Reproductive compensation
PATRICIA ADAIR GOWATY
Department of Ecology and Evolutionary Biology, 621 Charles E. Young Drive, University of California, Los Angeles 90095, USA and The Smithsonian Tropical Research
Institute, Unit 0948, APO AA 34002-0948, USA
Introduction
But if you try sometimes you might find, You get what you
need
The Rolling Stones
What do individuals do when they are constrained to
reproduce with nonpreferred partners? If constrained or
coerced reproduction leads to lower fitness than repro-
duction with preferred partners, whenever heritable
variation (in genes, epigenetic elements, other develop-
mental programmes, etc.) exists, selection will result
in individuals sensitive to fitness outcomes and able
to flexibly resist mating and reproduction with non-
preferred partners. But, there are situations in which
reproduction with nonpreferred partners is the only
option (Gowaty, 1997). The question then becomes,
what can individuals ? constrained to mate with partners
they do not prefer ? do, if anything, to make up likely
fitness deficits compared with those individuals mating
Correspondence: Patricia Adair Gowaty, Department of Ecology & Evolu-
tionary Biology, University of California, Los Angeles, California 90095,
USA.
Tel.: 310 206-2186; fax: 310 206-0484;
e-mail: gowaty@eeb.ucla.edu
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Keywords:
constraints;
differential allocation hypothesis;
dispersal limitation;
life history trade-offs;
mate preferences;
offspring viability selection;
phenotypic plasticity;
sexual coercion.
Abstract
The reproductive compensation hypothesis says that individuals constrained
by ecological or social forces to reproduce with partners they do not prefer
compensate for likely offspring viability deficits. The reproductive compensa-
tion hypothesis assumes that (i) pathogens and parasites evolve more rapidly
than their hosts, (ii) mate preferences predict variation in health and viability
of offspring, (iii) social and ecological factors keep some individuals from
mating with their preferred partners (some are constrained to mate with
partners they do not prefer), (iv) all individuals may be induced to
compensate, so that (v) variation in compensation is due to environmental
and developmental factors affecting between-individual abilities to express
compensatory mechanisms. Selection favouring compensation may act
through variation in prezygotic physiological mechanisms, zygotic mecha-
nisms, or parental care to eggs or young that enhance offspring health,
increasing the likelihood that some offspring survive to reproductive age, often
at a survival cost to the parents. Compensation may be through increased
number of eggs laid or offspring born, a compensatory effort working during a
single reproductive bout that sometimes will match the number of offspring
surviving to reproductive age produced by unconstrained parents during the
same bout. The reproductive compensation hypothesis therefore predicts
trade-offs in components of fitness for breeders, such that parents constrained
to mating with a nonpreferred partner, but who compensate sometimes match
their current productivity (number of offspring at reproductive age) to
unconstrained parents (those breeding with their preferred partners), and,
when all else is equal, die faster than unconstrained parents. The reproductive
compensation hypothesis emphasizes that reproductive competition is not just
between constrained and unconstrained individuals, but also among con-
strained individuals who do and do not compensate. The reproductive
compensation hypothesis may thus explain previously unexplained
between-population and within-population, between-individual variation in
reproductive success, survival, physiology and behaviour.
doi:10.1111/j.1420-9101.2008.01559.x
with individuals they do prefer? One possibility is that
constrained individuals attempt to compensate for pre-
dictable fitness deficits in their offspring (Foerster et al.,
2003; Gowaty, 2003; Bluhm & Gowaty, 2004a; Navara
et al., 2006; Byers & Waits, 2006; Anderson et al., 2007;
Gowaty et al., 2007).
Thinking about some of the ways reproduction may
occur under social constraints on female mate prefer-
ences inspired the reproductive compensation hypothesis
(Gowaty, 1996, 2003; Gowaty & Buschhaus, 1998), but it
is important to keep in mind that reproductive compen-
sation can be induced by ecological constraints on mating
with one?s best (preferred) partner for offspring viability,
such as dispersal limitation and demographic stochastic-
ity, not just social constraints. Known social constraints
acting on males and females include male?male compet-
itive contests, and in some species in which females are
invulnerable to social coercion, female mate choice may
limit males? options for mating partners. Sexually
coercive constraints limit females access to partners, but
also males? and include infanticide (Hrdy, 1974, 1977,
1979, 1981), forced copulation (Brownmiller, 1975;
Cheng et al., 1982, 1983; McKinney et al., 1983; Gowaty
& Buschhaus, 1998), male aggression against females
(Smuts, 1992, 1995; Smuts & Smuts, 1993), male mate-
guarding (Dickemann, 1979a,b, 1981; Gowaty, 1996),
sperm plugs and peptides that decrease females?
re-mating tendencies (Chapman et al., 1994; Chapman
& Partridge, 1996; Rice, 1996).
The reproductive compensation hypothesis emphasizes
how selection might act not just among constrained and
not constrained individuals, but between constrained
individuals who can and cannot trade-off components of
fitness to flexibly adjust physiology and behaviour in
ways that enhance the future survival of their offspring.
The reproductive compensation hypothesis is sexually
symmetric, predicting that both sexes of parent are
sensitive to, can assess, and respond flexibly to environ-
mental and social conditions, i.e. both sexes may
compensate. This paper contains a brief review of the
assumptions of the reproductive compensation hypo-
thesis, first presented in Gowaty (1996, 2003); Gowaty &
Buschhaus (1998), and Gowaty et al. (2007). It also
contains a quantitative description of components of
fitness essential for understanding the reproductive
compensation hypothesis, a comparison with the differ-
ential allocation hypothesis, and a discussion of the range
of predictions of the reproductive compensation hypo-
thesis with a focus on tests that depend on components of
fitness. Last, I include a discussion of the question, ?Can
compensation evolve??
