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A
Alternative Reproductive
Tactics
Carsten Schradin
Université de Strasbourg, CNRS, IPHC UMR
7178, Strasbourg, France
School of Animal, Plant and Environmental
Sciences, University of the Witwatersrand,
Johannesburg, South Africa
Definitions
Strategy A set of decision rules, which has
a genetic basis, leading to a tactic.
Tactic The behavioral phenotype, which
results from a strategy. A strategy
can have one, two, or several
different tactics.
Alternative
reproductive
tactics ARTs
Consistent variation in
reproductive behaviors between
males or females of one species.
Alternative
strategies
Two (or more) genetically based
strategies of one sex that lead to
two (or more) alternative tactics.
Mixed
strategy
One strategy that, depending on
frequency depending selection,
leads to two or more ARTs which
have equal mean fitness.
Conditional
strategy
One strategy which determines
that individuals follows a
subordinate tactic with low
reproductive success while they
are small with low
competitiveness, but switch to a
dominant tactic with high
reproductive success when
increasing competitiveness.
Single
strategy
One strategy with two or more
alternative tactics. The
environment determines which
tactic an individual chooses and
also whether ARTs have different
or same mean fitness. The single
strategy combines the mixed and
the conditional strategy,
emphasizing the importance of
the environment in determining
fitness outcomes.
Bourgeois
tactic
The tactic with the highest
possible fitness.
Best of a bad
job
An individual follows a tactic
with a lower fitness than an
alternative tactic, because it is not
competitive enough to
successfully follow the bourgeois
tactic.
Relative
plasticity
hypothesis
RPH
The RPH is based on the
assumption that differences
between ARTs are similarly
regulated via hormones as are the
differences between the sexes.
© Springer Nature Switzerland AG 2019
J. Vonk, T. K. Shackelford (eds.), Encyclopedia of Animal Cognition and Behavior,
https://doi.org/10.1007/978-3-319-47829-6_322-1
Introduction
Alternative reproductive tactics (ARTs) refer to
the consistent use of different reproductive behav-
iors between conspecifics of the same sex in one
population at the same time. Hereby the difference
between individuals is discontinuous, such that
one can put individuals into two or more catego-
ries. A tactic refers to the behavioral phenotype,
which results from a strategy. A strategy can have
different tactics, e.g., territorial male versus satel-
lite male. If a strategy has only one tactic, then
more than one strategy must be present in the
population for ARTs to be present. It is typically
tactics which are studied, not strategies.
Examples of ARTs in Males and in
Females
ARTs are more common in males than in females,
probably because reproductive success in males is
more skewed than in females. For example, in
species in which a few competitive males monop-
olies the access to fertile females, smaller and less
competitive males might develop best of a bad job
tactics to mate with these females and gain at least
some reproductive success before being big
enough to be a dominant male. If more than one
reproductive tactic occurs in a population, then
ARTs occur. This is basically the case in every
species where apart from bourgeois males (see
below), another type of males occurs that are
trying to fertilize females. In males, the following
tactics have been described:
•Bourgeois male: These are males which follow
the tactic with the highest mean fitness. Thus,
these are the most competitive and most dom-
inant males, which often defend a territory
and/or a group of breeding females (harem).
•Sneakers: These are small males trying to
sneak copulations with females defended by
bourgeois males. Satellite males, roamers, and
floaters are different types of sneaker males.
Sometimes this term is used for roamers and
floaters in reptiles, which means for subordi-
nate males that are not (like satellite males)
associated to a specific territory. Sneaker males
occur in many lizard species such as marine
iguana (Amblyrhynchus cristatus) and tree liz-
ard (Urosaurus ornatus), and in cichlid fish
such as Lamprologus callipterus.
•Satellite males: These males are associated to a
specific territory but do not defend a territory
themselves. They are typically less competitive
and smaller than bourgeois males. They try to
mate with females in the territory they are
associated with. In some species like bluegills
(Lepomis macrochirus), these males have
female mimicry, meaning they look and
behave like females, explaining why the bour-
geois males do not chase them away. Satellite
males occur in many lizard species such as
marine iguana (Amblyrhynchus cristatus) and
tree lizard (Urosaurus ornatus), in tree frogs
and several species of crickets.
