Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
Review
Social modulation of androgen levels in male teleost fish夞
Rui F. Oliveiraa,*, Katharina Hirschenhausera, Luis A. Carneiroa, Adelino V.M. Canariob
a
¸ ˜ em Eco-Etologia, Instituto Superior de Psicologia Aplicada, R. Jardim do Tabaco 34, 1149-041 Lisboa,
Unidade de Investigacao
Portugal
b
ˆ
Centro de Ciencias
do Mar, Universidade do Algarve, Campus de Gambelas, 8000-810 Faro, Portugal
Received 27 January 2001; received in revised form 1 May 2001; accepted 11 May 2001
Abstract
Androgens are classically thought of as the sex steroids controlling male reproduction. However, in recent years
evidence has accumulated showing that androgens can also be affected by the interactions between conspecifics,
suggesting reciprocal interactions between androgens and behaviour. These results have been interpreted as an adaptation
for individuals to adjust their agonistic motivation and to cope with changes in their social environment. Thus, male–
male interactions would stimulate the production of androgens, and the levels of androgens would be a function of the
stability of its social environment w‘challenge hypothesis’, Gen. Comp. Endocrinol. 56 (1984) 417x. Here the available
data on social modulation of androgen levels in male teleosts are reviewed and some predictions of the challenge
hypothesis are addressed using teleosts as a study model. We investigate the causal link between social status, territoriality
and elevated androgen levels and the available evidence suggests that the social environment indeed modulates the
endocrine axis of teleosts. The association between higher androgen levels and social rank emerges mainly in periods of
social instability. As reported in the avian literature, in teleosts the trade-off between androgens and parental care is
indicated by the fact that during the parental phase breeding males decreased their androgen levels. A comparison of
androgen responsiveness between teleost species with different mating and parenting systems also reveals that parenting
explains the variation observed in androgen responsiveness to a higher degree than the mating strategy. Finally, the
adaptive value of social modulation of androgens and some of its evolutionary consequences are discussed. 䊚 2002
Elsevier Science Inc. All rights reserved.
Keywords: Androgens; Behaviour; Challenge hypothesis; Mating system; Parental care; Social modulation; Teleost fish
1. Social modulation of male androgen levels:
the challenge hypothesis
Androgens are among the main hormones
involved in male reproduction in vertebrates.
夞 This paper was submitted as part of the proceedings of
the 20th Conference of European Comparative Endocrinologists, organised under the auspices of the European Society of
Comparative Endocrinology, held in Faro, Portugal, September
5–9, 2000.
*Corresponding author. Fax: q351-21-88-60-954.
E-mail address: ruiol@ispa.pt (R.F. Oliveira).
Extensive evidence suggests a role for androgens
in spermatogenesis, in the development of secondary sex characters, and in the expression of reproductive behaviours (for a review see Nelson,
1994). Many studies in different vertebrate groups
have shown the activational (or permissive) role
of androgens in the expression of male social
behaviours, both sexual and aggressive. However,
in recent years evidence has accumulated showing
that androgens are not only a causal factor for
reproductive behaviours but that they may also be
1096-4959/02/$ - see front matter 䊚 2002 Elsevier Science Inc. All rights reserved.
PII: S 1 0 9 6 - 4 9 5 9 Ž 0 1 . 0 0 5 2 3 - 1
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R.F. Oliveira et al. / Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
affected by the interactions between conspecifics
suggesting a two-way relationship between androgens and behaviour (Villars, 1983).
Several studies have shown effects of social
interactions on the short-term modulation of androgen circulating levels. For example, in mammalian
males (including humans) copulation induces a
rise in the circulating levels of testosterone (T)
and luteinising hormone (LH) (Harding, 1981).
Furthermore, in rodents simple exposure to a
female or to her odour is sufficient to activate this
response (Harding, 1981). In teleost fishes male
salmonids, for example, show a rise in sex steroid
and gonadotrophin levels and an increase in milt
production in the presence of ovulated females
(Liley et al., 1986, 1993; Rouger and Liley, 1993).
