Download Alternative Concepts of Reproductive Effort, Costs of Reproduction

AMER. ZOOL., 23:25-34 (1983)
Alternative Concepts of Reproductive Effort,
Costs of Reproduction, and Selection in
Life-History Evolution1
JUHA TUOMI
Department of Biology, University of Turku,
SF-20500 Turku 50, Finland
TUOMO HAKALA
Department of Biomedicine, University of Turku,
SF-20500 Turku 50, Finland
AND
ERKKI H A U K I O J A
Department of Biology, University of Turku,
SF-20500 Turku 50, Finland
SYNOPSIS. An outline for an organismic theory of reproductive tactics is presented to
develop the demographic theory of optimal reproductive tactics into a more realistic theory
of life-history evolution. Reproductive effort—denned as the proportion of resources
invested in reproduction—and the costs in somatic investment do not automatically result
in survival costs. Both the conditions where survival costs are produced and the conditions
where reproduction can take place without survival costs are specified. Compensation and
threshold hypotheses are put forward to allow weaker correlations between reproduction
and survival than the trade-off hypothesis, which assumes direct impacts by reproductive
effort on survival. Furthermore, reproductive tactics are unlikely to be moulded by the
demographic forces of selection only. An empirical example is shown where residual
reproductive value played no significant role in the evolution of reproductive tactics.
Selection probably operates not on separate life-history traits but on whole organisms
through their entire life-history. The structural and physiological intercouplings between
separate traits can result in phenotypic opportunity sets where selection can mould lifehistory traits only within the constraints of the opportunity sets. Optimization theory has
provided an efficient technique for modelling and making predictions. However, organismic selection does not necessarily optimize adaptive strategies but eliminates unfit strategies. Life-history theory, and evolutionary theory in general, can be developed along
alternative logical lines when different hypotheses are generated on how selection operates.
INTRODUCTION
optimized by maximizing fitness under the
The demographic theory of optimal re- P u r e l y demographic forces of selection,
productive tactics, first postulated by WilAlthough demographic theory is logiliams (1966a, b), is based on three basic c a l l y s o u n d > a n d several predictions have
ideas—reproductive effort, costs of repro- b e e n derived for empirical tests, its asduction, and selection as a process of de- sumptions may be violated on several critmographic optimization. Demographic >cal points, where alternative logical paths
theory has been formulated by assuming diverge. Assumptions other than those
that reproductive effort entails a fixed conventionally made can lead to different
trade-off between current and future re- predictions. Therefore, demographic theproductive success, and that reproductive ory represents only a specific line of reaeffort, and life-history traits in general, are soning and a specific approach to life-history evolution.
This paper outlines several alternatives
in
relation to reproductive effort, costs of
1
From the Symposium on The inter-face of Life-His- reproduction, and selection. Restrictions
tory Evolution, whole-Organism Ontogeny and Quantita-
',
,
r
•
u
•
,
tive Genetics presented at the Annual Meeting of the a n d w e a k P a r t s o f demographic theory are
American Society of Zoologists, 27-30 December also pointed out. T h e possibilities not COn1981, at Dallas, Texas.
ventionally taken into account are sum25
26
TUOMI ET AL.
• '•
B1
i
I
•
B3
FIG. 1. The same absolute investments in reproducB2systems where
tion (Ir) produced by four allocation
somatic investments of reproductive individuals (I,)
vary in relation to the standard level of somatic investments of nonreproductive individuals (In). The
resources for reproduction can be produced at the
expense of somatic investments (A) or by increasing
resource input (Bl and B2) or by both means (B3).
marized as a preliminary outline for an organismic theory of reproductive tactics.
REPRODUCTIVE EFFORT
Reproductive effort (E) was introduced
as a measure of both the fraction of resources invested in reproduction and the
costs of reproduction in somatic investments. This definition implied a direct
trade-off: an increase in reproductive effort increases current reproductive output
at the expense of survival due to reduced
somatic investment (Williams, 1966a, b;
Gadgil and Bossert, 1970).