•Roamers: This term is usually only used for
mammals. Roamers typically have a well-
defined home range that is very large and over-
laps the home range of several bourgeois males
but not defended as a territory. These males
roam over a large area, trying to avoid the
bourgeois males but to meet and to copulate
with any females they encounter. Example:
African striped mouse (Rhabdomys pumilio).
•Floaters: This term is used mainly for birds and
mammals. Floaters are males that, in contrast to
roamers, do not have a well-defined home range,
but float through the population, trying to copu-
late with females defended by bourgeois males.
Floaters occur in many bird species such as the
red-winged blackbird (Agelaius phoeniceus).
•Helpers: Helpers are males that help a breeding
pair to raise the pair’s offspring i.e., they help
to raise young that are not their own. In many
species, helpers also try to fertilize eggs/
females, either of the pair they are helping
(cichlid Neolamprologus pulcher;piedking-
fisher Ceryle rudis), or of neighboring groups
(African striped mice, meerkats Suricatte
suricata; superb fairy-wrens, Malurus cyaneus).
While ARTs have been mostly studied in
males, female ARTs also occur. This is the case
when the investment of other females such as
2 Alternative Reproductive Tactics
maternal care can be exploited or when females
monopolies the parental investment of males by
forming one female-multiple male groups, mating
polyandreously. As ARTs are alternative ways to
gain fitness via reproduction, alternative mating
tactics, such as monogamous versus polynadreous
mating of females also represent ARTs, but such
alternative mating tactics are difficult to measure
and received little attention. In females, the fol-
lowing ARTs have been described:
•Solitary versus communal breeding in African
striped mice, house mice, and probably many
other small mammals.
•In eusocial insects, workers that are laying
eggs in the nest dominated by a queen.
•In some wasps, females can either join the nest
of another female (communal breeding) or start
their own nest (single breeder).
•Female dunnocks can mate monogamously,
polyandrously, or polygynandrously.
•Fire ants (Solenopsis invicta) females can form
colonies with either one single monogynous
queen or colonies with several breeding females.
Species With and Without
Morphological Differences
Between ARTs
In some species, males following different tactics
do not only differ in their behavior but also in
their morphology. For example, in several lizard
species with ARTs, the different tactics also dif-
fer in the coloration of their skin, such as the
coloration of dewlaps in tree lizards. In species
with genetically determined alternative strate-
gies, males can differ dramatically in size, for
example, in the cichlid fish Lamprologus
callipterus, where bourgeois males are 10 cm
long and weight 36 g, while dwarf males reach
only 2.5 cm and 0.9 g. In some case, such as
dwarf males parasitizing bourgeois males, the
reason for the phenotypic difference is obvious.
In contrast, why male lizards following ARTs
differ in coloration is still not understood, and
this question also received little scientificatten-
tion.ManystudiesonARTSfocusedonsuch
species where the different tactics can easily be
distinguished, as obviously this makes it easier to
study ARTs. However, in the huge majority of
studies, individuals following ARTs differ
mainly in behavior and often additionally to a
small, not always (to the observer) obvious
extent in body mass. Thus, species where ARTs
are also phenotypically different are a
special case.
What Does Not Represent ARTs?
No examples of ARTs are interspecific brood-
parasitism, sex change, simultaneous hermaphro-
ditism, and infanticide (Taborsky 2008). In many
species, each male might have different tactics to
fertilize females, without these representing
ARTs. For example, in most passerine birds,
males are pair-living, copulating with their female
partner, and additionally seeking to copulate with
neighboring females to gain extra-pair paternity.
As all males follow this strategy, it does not rep-
resent ARTs, as there is no consistent variation
between males. However, if it would be shown in
one species that some males invest heavily in
guarding their mate and not in extra-pair copula-
tions, while other males don’t invest in mate
guarding but in extra-pair copulations, then this
consistent variation would represent ARTs.