The assumptions
The assumptions of the reproductive compensation
hypothesis include: (i) The most ubiquitous and persis-
tent threats to offspring health are pathogens and
parasites (Van Valen, 1973). (ii) Variation in offspring
viability favours mate preferences in both sexes (Bondu-
riansky, 2001; Gowaty & Hubbell, 2005). (iii) Impedi-
ments (ecological and social) to reproduction with one?s
best partner exist (see references above). (iv) Mecha-
nisms of compensation evolve rapidly to fixation, so that
all individuals may compensate and (v) variation in
expressed mechanisms of compensation is due primarily
to environmental and developmental factors affecting
individual ability to express compensatory mechanisms.
The Red Queen?s challenge to parents, mate
preferences and constraints on mate preferences
As the metaphor of the Red Queen stresses, pathogens
evolve more rapidly than their hosts. This means that the
pathogens that attack the parental generation may not be
the same pathogens challenging the health of offspring.
As Hamilton & Zuk (1982) said, if host?parasite cycles of
evolutionary response ??are very short, then trying to
choose mates for the ?right? genes for resistance is a
perverse task?? (p. 384). In this case it would be unlikely
that elaborate traits in potential fathers signalled ?good
genes? for offspring health. If variation in the underlying
genetic components of offspring viability favour mate
preferences as the reproductive compensation hypothesis
assumes, there is unlikely to be a single best male, better
for all females than any other male, because females
vary, and like males, contribute to the genetics, (as well
as the epigenetics, ecology, development and culture) of
offspring viability. If indicator traits show the true health
status of the signaller, they may be honest indicators of
an individuals? ability to provide direct benefits to
females and to their offspring, but still say little about
the genetics and development of offspring immune
systems that must be an important component of
offspring viability ? unless there is little or no evolution
of pathogens between parental and offspring generations.
However, if offspring viability is influenced by alleles that
work against offspring generation pathogens, the current
health status of a potential mate may not predict the
health of offspring. In such cases, it is possible that
?honest? indicators manipulate or dazzle choosers,
exploiting their pre-existing sensory biases (West-Eber-
hard, 1979, 1984), so that choosers make reproductive
decisions that may not favour offspring health. Thus,
showy and elaborate traits could be simultaneously
honest about some components of fitness (e.g. the
breeders? current health and ?or probability of survival),
but may provide limited or no information relevant to
other components of fitness. This perspective emphasizes
that there may be other effects of host?pathogen arms
races on individuals? reproductive decisions besides the
evolution of elaborate traits in males. Of central impor-
tance here is that the perennial evolutionary arms races
between hosts and their pathogens challenge parents
anew in every generation.
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In Fig. 1a,b, the dark solid curves are cartoons of an
adaptive response to theRedQueen?s challenge to parents.
These high-variance curves are frequency distributions of
the pathogen-fighting phenotypes unconstrained parents
produce. The phenotypes likely to work against the
pathogens in the parental generation are between
the vertical dashed lines. However, these phenotypes will
benomore, and,moreoften, less effective against offspring
generation pathogens. This will be so if pathogens differ-
entially evolve offensive mechanisms against the most
commondefensive phenotypes in the parental generation.
The biggest challenge parents may face, therefore, is to
produce the rare phenotypes that are likely towork against
the modified pathogens in the offspring generation. Rare
phenotypes in Fig. 1a,b are in the tails of the distribution of
offspring phenotypes parents can produce (those outside
the vertical dashed lines).
Red Queen logic led Brown (1997) to argue that
selection favours female mate preferences for hetero-
zygosity in males and Wedekind & Furi (1997) and
Wedekind et al. (1995) to argue that selection favours
female mate preferences for complementary (dissimilar)
immunogenes, an argument Penn & Potts (1999) for-
malized for vertebrates in their focus on the major
histocompatibility complex (MHC). The mechanisms of
mate preference posited by Brown, Wedekind, Penn and
Potts are consistent with the idea that mate preferences
are favoured by offspring viability selection, perhaps
based on compatibility between mates (Ryan & Altmann,
2001). The focus here then is not on the cues associated
with mate preferences, but on the fitness consequences
of reproducing under social constraints on the free
expression of preferences for both sexes. This analysis
assumes that offspring viability favours mate preferences
by both sexes independent of patterns of parental
investment (Hubbell & Johnson, 1987; Ryan & Altmann,
2001; Gowaty et al., 2003; Gowaty & Hubbell, 2005).
I also assume that offspring viability selection works in
invertebrates not just vertebrates and can favour mate
preferences mediated not just through MHC variation,
but also through variation in innate immunity.
Against this backdrop, the question becomes, what can
individuals of either sex do when ecological or social
forces constrain them to reproduction with partners that
are nonoptimal for offspring viability? Constrained par-
ents may attempt to compensate for offspring viability
deficits by flexibly adjusting the number of offspring born
or eggs laid, i.e. fecundity (Fig. 1a) to affect other fitness
components (Tables 1 and 2), or physiology and behav-
iour (Table 3) in attempts to compensate for relative
deficits in offspring viability.
Note that I am using the term ?constrained? to refer
to the constraint of mating with a nonpreferred partner,
specifically when mate preferences ? evaluated in the
absence of within sex interactions or between-sex
coercion (so that sexual selection and sexual conflict
are controlled) ? predict variation in offspring viability.