This definition of reproductive effort can
be used properly only when resources are
invested in reproduction at the same rate
that reproduction drains resources from
somatic investment. This concept loses accuracy if resources are invested in reproduction at a different rate than they are
drained from somatic investment. Resources could be invested in reproduction
only partially at the expense of somatic
investment, and perhaps at no expense to
somatic investment in certain cases.
Several definitions and indices of reproductive effort have been suggested (Hirshfield and Tinkle, 1975; Leon, 1976; Randolph et al., 1977; Haukioja and Hakala,
1978; Calow, 1979). The problem is that
demographic theory is based on a definition logically different from that of most
empirical studies. Furthermore, the conventional definition (E) of reproductive effort is an adequate measure only in one
allocation system.
Allocation systems
Reproductive effort is always defined in
relative terms, but the definitions can be
treated best after the parameters dictating
resource partitioning have been defined in
absolute terms.The somatic investment of
nonreproductive individuals (In) can be
taken as the standard against which other
investments are compared. The total
investment (Ia) of reproductive individuals
consists of somatic investment (Is) and
reproductive investment (Ir)
I. = I. + IrThe absolute costs to somatic investment
caused by reproduction are given by
RS = In - I,
and the absolute amount of resources produced by differences in resource input between reproductive and nonreproductive
individuals is given by
Ra = la - InThe inconsistencies between definitions of
reproductive effort are due to the fact that
the same absolute investment in reproduction can be produced by different systems
of allocation (Fig. 1). (We ignore the costs
of resource processing.):
A.
B.
Both reproductive and nonreproductive individuals have equal resources
available for investment (Ia = In). Then
all resources invested in reproduction
are produced at the cost of somatic
investment, and Ir = Rs and Ra = 0.
The total amount of resources avail-
27
ALTERNATIVE CONCEPTS IN LIFE-HISTORY EVOLUTION
able for the investment of reproductive individuals exceeds the level of
nonreproductive individuals (Ia > In).
Bl. All resources produced by the increased resource input are invested in
reproduction and there are no costs
to somatic investment (Is = In). Then
Ir = Ra and Rs = 0.
B2. There are no costs to somatic investment and only part of the resources
produced by the increased resource
input is invested in reproduction (Is >
In). Then Ra > Ir > 0 and Rs < 0.
B3. All resources produced by the increased resource input are invested in
reproduction and there are costs to
somatic investment (Is < In). Then Ir
= Rs + Ra where Rs > 0 and Ra > 0.
Here Ir, Rs, and Ra are the basic parameters
of reproduction which describe various aspects of resource investment in absolute
terms. A satisfactory theory of reproduction must be able to treat all such systems
of allocation, in both absolute and relative
terms. For this purpose, either a definition
of reproductive effort must be found which
is accurate in all allocation systems, or the
concept of reproductive effort must be defined separately for each allocation system.
Definitions and their limitations
The meaning of the term "reproductive
effort" varies depending on the components of resource investment included in
the definition. Here we consider some definitions which are based on the absolute
basic parameters mentioned above:
RE = I r /I.
RES = (In -
In = R s /I n
and
REa = (I. - I n )/I, = R./I,.
Given specific allocation systems, other alternatives exist:
E = I r /I. = R s /I n
and
RE, = I r /I, = R./I,.
The first specific definition (E) refers to
allocation system A. Here RE = RES and E
TABLE 1. Alternative definitions of reproductive effort (E,
/?£„ and RE) and allocation systems (Fig. I). *
Allocation systems
A
E; RE = RE,
RE,; RE = RE,
RE
RE,
RE,
Bl
B2
B3
+
+
+
+
+
0
+
0
+
+
+
* The relative costs in somatic investment (RE,) and
the proportion of resources produced by the increased resource input (REa) are also shown. The values of RE, can vary from positive to negative depending on the allocation systems.
+
+
equals both the proportion of resources
invested in reproduction and the costs to
somatic investment. This definition can be
used only if Ia = In and Ir = Rs. RE and RES
can be denoted by E in allocation system
A but not in Bl, B2, and B3. The second
specific definition (RE,) is reproductive effort defined for allocation system B1 where
RE = REa, Is = In, and Ir = Ra. Here RE,
equals both the fraction of resources invested in reproduction and the proportion
that increased resource input forms of the
total investment of reproductive individuals. Although there is no need to define
RE and REa separately in allocation system
Bl, they must be kept separate in both B2
and B3. Consequently, E and RE; are very
limited definitions of reproductive effort
for allocation systems A and Bl respectively (Table 1).