Alternative tactics can also occur in other
behaviors than reproduction. For example, alter-
native dispersal tactics have been described in
African striped mice (Rhabdomys pumilio),
where the largest males disperse over short dis-
tances (less than 500 meters), intermediate males
over large distances (several kms), and small
males not at all (Solmsen et al. 2011). While
these alternative dispersal tactics are correlated
with ARTs (territorial male versus roaming male
versus philopatric males), they do not represent
ARTs themselves but rather a tactic of males of
intermediate body mass to reach the high fitness
tactic of territorial male in a distant subpopulation
instead of becoming a roamer in the natal popula-
tion. Similar alternative tactics that are not repro-
ductive tactics can occur for different foraging
strategies.
Alternative Reproductive Tactics 3
The occurrence of an alternative male (or female)
morph that does not reproduce is not regarded as
ARTs. Thus, traditionally cooperatively breeding
species with nonbreeding helpers have not been
considered as examples of ARTs. However, more
detailed studies often found that helpers might breed
when the opportunity arises, without changing their
social status. Examples for this are female workers
of many hymenopterans, male helpers in meerkats,
in striped mice and in superb fairy-wrens, and
helpers of both sexes in the cichlid Neolamprologus
pulcher.
Strategies Underlying ARTs
It is important to differentiate between the observed
tactic and the underlying strategy (Gross 1996).
A strategy refers to decision rules which determine
which alternative tactic is shown. A strategy has a
strong genetic basic but is not totally genetically
fixed, as there is variation between individuals, for
example, when exactly to switch from one tactic to
another. The strategy is determined by specific
mechanisms which are a response to environmental
cues. An example for a strategy might be the fol-
lowing decision rule: If you are larger than X,
increase your testosterone level and become a terri-
torial male, otherwise be a satellite male.
It has been stated that the differentiation
between strategies and tactics is not useful as
both relate to the same issue (Taborsky 2008).
However, the differentiation between strategy
and tactic can be very important, as it clearly
indicates one shortcoming in our understanding
of ARTs: Nearly all research has focused on the
tactics themselves, i.e., the fitness consequences
and the underlying endocrine mechanisms leading
to ARTs (all the rest of the current article reviews
this), while the underlying strategies have been
ignored. Thus, for most species showing ARTs the
underlying decision rules have never been esti-
mated, tested, and validated. However, formulat-
ing these decisions rules can help us with coming
up with better and more meaningful predictions,
for example, about the expected fitness conse-
quences of ARTs. On the other hand, if no clear
set of decision rules (a strategy) can be
formulated, this indicates a lack in our under-
standing of the ARTs of this specific species.
For male African striped mice, it has been
proposed that they have one strategy, the decision
rules of which determines which of the three pos-
sible ARTs a male follows, while the environment
determines the fitness outcomes (Schradin and
Lindholm 2011):
1. Decision: To remain philopatric to your natal
group or to disperse?
(a) Remain a philopatric male if all females
breed in communal groups defended by
breeding males and your body mass is
below the population mean and there are
more sexually mature males than female
groups in the population. Mate with any
female from neighboring groups.
(b) Leave your natal group if:
(i) At any time of the year, a breeding
position becomes vacant in a neigh-
boring group which you can fill.
(ii) At the beginning of the breeding sea-
son if population density is low and
several single undefended females
are present in the population which
has a female biased sex ratio.
(iii) At the beginning of the breeding sea-
son if your body mass is above the
mean of the population, independent
of population density.
2. Decision: To become a roamer or try to become
a territorial breeder?
(a) If all female breed solitarily then become a
roaming male.
(b) If you find a group of communally breed-
ing females that are not defended by a male
that is larger than you then become the
breeding male of this group, defend the
territory of this group against other males,
and try to copulate with all your females
plus all females from neighboring groups.
This set of decision rules makes clear that
being a roamer can be the result of two different
processes: (1) an active choice, because many
females breed solitarily and roaming is the best
tactic or as good as being a territorial breeder.