Reproductive compensation via enhanced fecundity
Because the most radical prediction of the reproductive
compensation hypothesis is that mothers constrained to
reproduction with partners they do not prefer increase
fecundity (the solid light line in Fig. 1a), I emphasize
Fig. 1 Cartoon models of the Red Queen?s challenge to parents and
reproductive compensation by (a) increasing fecundity (the number
of offspring born or eggs laid) and (b) increasing variance in offspring
phenotypes without increasing fecundity. Assuming that pathogens
evolve more rapidly than their hosts, that mate preferences predict
viability of offspring, and that ecological and social constraints keep
some individuals from mating with their preferred partners, the
wide, dark curve represents offspring phenotypes produced by
unconstrained parents. The peaked areas of the curves in the centre
of the graphs between the vertical, dotted lines represent the
offspring phenotypes parents are most likely to produce, i.e.
offspring phenotypes likely to resist the pathogens and parasites of
the parental generation. The areas under the curves in the tails of the
distributions represent those phenotypes likely to resist the novel
pathogens and parasites in the offspring generation. The dotted
curve represents the offspring phenotypes produced when parents
are constrained to reproduction with partners they do not prefer.
The narrow, solid line represents the offspring phenotypes produced
when constrained parents attempt to compensate by increasing the
number of eggs laid or offspring born (a) or by increasing the
variance in offspring phenotypes they produce (b). When con-
strained parents increase fecundity as in (a), the area under the
curve in the tails of the distribution would be increased, enhancing
the probability that some of their offspring are able to resist offspring
generation pathogens. When constrained parents increase the
variance in offspring phenotypes without increasing fecundity,
perhaps through mating with more than one partner, the area under
the curve in the tails of the distribution would be increased,
enhancing the probability that some of their offspring are able to
resist offspring generation pathogens.
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discussion of compensation via fecundity in this section
and discuss compensation by other means (Table 1 and 3)
further on. The discussion that follows is an operational-
ized discussion of the trade-offs in components of fitness
associated with compensation by an increase in fecundity.
Define offspring viability, V, as the fraction of indi-
viduals born or eggs laid (F or fecundity) that survive to
reproductive age, (N or productivity) (see Table 1 for
a list of fitness components). The reproductive compen-
sation hypothesis says that within- and between pop-
ulation variation in V arises most reliably because of
within- and between-population variation (1) in the
degree of constraints on parents? reproductive decisions
and (2) in the rate of pathogen evolution. Breeder
productivity, N (the number of offspring that survive
to reproductive age, a, see Table 1), is the product
of breeder fecundity, F and offspring viability, V. Here
variation in V is a component of offspring fitness
(Anderson et al., 2007) that, through its effects on N,
acts as a selection pressure on parents.
Under pathogen pressure, as the degree of constraint on
individual reproductive options increases, V declines. This
causes selection on constrained parents to compensate for
Table 1 Definitions and symbols for com-
ponents of fitness for breeders and offspring.Component of fitness Symbol Definition
Offspring viability V Fraction of offspring born or eggs laid, F, surviving to time a
Offspring age of first
reproduction
a Time from birth or hatch to first reproduction, i.e. age at first
reproduction
Breeder fertility B Number of bouts of reproduction: > 1 for iteroparous species
Breeder fecundity F Number of offspring born or eggs laid per B
Breeder productivty N Number of offspring that survive to reproductive age per B
Breeder time between
reproductive bouts
I Time interval between Bs
Breeder survival probability S Likelihood of continued survival
Table 2 Variation in components of fitness predicted by the hypothesis of reproductive compensation and differential allocation (sensu Burley,
1988).
Reproductive compensation
(constrained to mate with partners
individuals do not prefer, c, vs.
nonconstrained, nc, mating with
partners individuals do prefer)
Differential allocation (mated with attrac-
tive, a, or unattractive, ua, partners)
Fitness component Females Males Females Males
V, offspring viability Vnc > Vc Vnc > Vc No prediction
N, parent productivity Nnc > Nc Nnc > Nc Na > Nua Na > Nua
S, parent probability of survival Snc > Sc Snc > Sc Sa < Sua Sa < Sua
M, parent number of mates Mnc > Mc Mnc > Mc Ma < Mua Ma < Mua
F, parent fecundity (num offspring born or eggs laid) Fnc < Fc Fa > Fua
SP, sperm ejaculated SPnc < SPc SPa > SPua
B, parent fertility (num reproductive bouts) Bnc < Bc Bnc < Bc Ba > Bua Ba > Bua
I, parent interval between reproductive bouts Inc > Ic Inc > Ic Ia < Iua Ia < Iua
a offspring age at first reproduction anc > ac anc > ac No prediction No prediction
Table 3 The reproductive compensation hypothesis predictions
about physiology and behaviour when individuals do and do not
make reproductive decisions under constraints. ?c? indicates ?con-
strained? and ?nc? indicates ?nonconstrained?.
Timing
Morphological,
physiological, and
behavioural traits of
breeders and parental
effects on offspring
Predictions of
the reproductive
compensation
hypothesis
Pre-mating Aggressive c > nc
Dominant c > nc
Most exaggerated ?indicator? traits c > nc
Multiple mating (?profligacy?,
extra-pair copulations)
c > nc
Pre-zygote Number of sperm per ejaculate (males) c > nc
Number of eggs ovulated (females) c > nc
Post-zygote Intensity of brooding or fanning eggs c > nc
Food provisioning c > nc
Immune elements contributed
through nursing or other provisioning
c > nc
Parental contributions to eggs, foetuses,
or offspring of hormones or peptides
facilitating ?puberty acceleration?
c > nc
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lower N by increasing F (Fig. 1a, light solid curve), other
fitness components (Table 2), or offspring and ?or parent
physiology and behaviour (Table 3) related to offspring
health (Fig. 1b). Increased parental fecundity increases
the likelihood that some of the offspring express rare
phenotypes that may confer better resistance against
offspring generation pathogens (Fig. 1a, solid light curve).