RE is the best candidate for the general
definition of reproductive effort, because
it can be used in all allocation systems (Table 1). However, RE indicates only the fraction of resources invested in reproduction.
It does not necessarily imply any trade-off
between reproduction and somatic investment. If RE is taken as the standard definition of reproductive effort, theories of
reproductive tactics could operate in all allocation systems, but then reproductive effort is a purely descriptive concept which
does not specify the sources of the resources invested in reproduction. The resources can be produced at the cost of somatic resources a n d / o r by increasing
resource input during reproduction.
RES (the stress of reproduction; somatic
28
TUOMI ET AL.
costs) measures the costs to somatic investment. It indicates the proportion of resources invested in reproduction only in
allocation system A. Allocation system B2
is a special case where RES is negative and
reproductive individuals invest more resources in somatic investment than do nonreproductive individuals.
REa (resource increment) indicates the
proportion of increased resource input
from the total investment of reproductive
individuals. It does not generally measure
the proportion of resources invested in reproduction, excluding allocation system B1,
or the costs to somatic investment.
The distinction among RE, RES, and REa
suggests a revision of our view of resource
allocation. Demographic theory has operated with the special definition (E) of reproductive effort limited to allocation system A. Since this special definition cannot
be used in all allocation systems, the original concept should be replaced by RE.
However, reproductive effort as given by
RE is not necessarily a biologically useful
quantity because offspring production may
not be restricted by the values of RE as
such, but by the causal mechanisms producing resources for reproduction. In such
cases, offspring production depends on
both (a) the resources invested in reproduction at the cost of somatic investment
and (b) the resources which can be made
available for reproduction by increasing
resource input. Therefore, RES and REa
may be biologically more important quantities than reproductive effort (RE).
COSTS OF REPRODUCTION
The demographic theory of optimal reproductive tactics is based on the idea of a
trade-off as implied by allocation system A.
This hypothesis (Williams, 19666) can be
summarized as three postulates:
(1) When both reproductive and nonreproductive individuals have the same
limited amount of resources available
for investment, an increase in reproductive effort inevitably results in both
an increase in current reproductive
output and a reduction in somatic investment ("somatic costs").
(2) When reproduction takes place at the
expense of somatic investment, the somatic costs reduce the probability of
surviving to the next breeding season
("survival costs") and/or reduce future reproductive output ("fecundity
costs").
(3) When reproduction results in survival
and/or fecundity costs, there is a tradeoff between current reproductive output and residual reproductive value.
However, the postulates of the trade-off
hypothesis do not necessarily hold in allocation systems other than A. First, increased resource input can uncouple somatic costs from the direct influences of
reproductive effort. Reproduction can take
place only partially or not at all at the expense of somatic investment. Second, reproductive individuals can adapt to resist
somatic costs, within specific limits, without any survival costs. Thus reproduction
need not automatically result in survival
costs, although survival and fecundity costs
can be indirect results of reproduction in
critical environmental conditions. (Fecundity costs are neglected below.)
Somatic costs: compensation hypothesis
The stress of reproduction defined as
RES = (In - I5)/In = (In - I. + I r )/I n
measures the somatic costs of reproduction
by the extent to which reproduction reduces the somatic investment of reproductive individuals below the standard level of
nonreproductive ones living in the same
environmental conditions. As with the
trade-off hypothesis, reproductive effort
(RE) equals RES when resource availability
is the same for the investment of both reproductive and nonreproductive individuals. Then In = L,, RES = I r /I a = RE, and
RE always results in corresponding somatic
costs as indicated by RES.