4 Alternative Reproductive Tactics
(2) Result of low competitive ability, i.e., the male
chose to disperse and would choose to become a
territorial breeder, but he cannot, because all com-
munal female groups are defended by larger
males. This is similar to the situation in stoplight
parrotfish (Sparisoma viridae) where males start
with the tactic of bachelor and the availability of
free territories and their relative body size deter-
mines when they can switch to the territorial tactic
(Cardwell and Liley 1991).
Development and ARTs
The tactic an individual follows to have reproduc-
tive success develops during its life and can
change during development (Fig. 1). Obviously,
the time point when an individual reaches sexual
maturity is important for the expression of its
reproductive tactic. In species where the
reproductive tactic is genetically fixed, the tactic
that an individual will follow throughout its life
will then be expressed. If depending on the geno-
type two or more alternative tactics might be
expressed, then we observe ARTs in this popula-
tion (Fig. 1, top). In other species, it’s the envi-
ronment that determine which of two (or more)
ARTs is expressed (Fig. 1, middle). However,
especially in males, whether or not individuals
can reproduce not only depends on when it
reaches sexual maturity but also on its competi-
tiveness, for which body mass is often a very good
proxy. Large dominant males might reproduce,
while small males, even though sexually mature,
might have to wait and grow, possibly forming
bachelor groups of nonbreeding males or
remaining as nonbreeding subordinate males in a
group.
There is strong selection pressure on individuals
to reproduce, and accordingly in many species
Developmental (fixed) plasticity
Developmental (genetically fixed) sequence
Flexibility (reversible plasticity)
Genetically fixed
Plasticity
One
genotype
Two
genotypes
Alternative Reproductive Tactics, Fig. 1 A simplified
overview of the different pathways that can lead to ARTs,
adapted from (Taborsky 2008). Top: ARTs can arise out of
two (or more) different main genotypes determining which
of the alternative tactics is expressed in each individual.
Middle: One genotype can lead to ARTs via nonreversible
developmental plasticity, where one out of two (or more)
alternative pathways leading to ARTs is chosen. Empirical
evidence for his mechanism leading to ARTs is missing. In
contrast, most cases of ARTs are due to flexibility, i.e.,
reversible phenotypic plasticity, for example, many cases
where males follow either a best of a bad job or a bourgeois
tactic, depending on their relative competitiveness. In
some tree frogs, the biggest males are calling, smaller
males are satellites, but when bigger males arrive/disap-
pear, males can immediately switch their tactic, and later
can switch again. Bottom: One main genotype can lead to
ARTs when individuals follow different tactics during their
development, for example, following a doing the best of a
bad tactic as young small adults, and changing to the
bourgeois tactic when older and more competitive
Alternative Reproductive Tactics 5
subordinate males are trying to mate with females,
even when being small and dominated by larger
males that try to monopolies access to receptive
females. Such small males might follow a best of a
bad job tactic, often called satellite or sneaker tactic,
until they become larger and can follow the domi-
nant bourgeois tactic (Fig. 1, bottom). In these spe-
cies, which tactic is followed is mainly determined
by growth after reaching adulthood, and as such
determined by development during adulthood.
While some authors do not regard such develop-
ment dependent tactics as ARTs, they clearly are, as
we need (1) ultimate explanations for the occurrence
of such best of a bad job tactics which are (2) con-
trolled by specific endocrine mechanisms, which
evolved to maximize lifetime reproductive success.
Tactics can be genetically fixed or plastic
(Fig. 1). Within the plastic tactics, developmental
plasticity might lead permanently to one out of
several alternative tactics, which the individual
then cannot change anymore. The sequence of
tactics might also be developmentally fixed, for
example, from small sneaker to large bourgeois
male, as described above. However, in many spe-
cies, individuals can flexibly change their repro-
ductive tactic repeatedly. This is also a form of
plasticity, which in contrast to fixed developmen-
tal plasticity is called flexibility.
Evolution of Strategies Underlying ARTs
The phenomenon of alternative reproductive tac-
tics has been analyzed by game theory, where a
tactic refers to a specific behavior resulting from
individual decision rules, so-called strategies.