Parents may compensate by increasing fecundity or
similarly the number of bouts of reproduction (B or
fertility, Table 1), because as the number of offspring
produced increases, the number likely to express rare
phenotypes that may work best against offspring genera-
tion pathogens also increases, a simple mean to variance
argument (Fig. 1a, light solid curve).Note that thenumber
of offspring born or eggs laid, F, is expected to be higher for
constrained breeders who do compensate (Fig. 1a, light
solid line) comparedwith constrained breederswhodonot
compensate (Fig. 1a, dashed line) and also compared with
unconstrained breeders (Fig. 1a, high variance, dark solid
line). Note that although the phenotypic offspring vari-
ance of the dotted curve (constrained, but noncompen-
sating) and the light solid curve (constrained and
compensating) are the same, because the compensation
curve is higher (higher fecundity), there are numerically
more offspring in the tails. The phenotypic variance has to
be the same because there is no change in the parental
genotypes, just in the number of offspring that they have.
Thus in a comparison of constrained parents, those that
compensate will produce absolutely more offspring than
those who do not.
For equivalent fertility, unconstrained breeders will
expose more phenotypic variation among their offspring
for defence against evolving pathogens than will con-
strained breeders (Fig. 1a). However, if constrained
breeders increase their fertility (B, the number of bouts
of reproduction), they can potentially expose more
variation in offspring phenotypes for pathogen resis-
tance. Increased F increases the probability that at least
some offspring of constrained breeders will be resistant to
evolving pathogens (Fig. 1a). This effect is compensatory
because it reduces the difference in the productivity
of parents constrained to breed with partners they do
not prefer (Nc) and the productivity of parents not
constrained (Nnc). (In the following the notation, ?c?
indicates constrained to mating with partners nonpre-
ferred and ?nc? indicates not constrained, so that individ-
uals mate with those they prefer).
It is worth emphasizing that even production of more
offspring with the parental phenotypes is a compensatory
benefit in response to lower survival of these offspring. The
compensatory benefit accrues over the entire distribution
of offspring phenotypes that parents produce, not just in
the tails of the distribution, because unless constrained
parents adaptively control the distribution of offspring
phenotypes so that their variance is increased (Fig. 1b)
they will produce more compensatory offspring between
the dotted vertical lines in the middle of the distribution
than in the tails of the distribution. Thismight often be the
major benefit of compensating. Figure 1b is a cartoon
model showing a distribution of offspring phenotypes
unconstrained parents produce (dark solid line as in
Fig. 1a) along with the distribution of phenotypes con-
strained parents might produce if they compensate by
adaptive modification of the variance in offspring pheno-
types (light solid line). Here, the compensatory effect is not
through increasing numbers throughout the distribution
of offspring phenotypes, but through adaptive distribution
of offspring numbers into the tails of the distribution,
a variance increasing effect. Mating with more than one
partner may be a compensatory mechanism to achieve
adaptivemodification of variance in offspring phenotypes.
Two conditions induce compensation
Compensation can be induced by variation in constraints
on mate preferences that predict offspring viability or by
changes in the pathogen environment alone.
When no constraints on the expression of mate prefer-
ences exist (i.e. no stochastic effects, no ecological or
dispersal limitations, no sexual selection and no sexual
coercion), the mean strength of pathogen challenge alone
will be a primary determinant of breeder productivity,N. If
pathogen challenge increases during a given breeder?s
lifetime, mean offspring viability, V, would decline. In
response, all breeders with appropriate developmental
flexibility should attempt to compensate. As with individ-
uals under social or ecological constraints on their mate
preferences, individuals who respond to pathogen chal-
lenge can increase productivity, N, by increasing fecun-
dity, F, whichmay expose low-frequency variation among
progeny in the genetic and phenotypic elements likely to
work against offspring generation pathogens (Fig. 1). Or,
they might compensate in other ways (Table 3).
Whether compensation is induced by variation in
constraints on mate preferences or from pathogenic
change, increasing F and ?or other compensatory adjust-
ments are expected to be costly to breeders, so that
breeders who compensate may incur costs, which should
be obvious in terms of declines in breeder survivorship,
S (Table 1). Elsewhere we model the social-selective
conditions under which a quantitative trait for reproduc-
tive compensation can evolve (P. A. Gowaty & S. P.
Hubbell, unpublished data). Under a large range of
selective scenarios, even when breeder survival costs are
quite high, compensation evolves (see below).Moore et al.
(2003) and Anderson et al. (2007) reported survival costs
of compensation respectively in Nauphoeta cinera and
Drosophila pseudoobscura.
The offspring viability assumption
The assumption that Vc < Vnc is met in a wide variety of
species including flies (Anderson et al., 2007), mice
(Drickamer et al., 2000, 2003), pronghorn (Byers &
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Waits, 2006), ducks (Bluhm & Gowaty, 2004b) and other
species (see review in Gowaty et al., 2007). For compen-
sation to be successful, compensatory efforts need only
increase productivity, N, of constrained breeders that do
compensate above constrained breeders that do not
compensate. When constrained breeders compensate,
they may rarely succeed in achieving perfect compensa-
tion (i.e. Nc = Nnc) partly because of the costs of
compensation. Compensation would, nevertheless, be
favoured whenever there is variation among constrained
individuals in their abilities to compensate. Thus, the bar
is set in two places for constrained individuals: first, in
comparison to unconstrained competitors and, second, in
relation to variation in the ability of other constrained
individuals to compensate.