But the situation is fundamentally different when reproductive individuals can
increase their Ia above the level of nonreproductive individuals (In). The increased
resource input (or some part of it) can be
invested in either reproduction or compensation for the somatic costs caused by
ALTERNATIVE CONCEPTS IN LIFE-HISTORY EVOLUTION
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UJ
o
<
o
/
R
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29
REPRODUCTION
i
Fie. 2. The absolute investments in reproduction
(Ir) produced by the increment (Ra) in resource input
and by the reduction (R,) in somatic resources. The
weight of nonreproductive individuals (Wn) is assumed to remain constant while the somatic weight
of reproductive individuals (Wr) fluctuates in time due
to reproduction.
reproduction. In both cases, increased resource input results in a reduction of RE5
because now
RES = I r /I n - (I, - I n )/I n
= (I a /I n )RE - R a /I n
which is the equation of a straight line with
slope I a /I n and the intercept - R a / I n (see
Fig. 3, below). Since the resources increase,
the somatic investment of reproductive individuals is reduced below the level of nonreproductive individuals only when
RE > (I, - I n )/I a = REa.
When reproductive effort (RE) is equal to
REa, reproduction is not associated with
somatic costs because RES = 0. When RE
is smaller than REa, reproductive individuals allocate more resources to soma than
nonreproductive individuals. Therefore,
RES can be negative if reproductive effort
is low enough. (For an example, see the
Anodonta population n:o 550 in Fig. 5.)
There are at least two ways in which reproductive individuals can increase their
Ia above the level of In. First, they can in-
FIG. 3. The maximum reproductive effort without
survival costs in the trade-off hypothesis (RE,), the
compensation hypothesis (RE2), and the threshold hypothesis (RE/ and RE2') when the line RE, = C/I n
represents the threshold value of somatic costs (RE,).
crease their resource intake and ingestion
during reproductive period above the level
of nonreproductive individuals (Randolph
etal., 1977). Second, reproductive individuals could invest more resources in somatic
growth prior to reproduction and transfer
this increment in somatic resources later
to offspring production (Fig. 2). In the latter case, the extra resources accumulated
during somatic growth form the resource
pool for reproduction, and reproduction
would result in seasonal fluctuations in the
weight of reproductive individuals, as reported in fish (lies, 1974). The weight of
nonreproductive individuals can also fluctuate, but the amplitude of fluctuations
should be higher in reproductive individuals if this mechanism is operating.
Survival costs: threshold hypothesis
If somatic costs are assumed to result in
survival costs, then maximal reproductive
effort without any somatic costs and survival costs is RE, = 0, when Ia = In. The
corresponding maximal effort is RE2 =
REa > 0, when reproductive individuals are
able to increase their Ia above the level of
In (Fig. 3). Then reproduction can take
place without somatic and survival costs
only if RE < REa. A further possibility is
that somatic costs do not entail equivalent
survival costs.
30
TUOMI ET AL.
This is not an unrealistic possibility because resource shortage does not automatically mean a shorter life-span. On the
contrary, moderately starved animals can
live even longer than animals feeding ad
libitum {e.g., Ross and Bras, 1975). This
shows that a decrease in somatic investments does not necessarily lead to survival
costs, and indicates that organisms may
have physiological mechanisms which allow them to resist moderate resource deficiencies. However, it is not clear how
closely this situation resembles the resource deficiency caused by the somatic
costs of reproduction. In some plants, reproduction per se seems to be the cue leading to the death of the parent individual
(Woolhouse, 1978). But, among iteroparous organisms, there are probably cases
where parents suffer survival costs due to
the somatic costs of reproduction only when
the somatic investments are reduced below
a specific minimum level, say ln — C. Then
survival costs would occur only when Is <
In — C and reproductive effort is maximal
without survival costs when Is = In — C and
RES = C/I n .
Physiological resistance to somatic costs
could allow the maximum effort to increase above RE, and RE2 without survival
costs. When Ia = In, this maximum level of
effort would be RE,' = C/I a = C/I n , where
RE,' > 0 if C > 0. When Ra > 0 and C >
0, the maximum effort without survival
costs would be RE2' = (C + R a )/I a , where
RE2' > RE2 > 0 (Fig. 3). Here C/I n is the
threshold value of RES. Reproduction produces no survival costs when somatic costs
remain below the threshold level. But the
survival of reproductive individuals would
decrease when somatic costs exceed the
threshold level.