Reproductive tactics have a strong influence on
individual fitness and are thus under strong selec-
tion pressure. However, it is rather the underlying
strategies, i.e., developmental and cognitive deci-
sion rules that evolve and then produce the
observed tactics. In a classical paper, Gross
(1996)defined three categories of strategies
(Fig. 2):
1. Alternative strategies: Genetically polymor-
phic, based on frequency-dependent selection.
Different tactics yield the same average fitness.
Examples are giant versus dwarf males of the
cichlid fish Lamprologus callipterus. Alterna-
tive strategies are represented by genetically
fixed tactics in Fig. 1.
2. Mixed strategies: Genetically monomorphic,
based on frequency-dependent selection. Dif-
ferent tactics yield the same average fitness. No
good empirical examples exist. Mixed strate-
gies have also been characterized by a proba-
bilistic basis, i.e., a probability x to play tactic
X and probability 1-x to play tactic Y. These
represent developmental fixed plastic tactics in
Fig. 1, where tactics have the same average
fitness and the chosen tactic then depends on
the frequency of all tactics in the population.
3. Conditional strategies: Genetically monomor-
phic, based on status-dependent selection. Dif-
ferent tactics yield different fitness. The tactic
that an individual chooses depends on its com-
petitive abilities. The most competitive indi-
viduals follow the tactic that yields the
highest fitness payoff, called the bourgeois
tactic. Less competitive males (often called
sneaker or satellite), that are smaller and youn-
ger than the bourgeois males, make the best of
a bad job, following a tactic with lower fitness
that is still better than no reproductive success
at all. These males change to the bourgeois
tactic when they grow larger. Many examples
exist in both vertebrates and invertebrates.
These represent flexible (reversible plasticity)
and developmental sequenced tactics in Fig. 1.
Empirical studies on the African striped mouse
revealed that fitness consequences of ARTs can be
environment dependent. Male striped mice follow
one of three ARTs: (1) Territorial breeding males
defend a group of communally breeding females;
(2) Solitary roaming males trying to copulate with
any females they encounter; (3) Philopatric males
that remain in their natal group and try to sneak
copulations with females from neighboring
groups. Under high population density, breeding
males have 10 times higher reproductive success
than roamers and 100 times higher reproductive
success than philopatrics. However, under inter-
mediate population density, breeding males and
6 Alternative Reproductive Tactics
roamers have the same mean fitness, and no
philopatrics occur (as all sexually mature males
leave their natal group). Under very low popula-
tion density, all males follow a roaming tactic,
and some of these roamers have a very high
reproductive success, higher than that of
breeders under high population densities. These
observations lead to the formulation of the single
strategy, which contains both the mixed and the
conditional strategy proposed by Gross (1996;
Fig. 2).
The single strategy is a new term introduced by
Schradin and Lindholm (2011) to replace the terms
mixed and conditional strategy, which differ mainly
in the predicted fitness consequences (equal fitness
for mixed versus different fitness payoffs for tactics
arising from conditional strategies). Single strategies
are not based on genetic polymorphisms, but all
individuals follow the same or very similar decision
rules when choosing a tactic. Individuals have flex-
ible tactics, which means they can switch tactics,
often repeatedly. Environmental conditions deter-
mine whether the different tactics yield similar or
different fitness. By formulating the single strategy
(=decision rules; see above) for striped mice, it
became evident that fitness outcomes depend on
the prevailing environment. To become a roamer
can be the result of a male choosing to disperse
and to roam, as the tactic yields high fitness. Alter-
natively, it can be the result of a male choosing to
disperse and attempts to become a territorial breeder
but not being competitive enough to do so. In the
latter case, being a roamer would be a best of a bad
job tactic.
The definitions by Gross (1996) have been
criticized on theoretical grounds because of its
focus on genetic polymorphism versus genetic
monomorphism: even if different animals follow
very similar decisions rules and show flexibility,
i.e., they can change between tactics, they still
might differ genetically, e.g., in their decision
when to switch tactics (Shuster and Wade 2003).