Because V, offspring viability, is operationally defined
here as N ?F, there are nine possible relationships
between fecundity, F, and productivity, N characterizing
Vc and Vnc (Fig. 2). In Fig. 2, panels c, d, and f show that
Vnc > Vc and therefore, only these relationships between
F and N for constrained and unconstrained individuals
meet the reproductive compensation hypothesis assump-
tion that Vc < Vnc. Figure 2c shows Fnc = Fc, but
Nnc > Nc so that although Vc < Vnc, there exists no
evidence of attempted compensation via increased F.
However, Fig. 2d and e indicate Fc > Fnc, consistent with
attempts to compensate for Vc < Vnc. Figure 2d shows
completely successful compensation via increased F,
because Nc = Nnc. Figure 2f shows unsuccessful compen-
sation because despite Fc > Fnc, Nc < Nnc.
Observation of relationships in Fig. 2a,b,e,h and i
would indicate that the assumption of the reproductive
compensation hypothesis is not met. This is because
variation in F and N is such that Vnc < Vc.
The discussion above emphasizes what is expected if
mothers compensate by increasing fecundity, but other
compensatory mechanisms (discussed below) are possi-
ble. The selection differential, Nnc > Nc will favour
compensatory fecundity, fertility, behaviour or physio-
logy (Tables 2 and 3) such that the differences in
productivity, Nnc and Nc, are minimized relative to
existing pathogen pressures. Even when compensation is
completely successful via increased F (Fig. 2d), bouts of
reproduction, B, longer intervals between reproductive
bouts, I (Table 3) or via various types of parental care,
so that Nc = Nnc, the costs of compensation for Vnc < Vc
often will result in lower survival, S, of breeders repro-
ducing under constraints, i.e. Snc > Sc. This should be so
even when Bnc = Bc and even when breeder fecundity is
Fnc = Fc. The predicted relationship between Snc > Sc is
not simply due to higher Fc but due to the costs of
attempts to compensate for lower Vc, which could occur
through fecundity compensation or another compensa-
tion mechanism altogether (see below).
Compensation is unlikely when variation in
developmental flexibility is low
The reproductive compensation hypothesis does not
predict fecundity variation in highly inbred pairs in
which genetic and developmental variation are low or
nonexistent (Meagher et al., 2000); it does predict com-
pensation via increased fecundity whenever latent var-
iation can be uncovered by increasing the number of
offspring produced. Of course, inbred pairs may com-
pensate by other means (Table 3) including, but not
limited to, increased B, number of bouts of reproduction,
or shorter I, intervals between bouts of reproduction
(Tables 1 and 2).
Pre-copulation compensatory mechanisms
Males may compensate by increasing access to females
through enhanced within-sex aggression, dominance
Fig. 2 All possible combinations of fecun-
dity, F (solid lines), and productivity (num-
ber of offspring reaching reproductive age), N
(dashed lines), when breeders are noncon-
strained, reproducing with partners they
prefer, and constrained, reproducing with
partners they do not prefer. Offspring via-
bility, N ? F, is the same for constrained and
unconstrained in (a, e, and i). N ? F is greater
in constrained than nonconstrained in (b, g,
and h). Thus, (a, e, i, b, g, and f) fail to meet
the assumption of the reproductive com-
pensation hypothesis that offspring viability
is greater for nonconstrained breeders. This
assumption is met in panels (c, d, and f).
However, compensation is fully successful
only in panel (d) in which N is the same for
nonconstrained and constrained individuals.
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behaviour and their rate of attempted reproduction with
multiple females (Table 2). Similarly, females may com-
pensate by increasing their numbers of extra-pair mates
to enhance their access to alleles favourable to enhanced
offspring viability (Foerster et al., 2003).
Exaggerated male dominance or aggression, or exag-
gerated indicator traits may be compensatory for likely
Vc < Vnc. This possibility allows predictions about which
males within a population are most likely to be aggres-
sive, dominant or fancy (Moore et al., 2002) and
profligate (Table 3). If the reproductive compensation
hypothesis is correct, in genetically structured popula-
tions, males least likely to be preferred (those that are
perhaps most similar to the females at immune coding
genes) are more likely to express compensatory within-
sex aggression and dominance behaviour than males
more likely to be preferred.
Compensatory mechanisms during copulation
The reproductive compensation hypothesis predicts that
males copulating under constraints with partners they do
not prefer ejaculate more sperm than males copulating
with fewer or no constraints with partners they do prefer
(Table 3). Larger ejaculates would increase the number
of and, thus, the variation among male gametic haplo-
types available to females to sort among. Kim et al.
(2005) showed that male D. pseudoobscura ejaculate more
sperm when mating with females they do not prefer and
with females who do not prefer them. The hypothesis
predicts males copulating under constraints with females
they do not prefer will contribute more peptides or
nutrients in their ejaculates that will enhance immunity
of zygotes and that they will do this flexibly in response
to encountered circumstances. Likewise, the reproduc-
tive compensation hypothesis predicts that females
physiologically select among the sperm of males they
do not prefer, so as to increase the likelihood that
resulting zygotes will have a higher probability of
survival to reproductive age than they otherwise would.
It predicts that females mating under constraints with
males they do not prefer will produce more oocytes to
increase the likelihood of rarer haplotypes in eggs
available for fertilization. It predicts that females and
males contribute more nutritive, immunity-enhancing
resources to the cells and tissues supporting their gametes
and resulting zygotes when they are constrained to
reproduction with partners they do not prefer than with
partners they do prefer.