The threshold hypothesis might explain
some physiological aspects of age-specific
variation in reproductive effort (RE) and
somatic costs (RES) in species where individual organisms invest resources in reproduction only to the extent that such investment does not reduce their own
survival. Resistance to somatic costs
(Svardson, 1949), as well as the ability to
compensate for somatic costs by means of
increased resource input, can vary with the
age and/or size of individuals. The threshold value of RES could also depend on the
environment (Haukioja and Hakala, 1979)
and the physiological state of the individuals themselves.
Direct and indirect survival costs
Reproduction can result in survival costs,
or it may entail no somatic costs and/or no
survival costs. A reduced level of somatic
investment could lead to survival costs in
two ways.
First, somatic costs can result in direct
survival costs when the reduced level of
somatic investment as such reduces the survival of reproductive individuals. When reproductive effort approaches 1.0 (Fig. 3),
somatic costs could become so high that
the reduced level of somatic investment itself leads to the death of reproductive individuals. However, reproduction may not
lead to direct survival costs with low or
moderate reproductive effort.
Second, reproduction could also produce indirect survival costs when somatic
costs cause no direct survival costs but increase the vulnerability of reproductive individuals to predators (Shine, 1980), disease (Hirshfield, 1980), or other critical
factors in the environment (Haukioja and
Hakala, 1979). Indirect survival costs arise
only when a specific critical factor of the
environment is present.
Consequently, several causal paths could
result in survival costs, but it is conceivable
that nearly as many do not. Therefore, theories of reproductive tactics require alternative models, with and without survival
costs. Theory and experiment should address three questions:
(1) Does reproduction generally lead to
survival costs?
(2) What are the causal mechanisms producing survival costs when they arise?
(3) Are survival costs generally highenough to produce significant effects
on the evolution of reproductive tactics?
Demographic optimality models have simply assumed ineluctable mechanisms which
ALTERNATIVE CONCEPTS IN LIFE-HISTORY EVOLUTION
REPRODUCTIVE VALUE AI
THE AGE X+l A!iD SURVIVAL
1YPOTHETICAL GEHES
OF ALLOCATION AT THE AGE )
FECUNDITY COSTS
CURRENT REPRODUCTIVE
OUTPUT AT THE AGE X
RESIDUAL REPRODUCTIVE
VALUE AT THE AGE X
RRV.
REPRODUCTIVE VALUE AT
~THE AGE X
SELECTION FOR OPTIMAL
TACTiCS DEPENDING ON
PAYOFFS IN FITNESS
FIG. 4. An outline of the demographic theory of
optimal reproductive tactics. Age-specific reproductive tactics are assumed to evolve under the purely
demographic forces of selection.
lead to survival and fecundity costs which
have significant evolutionary consequences on reproductive tactics.
31
effort is heritable. Demographic theory has
also minimized the role of organisms themselves in the evolution of reproductive tactics. It represents a specific approach to the
evolution of reproductive tactics from the
purely demographic angle (Stearns, 1980).
Selection is supposed to operate on separate life-history traits rather than on individual organisms (Tuomi el al., 1983).
We show an example where residual reproductive value seems to play no role in
the evolution of age-specific reproductive
tactics. We also discuss the role of organismic selection in the evolution of reproductive tactics.
A test of the theory
One cannot test empirically whether
maximizing fitness and reproductive value
are equivalent or whether selection maxiSELECTION
mizes rm. These questions are primarily
Demographic theory compressed natu- theoretical and beyond the scope of direct
ral selection into the demographic equa- empirical tests. However, it is possible to
tions representing fitness (e.g., intrinsic rate test whether age-specific reproductive tacof increase, rm) and reproductive value (Fig. tics correlate with RRV. Williams (19666)
4). Williams (\966b) proposed that selec- predicted a negative correlation between
tion optimizes reproductive tactics at each reproductive effort and residual reproducage depending on reproductive value mod- tive value. This prediction can be tested by
ified by current reproductive output and comparing age-specific values of reproducresidual reproductive value (RRV). Schaf- tive effort and RRV within the same popfer (1974) derived an analytical model by ulation. But the prediction should also hold
assuming that maximizing fitness and re- when comparing the same age-classes beproductive value are equivalent. Later, a tween different populations. Also in this
number of models were generated to pre- case, there should be a negative correlation
dict age-specific variation in reproductive between reproductive effort and RRV, if
effort {e.g., Pianka and Parker, 1975; reproductive effort is optimized in each
Charlesworth and Leon, 1976; Stearns, population depending on RRV.