Alternative Strategies
Genetic
Monomorphism
Frequency
depending selection
One strategy with
different tactics of the
same fitness
Genetic
Monomorphism
Status depending
selection
One strategy with
different tactics of
different fitness
Mixed Strategy C
onditional
Strategy
Genetic
polymorphism
Frequency
depending selection
Two or more
strategies with the
same
fitness.
Alternative Reproductive Tactics, Fig. 2 Bottom: Tra-
ditional categorization of reproductive strategies (decision
rules leading to tactics) by Gross (1996) and top modified
by Schradin and Lindholm (2011). Differences between
strategies refer to whether the shown tactic is genetically
fixed (Alternative Strategies) or not (all other strategies).
While Gross (1996) further differentiated whether the fit-
ness of ARTs is similar (Mixed Strategies) or different
(Conditional Strategies), Schradin and Lindholm (2011),
see the fitness outcome as variable depending on the cur-
rent environmental conditions (Single Strategy)
Alternative Reproductive Tactics 7
(Tomkins and Hazel 2007) further concluded that
mathematical models can neither prove that fit-
ness must be unequal (as was proposed by Gross
1996) nor that fitness must be equal (as was pro-
posed by Shuster and Wade 2003).
Endocrine Mechanisms of ARTs
The relative plasticity hypothesis (RPH) has been
developed to explain the endocrine mechanisms
underlying ARTs (Moore 1991). The RPH bases
on the theoretical assumption that individuals of
one sex that follow ARTs differ in their hormonal
mechanisms in a similar way as is observed in
primary sex differentiation between males and
females (Moore 1991; Moore et al. 1998). Thus,
in the same way as males and females differ hor-
monally, males of different reproductive tactics
are also expected to differ hormonally. Hormones
can influence behavior via two main ways
(Phoenix et al. 1959): (1) Early in life, hormones
can have organizational effects that permanently
change the central nervous system and as such
adult behavior. Organizational effects are non-
reversible. For example, male rodents that experi-
ence high levels of testosterone in utero will be
more aggressive when being adult. (2) During
adulthood, hormones have activational effects,
acting on the central nervous system (which was
formed via organizational effects during early
development), making the expression of specific
behaviors more likely. Activational effects are
reversible, i.e., when the hormone secretion
decrease, the behavior ceases. An example
would be singing in song birds, which is activated
by testosterone in spring and ceases in summer/
autumn when testosterone levels decrease.
The RPH predicts that individuals following
fixed ARTS differ in their hormone profiles early
in development (organizational effects; Table 1).
In contrast, when ARTs are sequential or flexible,
individuals following different ARTs are pre-
dicted to differ in hormone profiles in adulthood
(activational effects; Table 1). The main hormones
involved in the regulation of male ARTs are andro-
gens, such as testosterone. Bourgeois males typi-
cally have higher androgen levels than other males.
Progesterone and glucocorticoids are other hor-
mones that can be involved in the regulation of
ARTs. While originally the RPH was formulated
for these steroid hormones only, it is now known
that peptide hormones such as prolactin and neu-
ropeptides (oxytocin and vasopressin) can also be
involved. Figure 3shows as an example of how
hormone levels differ in male striped mice follow-
ing ARTs. In this species, it has also been shown
that males of the different tactics do not only differ
in their endocrine profile but also that individual
males change their hormone levels when
switching tactics, and that experimental increase
of testosterone might induce tactic change.
Alternative Reproductive Tactics, Table 1 The hor-
mone profile of males following ARTs as predicted by the
RPH (Moore et al. 1998) and a revised version of the RPH
which I suggest here. ACT: Activational effects leading to
different ARTs. ORG: Organizational effects leading to
different ARTs. PHYS: Physiological effects resulting
from different ARTs
ART type Relative plasticity hypothesis by Moore 1998 Modified relative plasticity hypothesis
Fixed ORG: Hormonal differences in early development.
Adults have similar hormone profiles, except when
affected by different social experiences
ORG: Hormonal differences in early
development.
PHYS: Hormonal differences between ARTs
(adults) are similar to differences observed
between sexes.