Post-zygotic compensatory mechanisms, and
contrasts with the differential allocation hypothesis
Parents of either sex may attempt to compensate for
lower offspring viability, V, by increasing types of
parental care that mitigate the effects of pathogens on
their offspring. The reproductive compensation hypo-
thesis predicts that constrained mothers will lay bigger
eggs, as found in ducks (Bluhm & Gowaty, 2004a) or
nurse their offspring longer than unconstrained mothers,
as found in pronghorn (Byers & Waits, 2006). It predicts
that constrained mammal mothers will contribute more
antibodies over longer periods to dependent offspring
than those reproducing with preferred partners. It
predicts, all else equal, that constrained avian parents
more reliably incubate eggs than unconstrained parents,
whenever thermal stress to embryos is associated with
increased susceptibility to disease in embryos. For frogs
and fish that aerate egg masses to control against fungal
contamination, all else equal, the reproductive compen-
sation hypothesis predicts that constrained parents aerate
egg masses more than unconstrained parents. The
reproductive compensation hypothesis predicts that con-
strained parents may manipulate their offspring through
?parental effects? in ways that reduce the age of first
reproduction relative to the offspring of unconstrained
parents. Given that the host?pathogens arms races are
renewed in each generation, a parental effect to lower
the age of first reproduction of their offspring from
constrained matings would enhance the likelihood that
they would have grand-offspring.
In contrast to the reproductive compensation hypoth-
esis, the differential allocation hypothesis (Burley, 1988)
predicts greater parental allocations when individuals
reproduce with relatively attractive partners. This hypo-
thesis says that in socially monogamous species, selection
would favour individuals that flexibly adjust their alloca-
tions to offspring as a function of the relative attractiveness
of each of the parents, with the less attractive parent
allocating more parental effort than the more attractive
parent. Sheldon (2000) extended this idea to species
without bi-parental care, and predicted that females
allocatemore resources to the offspring of attractivemales.
Whether the predictions of this hypothesis contrast with
predictions of the reproductive compensation hypothesis
depends on whether consensus attractive individuals are
also individually preferred (Table 4) and on whether
consensus attractiveness predicts offspring viability (see
discussion above in relation to Hamilton & Zuk?s (1982)
hypothesis).
If attractive individuals are those that opposite sex
individuals display to the most in arenas containing more
than one of each sex as in Cunningham & Russell (2001),
it is possible that ?attractive? is not the same as a preferred
partner in an arena that eliminates intra-sexual interac-
tions and inter-sexual coercion to measure individual
preferences as in Bluhm & Gowaty, (2004a,b). If off-
spring viability is equal or lower when females mate with
consensus attractive partners rather than consensus
unattractive partners, one could speculate that ?attractive
traits? exploit chooser sensory biases so that choosers
make reproductive decisions that fail to enhance off-
spring viability or that group level attractiveness is
manipulated by intrasexual interactions or coercive
Reproductive compensation 7
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signalling; if this happens, females mated to ?attractive?
partners might be constrained, mating with partners they
do not individually prefer. Then, the predictions of the
two hypotheses would match, e.g. both would predict
enhanced number of eggs laid or offspring born, F,
or enhanced care, for example (Table 4). If consensus
attractive partners have offspring of higher viability than
consensus unattractive individuals; however, the predic-
tions are contrasting, with the differential allocation
hypothesis predicting higher F for females mated with
consensus attractive males and the reproductive com-
pensation hypothesis predicting higher F for females
mated with males they do not individually prefer. Tests of
these two hypotheses depend on the offspring viability
assumption, and before comparative tests of these two
hypotheses are carried out, the association with offspring
viability of consensus attractiveness and individual pref-
erences should be evaluated.
It is important in this context to emphasize the
meaning of ?attractive? and ?constrained to mate with a
partner one does not prefer?. In the reproductive com-
pensation hypothesis preference is about ?self-referential
preferences? (Ryan & Altmann, 2001); explicitly, this
means that there is unlikely to be a best male that all
females prefer or a best female that all males prefer. In
contrast, the differential allocation hypothesis (Burley,
1988) depends on there being males and females that are
attractive to most opposite sex individuals, i.e. consensus
attractive. Thus, whether these two hypotheses always
make contrasting predictions (Table 2) depends on the
special assumptions of the compensation hypothesis, and
the definitions and methods for evaluating ?individual
preferences? and ?consensus attractiveness?.
Do unconstrained breeders compensate?
Unconstrained breeders will compensate whenever there
is an increase in pathogenic challenge relative to back-
ground conditions. Thus, the reproductive compensation
hypothesis predicts within population variation in F as
a function of temporal variation in pathogen exposure,
even when social or ecological constraints on mate
preferences are absent. So, when pathogenic challenge
is changing relatively rapidly, unconstrained breeders
might compensate.
However, when pathogen challenge is not changing
more rapidly than usual between parents and offspring
generations, constraints on the expression of mating
preferences theoretically determine which parents com-
pensate. So that when some breed with partners they do
not prefer, whereas some breed with partners they
do prefer, the reproductive compensation hypothesis
says that individuals adjust F so that N for constrained
breeders might approximate N for unconstrained breed-
ers (Fig. 2c). However, except for the compensatory
effects against pathogens described in the preceding
paragraph, the theory does not predict compensation by
unconstrained breeders. This is because compensation is
likely to impose costs that lower parental survival. When
constrained breeders differ in resource availability, one
might expect that compensation would be expressed
more readily for those with high access to resources
because the effects of compensation on parental survival
could be reduced depending on the expressed mecha-
nism of compensation. Furthermore, because compensa-
tion by constrained breeders should rarely increase N
above that for nonconstrained breeders (see for example,
Anderson et al., 2007), the reproductive compensation
hypothesis says that N of unconstrained breeders is the
fitness component that constrained compensating indi-
viduals attempt to match.