1976; Bell, 1980).
Mantyla (1981) has studied the age-speHowever, the mathematical basis of de- cific reproductive tactics of a freshwater
mographic theory has been questioned. It mussel, Anodonta piscinalis (Unionidae), in
is not clear whether maximizing fitness and eight local populations. He estimated
reproductive value are always equivalent "reproductive effort" by using the index
(Schaffer, 1979, 1981; Caswell, 1980;
RE5 = (Wn - W r )/W n
Ricklefs, 1981), and maximizing rm, or other abundance measures of fitness, is itself which corresponds to the present definia questionable evolutionary principle tion of somatic costs. The index (Haukioja
(Yodzis, 1981). Other fitness definitions are and Hakala, 1978) measures how much the
available, too (Stearns, 1983; Stearns and somatic weight of reproductive individuals
Crandall, 1981). Furthermore, the biolog- (Wr) is reduced during reproduction below
ical basis of demographic theory is highly the somatic weight of individuals of the
simplified. No evidence has been presented same age in the nonreproductive stage (Wn).
that age-specific variation in reproductive
RE5 was observed to increase almost lin-
32
TUOMI ET AL.
TABLE 2. Correlations of the index of somatic costs (REJ
with current reproductive output mo residual reproductive
value RRVa and the ratio mx/RRVx in three age-classes of
Anodonta piscinalis."
403020-
Age-class (x)
4yr
""
5yr
10-
m,
RRV X
m x /RRV x
<n
111
tr <H
r
AGE
0.845**
-0.109
0.891**
0.830*
-0.056
0.833*
• The correlations were calculated by comparing
the eight populations shown in Figure 5. From Mantyla (1981).
*P < 0.05, ** P < 0.01.
-10-
i
0.836**
-0.245
0.860**
(YEARS)
Fic. 5. Age-specific trends in the index of somatic
costs (RE,) in eight populations of Anodonta piscinalis
(Mollusca, Unionidae) studied by Mantyla (1981).
early with age in all the populations studied
(Fig. 5). But there was no clearly inverse
relation between RES and RRV within the
populations because RRV increased in
young age-classes, at least up to the 4th
year of life. The increase in fecundity more
than compensated for adult mortality in
RRV, which began to decrease only in the
very old age-classes. Furthermore, there
was no significant correlation between RES
and RRV when the same age-classes were
compared between the populations (Table
2). The results indicate that RRV as such
played little or no role in the evolution of
reproductive tactics in Anodonta piscinalis.
The ratio between current reproductive
output and residual reproductive value
(m x /RRV x ) gave statistically significant
correlations, obviously due to the strong
correlations between RES and mx (Table 2).
It seems that in Anodonta populations reproductive tactics were not moulded by
purely demographic forces of selection, at
least not by RRV alone. Major factors
moulding the reproductive tactics of Anodonta might be physiological processes
modified by environmental resource availability and other environmental factors (see
also Haukioja and Hakala, 1978).
Selection and organisms
Life-history models describe selection as
a demographic abstraction where each lifehistory trait is separately optimized de-
pending on payoffs in fitness. For simplicity, physiology and ontogeny are omitted
(Stearns, 1980). However, it is useful to
study how the reasoning of demographic
theory changes if selection is assumed to
operate on whole organisms, rather than
on separate life-history traits (Table 3).
Separate life-history traits have no independent existence in nature; they are always dependent upon the structural and
functional organization of an individual organism. Therefore, individual life-history
traits are not free to coevolve under the
purely demographic forces of selection.
Structural, physiological and developmental constraints can restrict the potential evolutionary trajectories (Stearns, 1977,
1980; Gould and Lewontin, 1979). This
suggests the need for a shift from unconstrained to constrained optimization, where
the constraints determine the boundaries
of opportunity sets—the sets of feasible
phenotypes on which selection can operate. In such theory, selection is assumed to
mould the life-history strategies of organisms only within species-specific opportunity sets.
