping each other, then the Figure 6 diagrams relationships between differFisherian assumption of random mating is not ent categories of uncertainty. A few general points
met. Within a season green sea turtles have high may nevertheless be in order.
This paper has focussed on possible explananest-site fidelity for a particular stretch of beach
(e.g., Bosc and Le Gall, '86). If females also re- tions for the data on sex ratios rather than on exturn to the stretch of their natal beach where they planations for the existence of TSD, although the
hatched, there would be opportunities for inter- two are interrelated (for speculations on the adapactions between siblings (Mrosovsky, '80). How- tive value of TSD see Bull, '80, '81; Mrosovsky, '80;
ever, without more information, speculations about Deeming and Ferguson, '89; Ewert and Nelson,
'91; Janzen and Paukstis, '91a,b; Korpelainen, '90).
non-random mating are tenuous.
Again one needs t o distinguish between expla- The phylogenetic inertia explanation for the exnations of TSD and of skewed sex ratio. Sex ratio istence of TSD seems less attractive now that it
skews on account of non-random mating can oc- is known that different species within a family
cur in animals whose sex is determined by sex can exhibit either TSD or GSD (Ewert and Nelson,
chromosomes (e.g., competition for resources be- '91; Janzen and Paukstis, '91a).
On the other hand, the sex ratios resulting
tween sedentary females is associated with male
from TSD do appear t o be subject t o constraints.
biased sex ratios in prosimians) (Clark, '78).
In sea turtles, the combination of relatively
Disequilibrium states
similar pivotals, nest site, and nest season fixOne major reason for being open-minded about ity seem t o dictate overall sex ratios in a given
explanations of sex ratio data is that usually we year and the way the overall values are achieved,
do not know whether the populations studied are the SSPPs. Doubtless imaginative scenarios
in an equilibrium state. If a population is severely could be devised for why in midseason loggerdepleted, then patches that produce the fittest heads should produce females, and greens
turtles may not be fully occupied, and there will males, but I view these more as consequences
be opportunities for turtles that would otherwise rather than reasons for TSD. One might think
25
SEX RATIOS OF SEA TURTLES
Sampling
error
I
I
Valid
sample
Some possible
explanations
I
I
I‘hermally atypical
nesting season
I
Balanced
ratio
Equilibrium with Fisherian frequency-dependent factors dominant
Disequilibrium of Triversian situation
Atypical nesting
times within season
I
I
I
I
I
Beach
unrepresentative
of larger
breeding unit
I
I
I
I
I
Disequilibrium of Fisherian situation
Skewed
ratio
Equilibrium with Triversian condition-dependent factors dominant
Other Fisherian assumptions (e.g.,
random mating) not met
Evolutionary inertia, non-adaptive
Fig. 6. Simplified diagram of uncertainty domain (within box) for results of studies on
sex ratio and some possible explanations of results based on valid samples. Combinations
of the different results and explanations are possible. Fair spatial and temporal sampling
within a season are omitted because with sea turtles the large tracks make it easy to locate
nearly all the nests and sample accordingly The text argues that it may be premature t o
devote too much thought to the explanations before it is known where the results should be
placed within the box.
that TSD would liberate species t o perform all
sorts of clever manoeuvres with their sex ratios. Instead it seems t o have subjugated them
to the vagaries of the weather, with the greenhouse effect ominously on the horizon.
Suppose that long enough sampling periods (?
decades) were used t o average out these thermal
vagaries. If skewed equilibrium sex ratios were
found, then they might encourage explanations of
TSD in terms of condition-dependent effects on
male and female fitness, or non-random structure
of mating groups, or some other violations of the
assumptions of Fisherian theory If skews were
extreme, then for whatever reason those skews
might be desirable, or even if skews were only
temporary responses t o transient conditions
rather than being ESSs, it would suggest an additional function of TSD: t o provide a mechanism
for producing extreme skews. Korpelainen (’90)
concluded that “adaptive sex ratio variation is con-
siderably easier for organisms with ESD, and this
feature is the ultimate cause for the evolution and
maintenance of ESD.” Mrosovsky (’80) suggested
that TSD “would allow turtles greater scope in
varying sex ratio than if they were constrained
by a heteromorphic chromosome system.” Why
turtles might need such scope remains a mystery
ACKNOWLEDGMENTS
Many people, acknowledged by name in my
empirical papers, participated in these studies
or contributed in some way. I am fortunate t o
have had so much valuable help. Support came
from the Natural Sciences and Engineering Research Council of Canada. I thank M.R. Gross
for comments.
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