Sexual selection among constrained and
nonconstrained breeders favours compensation
Many investigators consider variation in offspring viabil-
ity to result only in natural selection. When compen-
sation is in response only to differential pathogen
challenge, this argument would hold. However, the
argument that offspring viability selection is only natural
selection ignores the fact that variation in offspring
viability also occurs in response to variation in social
constraints on reproductive decision-making. Within-
population, within-sex variation in individual abilities to
remain in control of their own reproductive decisions
(e.g. with whom they mate) also results in reproductive
success variation and fits the Darwinian definition of
sexual selection ? for females as well as males. For
example, whenever offspring viability is less for con-
strained than unconstrained females, reproductive com-
petition among females may occur through fitness effects
from variation in individuals? vulnerabilities to coercion
(Gowaty, 1996). This perspective suggests that offspring
viability and other lineage effects, usually not considered
in models of sexual selection, may, in fact, be important
Table 4 Similar and contrasting predictions about F or other trait
such as increased egg size from the differential allocation hypothesis
and the reproductive compensation hypothesis, when the differ-
ences in methods for evaluating consensus attractiveness and
individual preferences are taken into account.
Choosers?
partners*
Differential
allocation
hypothesis
Reproductive
compensation
hypothesis
C-A and I-NC + )
C-A and I-C + +
C-UA and I-NC ) )
C-UA and I-C ) +
As elsewhere in this paper, those mated with partners they
individually prefer are non-constrained, (i.e. I-NC) and those mated
with partners they individually do not prefer are constrained (i.e.
I-C). Individuals mated with consensus attractive partners is
indicated by C-A; those mated with consensus unattractive partners
by C-UA.
8 P. A. GOWATY
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to understanding the full range of mechanisms of within-
sex reproductive competition (sexual selection).
Testing the reproductive compensation hypothesis
Whenever Vnc ? Vc, the main assumption of the repro-
ductive compensation hypothesis is not met, so that the
reproductive compensation hypothesis would not apply.
Whenever Vnc > Vc, the main assumption of the
reproductive compensation hypothesis is met, so that it
would be reasonable to seek evidence of reproductive
compensation. If Fnc < Fc, the prediction of attempted
compensatory reproduction via fecundity enhancement
of constrained individuals would be fulfilled. However,
only if Nnc = Nc would reproductive compensation be
fully successful. Whenever constrained individuals pro-
vision more than unconstrained (e.g. as in pronghorn,
Byers & Waits, 2006), the prediction of attempted
compensation via enhanced provisioning would be ful-
filled. Again, however, only if Nnc = Nc would reproduc-
tive compensation be fully successful.
Thus, the contest is most intense not between uncon-
strained and constrained breeders, but between con-
strained breeders who do (Fig. 1a,b, solid light curve) or
do not (Fig. 1a,b, dashed curve) compensate or those
who compensate relatively more and less efficiently than
others.
Evaluation of F or N alone would be inadequate for
evaluation of the hypothesis (Fig. 2). In lab studies, to
evaluate variation in V, i.e. offspring viability for breeders
in which constraints vary, investigators often compare
the effect of being with preferred and nonpreferred
partners. As ornaments in one sex may manipulate
the behaviour of the other sex, one must control the
possibility that honest indicators of health nevertheless
may manipulate the opposite sex into mating with
partners that are nonoptimal for the viability of offspring.
To do this, one might evaluate offspring viability against
preferences determined at random with respect to phe-
notypic traits in the discriminated sex as in Drickamer
et al. (2000), Bluhm & Gowaty (2004a), Moore et al.
(2003) and Anderson et al. (2007). Field tests of these
ideas, such as Byers & Waits (2006) will require a large
amount of information on individual breeders, mate
status and their offspring. In most cases, in the field it
is not clear how to measure the expression of mate
preferences free of the presence of confounding factors
such as male?male combat, female?female interactions
and mechanisms of male control and female resistance.
When choices are manipulated or coerced, choices may
not reflect preferences: individuals may have paired
under multiple constraints, including ecological and
developmental ones. All these potential factors make
judging which are the constrained pairings in the wild
difficult. Despite this difficulty, evaluation of predicted
relationships in mean offspring V and mean breeder F
and N between populations differing in pathogen pres-
sures is possible. However, such studies must then take
into account the likelihood that within populations some
individuals may, and others may not, be reproducing
under further constraints and may be compensating.
Testing for compensation via trade-offs in fitness
components of adults and their offspring seems the most
comprehensive way to test compensation. Anderson et al.
(2007) used a demographic, components-of-fitness
approach to fitness variation in constrained and uncon-
strained individuals. Replication of their methodology in
studies of other species will be valuable in evaluating the
general ability of the reproductive compensation hypo-
thesis to explain usually unexplained variation in com-
ponents of fitness (Table 2).
Testing for compensation via parental effects on phys-
iology and behaviour will be more difficult. Although
making and testing predictions of egg-size variation or
nursing duration are relatively easy to imagine and carry
out, what is needed is a hierarchical set of predictions
about parental effects, perhaps ranked in terms of their
costs to compensating parents. Since the relative cost ?
either in calories or fitness ? of different compensatory
mechanisms is entirely unknown, this is a question for
the future.