Sequential ORG: Hormonal differences in adults when ARTs
are formed. Otherwise hormone profiles are similar
ORG: Hormonal differences during adulthood
when ARTs are formed
PHYS: Hormone levels should differ between
ARTs
Reversible ACT: Adult morphs will always differ in their
hormone profile, but no differences in early
development
ACT: Hormone levels should differ between
ARTs
8 Alternative Reproductive Tactics
Furthermore, this has consequences for their
metabolism, as resting metabolic rate (metabolic
rate to maintain basal functions only, measured as
oxygen consumption when being at rest at
thermoneutrality) also differs between ARTs.
The endocrinology of ARTs has been investi-
gated in more than 50 vertebrate species, espe-
cially in fish and reptiles, but also in birds and
mammals, and a role of hormones in regulating
ARTs has been reported in nearly every study
(reviewed in Oliveira et al. 2008). However, the
support for the predictions of the RPH has been
low, both for correlative and experimental studies.
Oliveira et al. (2008) concluded that the RPH fails
to explain a large amount of the observed varia-
tion and thus reject the validity of the RPH. Spe-
cifically, the existence of hormonal differences in
adults of species with fixed ARTs, and an effect of
hormone manipulations in adults with fixed ARTs
has led to a rejection of the RPH (Oliveira et al.
2008). However, these problems arise mainly
from two facts that should be taken into account
when considering the RPH (Table 2): (1) As the
RPH is based on the comparison between the male
and female sex, it does not predict that males of
two fixed ARTs should only differ hormonally
during development but not during adulthood. In
the same way, as males and females (fixed repro-
ductive tactics in most vertebrates) differ in their
hormonal profile, the same can be expected for
two ARTs in one sex. (2) The prediction that
hormone manipulations should have an effect in
early development in species with fixed ARTs and
an effect in adults of species with plastic ARTs has
been interpreted to mean it should otherwise have
no effect. However, even in males of species with
no ARTs, experimentally administering testoster-
one can have strong effects, such that the extracted
conclusion it should not have an effect in species
with fixed ARTs is not understandable. Further,
some species with plastic ARTs cannot change
their tactic at any stage, but only seasonally, for
example, from one breeding season to the next
(some blennies, a form of marine fish). Blennies
Cort ↓
T↑
PRL↔
RMR ↑
Cort ↔
T ↓
PRL ↑
RMR ↓
Cort ↓
T↑
PRL↑
RMR↔
Cort ↓
T↑
PRL↔
RMR ↑
Juvenile Breeder
Alternative Reproductive Tactics, Fig. 3 Physiological
change in male striped mice, which when reaching adult-
hood (not gray) can either remain as adult philopatric in
their natal group (blue), become a solitary living roamer
(black), or the breeding male of another group than their
natal group (red). These switches in tactics are associated
with changes in physiology, and it has been shown that
individual males change their physiological profile when
changing tactic. Cort corticosterone, PRL prolactin, RMR
resting metabolic rate, Ttestosterone, #decrease, "
increase, =does not change
Alternative Reproductive Tactics 9
with ARTs do not only show tactic specific behav-
ior but also tactic specific morphology, which is
difficult to change. Here, the effect of hormone
manipulation might be dependent on the time of
year, and experiments done during the breeding
season (when the tactic for the season is already
fixed) might be less meaningful than in the pre-
breeding season. In sum, when taking into
account physiological effects resulting from dif-
ferent ARTs and artificial effects that do not imply
a natural mechanistic pathway, then the RPH is
still highly valuable in understanding the endo-
crine control of ARTs.
I therefore suggest a modified version of the
RPH, which takes two facts into account: (1) Phys-
iological differences are expected in fixed ARTs in
adulthood in the same way as hormonal differ-
ences are observed between males and females in
most species (Table 1). (2) Experimental changes
of hormones, potent mediators of physiology and
behavior, can cause artificial effects on physiol-
ogy and behavior that are not observed under
natural conditions, as the imposed hormonal
changes (for example, artificially high testoster-
one levels) also do not occur under natural condi-
tions (Table 2).