The structural and physiological organization of an individual organism can also
result in intercouplings between individual
life-history traits. Then a change in one
trait could be automatically associated with
changes in other traits (e.g., when either
evolutionary or purely phenotypic changes
in developmental and growth rates automatically cause changes in the age of maturity and generation time). It is quite possible that the syndromes generalized as the
ALTERNATIVE CONCEPTS IN LIFE-HISTORY EVOLUTION
r/K-continuum (Pianka, 1970) reflect just
these intercouplings and not ecological selection pressures as assumed in the theory
of r and K-selection. Naturally the truth
could lie somewhere between these two
possibilities if both physiological intercouplings and the ecological conditions of living restrict the possible combinations of
life-history traits.
A further problem goes back to Darwin,
who assumed that natural selection operates in the same way as artificial selection,
allowing only the fittest to persist in the
population. If selection operates as conventional artificial selection, it would be an
extremely effective and sensitive evolutionary mechanism, which could modify the
adaptive strategies of organisms in every
detail.
However, an alternative hypothesis for
the operation of natural selection has been
suggested (e.g., Stearns, 1983; Tuomi et al.,
1983). Natural selection operating on
whole organisms need not necessarily operate in the same way as artificial selection,
but rather as negative mass selection
(Wright, 1980), in which deleterious mutants and unfit phenotypes are eliminated,
without precise optimization. Demographic theory is based on the implicit assumption that in nature organisms follow only
the best possible strategies of reproduction. But in fact nature can be less perfect
(Darlington, 1977; Gould and Lewontin,
1979), if organisms follow strategies that
are satisfactory or "good enough" in given
ecological conditions, but not necessarily
"optimal" in any sense (Stearns, 1983).
Optimality models have been effective
tools for making predictions in life-history
evolution, but that selection always operates in nature with the precision of optimization is only a theoretical possibility.
DISCUSSION
The value of life-history theory as a whole
for the biological sciences has been not so
much that it has successfully explained
variation in life-history traits, but that it
has brought the deficiencies of evolutionary theory into critical and open-minded
discussions. Evolutionary theory has
33
TABLE 3. A comparison of demographic theory with the
present outline for an organismic theory of reproductive
tactics.
Demographic theory
1. Resource limitation;
allocation system A;
reproductive effort
(E).
Trade-off between
current reproductive
output and survival
and/or future fecundity.
Separate life-history
traits are free to coevolve under purely
demographic forces.
Selection operates on
separate traits.
Selection optimizes
adaptive strategies.
Organismic theory
1. Allocation systems A,
Bl, B2, and B3; reproductive effort
(RE); somatic costs
(RE,); resource increment (RE,).
2. Compensation for somatic costs; cost
thresholds; direct and
indirect survival
costs.
3. Constraints and opportunity sets; physiological intercouplings
between traits.
4. Selection operates on
whole organisms.
5. Selection eliminates
unfit phenotypes but
does not necessarily
optimize adaptive
strategies.
undergone fundamental conceptual
changes since Darwin (Tuomi, 1981). Darwin formulated the general framework for
evolutionary theory, but his outline lacked
genetic, ontogenetic, and ecological mechanisms and details. The founders of theoretical population genetics together with
their modern followers have enriched the
original framework with detailed genetic
analyses and quantitative modelling. This
development culminated in the synthetic
theory, where population genetics was taken as the logical core of evolutionary theory as a whole. However, it has become
evident that while population genetics is
an essential speciality of evolutionary theory, ontogeny and ecology must also be
taken into account in evolutionary theorizing. Therefore, the synthetic theory
must itself evolve towards a more satisfactory theory, covering all the specialities
from genetics to developmental biology and
ecology. At present, we are far from such
a theory, but even modest attempts to combine these disparate specialities within the
34
TUOMI ET AL.
same framework provide steps towards that
goal.
ACKNOWLEDGMENTS
We thank S. C. Stearns and M. R. Rose
for useful and critical comments. The work
was supported by the Academy of Finland.
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