Within-population, between-sex variation in the ability
to compensate is likely affected by individuals? intrinsic
metabolic rate, the efficiency with which individuals
exploit resources and their access to extrinsic resources,
which probably interacts with the ability of individuals to
simultaneously compensate andwithstand the pathogenic
challenges they face (P. A. Gowaty & S. P. Hubbell,
unpublished data). Variation among females in their
abilities to avoid coercion will be a productive avenue for
future research on the costs and benefits of compensation.
Reproductive compensation can evolve
Is it reasonable to assume, given appropriate access to
resources, that all individuals can compensate? This is a
question related to the evolution of developmental
plasticity, flexibility and induced responses (West-Eber-
hard, 2003; Joblonka & Lamb, 2005) and the costs of
plasticity (Scheiner & Berrigan, 1998; Relyea, 2002; Bize
et al., 2004; Steiner & Van Buskirk, 2008). P. A. Gowaty
& S. P. Hubbell (unpublished data) have answered this
question theoretically using a simple quantitative
approach, which takes into account not only genetic
influences, but environmental, developmental and social
influences on compensation, as well as stochastic influ-
ences on fitness variances. In this model, the compen-
satory response is an increase in the number of eggs laid
or offspring born, F. Compensation, which is composed
of sensitivity to inducing stimuli, assessment of fitness
outcomes from mating with alternative potential partners
and responsiveness to individual assessments and to
inducing stimuli, is a metric trait influenced by 20 loci
and 40 alleles, and the strength of compensation is
Reproductive compensation 9
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dependent on the degree of similarity in ?immuno-genes?
of parents (how similar and dissimilar they are) and the
dose of compensation alleles. When access to resources is
held constant as we assume in the model, higher doses of
compensation alleles allow individuals to compensate
more. The degree of required compensation is set by the
difference in shared immuno-genes and the maximum
difference possible. Thus, when individuals have identical
access to resources, being able to compensate more means
that individuals have better assessments of fitness out-
comes, finer sensitivity to inducing stimuli and more
efficient physiological and behaviour mechanisms of
compensation. The individual-based model of fitness
variation of constrained individuals that do and do not
compensate shows that compensation can evolve to
fixation (all individuals are able to compensate) relatively
rapidly under high costs and relatively small benefits. In
the model each individual breeder had an immuno-
genotype. The more variable an individuals? immuno-
genotype the higher was its probability of survival. An
individual?s immuno-genotype when combined with the
immuno-genotype of anymate, influenced the probability
of survival of offspring they produced (there were also
stochastic effects on survival). When individuals mated,
compensation was induced relative to the maximum
possible percent shared parental immuno-genes in the
population, and the degree of compensation was a
function of the number of shared parental immuno-genes
so that those mating pairs with more immuno-genes in
common had offspring with a lower probability of survival
than pairs with dissimilar immuno-genes. Using the
model, we specifically evaluated the ability of compen-
sating individuals to increase fecundity, when breeders
differed in immuno-genes, which determined their
vulnerability to current pathogens, though holding
resource availability constant. We consider our model
conservative because compensation would be expected to
evolve more rapidly when resources vary among individ-
uals, as they do in nature. The cost of compensation was
allowed to vary due to intrinsic (e.g. age, size, previous
breeding experience) differences among individuals. Even
under high costs of compensation (extracted in terms of
breeders? survival probability to the next bout of
reproduction), compensation always evolved to fixation
relatively rapidly, within 200?400 generations.
So, what traits evolve when compensation evolves? As
in other flexibly expressed traits, for individuals to be able
to successfully compensate, they must to be sensitive and
responsive to inducing stimuli. Further, because repro-
ductive compensation assumes comparisons of individual
fitness outcomes, individuals must be able to assess likely
fitness outcomes of mating with alternative potential
mates (no consciousness implied) as well as the likely
fitness of offspring they would produce; i.e. relative to the
offspring of other breeders in the population (see similar
discussion in Gowaty & Hubbell, 2005; unpublished data).
Therefore, traits associatedwith sensitivity and assessment
of inducing stimuli, and responsiveness to stimuli must
evolve in order for compensation to evolve.
Thus, because in theory compensation evolves rapidly
even when costs are high and benefits relatively low, in
this paper, my assumption that all individuals in a
population may compensate, is reasonable. If this is the
case in nature, it means that the most important sources
of variation in expressed compensation and perhaps the
use of alternative compensatory mechanisms depends on
(1) the level of compensation that would approach
productivity (number of offspring that survive to repro-
ductive age) of individuals mating with partners they
prefer and (2) access to resources, which could affect the
level of individual responses and the extractive costs to
survival to the next reproductive bout.
Acknowledgments
I thank Steve Hubbell for constructively critical discus-
sions, for drawing the figures, and for comments on
previous versions of this manuscript. I thank J. P. Drury
for his careful reading and comments of the penultimate
version; John Byers and Geoff Hill for constructive
comments, and Henry Horn for reminding me in early
2005 after my seminar on the reproductive compensation
hypothesis at Princeton that the Rolling Stones song,
?You Can?t Always Get What You Want? was a prescient
statement of the reproductive compensation hypothesis. I
thank Wyatt Anderson and Yong-Kyu Kim for comments
about these ideas during the decade of our on-going
collaborative studies on flies. I first thought about the
reproductive compensation hypothesis in 1994 and
grants from NIH and NSF supported my research. The
motivation for pursuing the work funded in 1996 by NSF
Animal Behavior Grant IBN-9631801 ?Mate choice and
offspring quality? was to test the main assumption of the
reproductive compensation hypothesis about offspring
viability when breeders must make further reproductive
decisions under constraints on the free expression of
their mate preferences. I thank my generous collabora-
tors on that grant for their willingness to proceed despite
their scepticism.
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Received 19 February 2008; revised 29 April 2008; accepted 29 April
2008
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