In sum, the expression of fixed ARTs is regu-
lated by permanent organizational effects during
development which can then also lead to perma-
nent differences of hormone profiles in adults. In
species with plastic ARTs, the transition from one
tactic to another tactic is associated with changes
in the hormone profile, representing activational
(reversible) endocrine effects. For example,
androgen levels typically increase and glucocorti-
coid levels decrease when males switch from a
sneaker to the bourgeois tactic.
ARTs and Intraspecific Variation in Social
Organization
Intraspecific variation in social organization
(IVSO) occurs when a species shows two or
more of the following forms of social organiza-
tion: living solitarily, in pairs, one breeding male
with several breeding females, one breeding
female with several breeding males, or multi-
male multi-female groups. Hereby, each form of
social organization must be composed of breeding
individuals, not only dispersing solitary individ-
uals or bachelor groups. Thus, each sex must have
the option to live under alternative forms of social
organization. IVSO becomes obvious when indi-
viduals of both sexes change their reproductive
tactics. In other words, if in one species both
males and females can show ARTs, then this can
lead to IVSO. For example, the house mouse (Mus
musculus) can live solitarily, in pairs or in com-
munal groups, with resource availability modify-
ing the intensity of intrasexual aggression in
males and female infanticide. In striped mice,
Alternative Reproductive Tactics, Table 2 Predicted
effects of experimental manipulations of hormones in males
following ARTs as predicted by the RPH (Moore et al.
1998), and a revised version of the RPH which I suggest
here. ACT: Activational effects leading to different ARTs.
ORG: Organizational effects leading to different ARTs.
ARTI: Artificial effects that do not imply an evolved endo-
crine pathway that would occur under natural conditions
ART type
Relative plasticity hypothesis by
Moore et al. 1998 Modified relative plasticity hypothesis
Fixed ORG: Effective during early
development, but not in adults
ORG: Effects in early development long-lasting and similar to
effects observed in nature
ARTI ACT: Effects in adults short-lasting and similar or different
to observed differences between ARTs
Sequential ORG: Effective in adults but not
during early development
ORG: Effective in adults when ARTs are formed, long-lasting
and similar to effects observed in nature
ARTI ACT: Effects in final ART in adults short-lasting and
similar to observed differences between ARTs
Reversible ACT: Effective in adults but not
during early development
ACT: Effective in adults but not during early development
10 Alternative Reproductive Tactics
both sexes show ARTs, and both sexes can live
solitarily or in groups. Thus, solitary living or
living in large communally breeding groups
consisting of one male and two to four breeding
females can occur. In sum, when both males and
females show ARTs, both sexes can live in differ-
ent forms of social organization, which is called
intraspecific variation in social organization.
Conclusion
When different individuals of one sex follow dif-
ferent tactics to reach reproductive success, this
represents an interesting phenomenon for all stu-
dents of animal behavior, both those interested in
the evolution and those interested in the physiol-
ogy and mechanisms of behavior. Such ARTs
occur in both sexes though they seem to be more
common in males and are clearly understudied in
females. ARTs can evolve when either the alter-
native tactics yield the same average fitness, or if
following a suboptimal tactic allows individuals
to increase their lifetime reproductive success by
having some, even if low, fitness when being
subordinate, waiting to grow and increase com-
petitiveness before adopting the bourgeois tactic
with the highest reproductive success. The expres-
sion of ARTs is regulated by the endocrine sys-
tem. Permanent organizational effects (typically
early in development) cause fixed tactics, revers-
ible activational effects in adulthood cause
switches in plastic tactics. If ARTs occur in both
sexes, the social organization of an entire popula-
tion can change, causing intraspecific variation in
social organization. In sum, ARTs represent an
interesting phenomenon that allows us to study
the proximate causes and ultimate consequences
of different behavioral (and sometimes also mor-
phological) phenotypes within one single species.
Cross-References
▶Adaptation
▶Behavioral Flexibility
▶Development of Behavior
▶Ecology
▶Evolution
▶Natural Selection
▶Ontogeny
▶Proximate Causation
▶Reproductive Fitness
▶Social Behavior
▶Ultimate Causation
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