Anosmic males in the presence of sexually active
females have lower levels of sex steroids and a
lower sperm production than males with intact
olfactory epithelium, which suggests that chemical
signals may play an important role in this social
modulation of hormone levels. In cichlid fishes
(e.g. Oreochromis mossambicus) males are sensitive to the maturation stage of females, courting
more intensively ovulated females (Silverman,
1978) This effect also seems to be mediated by
chemical signals emitted by receptive females
(Falter and Dolisy, 1989). Male cichlids also
experience a rise in 11-ketotestosterone (KT) in
response to courtship interactions (Borges et al.,
1998).
Agonistic interactions and male–male competition may also induce an endocrine response in the
participating individuals, a response especially sensitive with respect to androgens. In different vertebrate groups, including humans, short-term
fluctuations of androgen concentrations have been
shown to be related to social interactions (Harding
and Follett, 1979; Eberhart et al., 1980; Harding,
¨
1981; Hannes, 1984; Sachser and Prove,
1984;
Hannes, 1986; Sapolsky, 1987; Wingfield and
Moore, 1987; Booth et al., 1989; Greenberg and
Crews, 1990; Cardwell and Liley, 1991; Oliveira
et al., 2001c). However, some studies have also
demonstrated that in some cases the levels of
aggression and the circulating androgen concentrations are seasonally dissociated (e.g. Dittami and
Reyer, 1984; Wingfield and Ramenofsky, 1985;
Logan and Wingfield, 1990). It seems as if correlations between androgens and agonistic behaviour
are stronger in periods of social instability (challenge), as is the case in the establishment of
dominance hierarchies, the foundation of a new
territory, the response to territorial intrusions or
the active competition with other males for access
to females (teleosts: Cardwell and Liley, 1991;
Pankhurst and Barnett, 1993; reptiles: Moore,
1986, 1988; aves: Ramenofsky, 1984; Wingfield
and Ramenofsky, 1985; Wingfield et al., 1987). In
contrast, during periods of social stability the
levels of aggression drop to a breeding baseline
and dissociation between androgens and aggression
may occur.
These results have been interpreted as an adaptive adjustment of the individual agonistic response
to changes in the social environment. Thus, male–
male interactions would stimulate the production
of androgens and the levels of androgens would
be a function of the stability of the social environment in which the animal was at that time. This
hypothesis was first proposed by Wingfield
(1984a,b) and is currently known as the ‘challenge
hypothesis’ (see also Wingfield et al., 1987, 1990).
The challenge hypothesis postulates that at the
beginning of the breeding season androgen levels
rise from a non-breeding baseline to a higher
breeding baseline that is sufficient for reproduction
(i.e. gametogenesis, the expression of secondary
sexual characters, and the performance of reproductive behaviour). In response to environmental
stimuli such as male–male interactions and the
presence of receptive females, androgen levels can
further increase until they reach a maximum physiological level.
This hypothesis has the merit of creating a
conceptual framework for the study of social
modulation of androgen levels in vertebrates. A
number of predictions can, thus, be generated from
the challenge hypothesis (Wingfield et al., 1990,
2000). In the present paper some of the predictions
of the challenge hypothesis will be revisited using
the available data to test its validity in teleost fish.
This will be followed by a discussion of the
evolutionary implications of the challenge
hypothesis.
2. Androgen levels, territorial intrusions and
social status acquisition
A first prediction of the challenge hypothesis is
that during territory establishment the levels of
androgens should be higher than in the subsequent
phase of territoriality when the territories are
already established (Hegner and Wingfield, 1987a;
R.F. Oliveira et al. / Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
205
Table 1
Comparison of androgen levels between territorialydominant and non-territorialysubordinate males of different teleost species
Species (Family)
Study type
(field vs. lab)
Testosterone
11-Ketotestosterone
Author
Sparisoma viride
(Scaridae)
Oreochromis mossambicus
(Cichlidae)
Field
T)NT
T)NT
Cardwell and Liley, 1991
Lab (group
formation)
Lab (dyadic
encounters)
Lab (groups)
D)S
D)S
Oliveira et al., 1996
DsS
DsS
Neat and Mayer, 1999
T)NT
T)NT
Francis and Fernald, 1993
Lab
DsS
ND
Lab (spawning
groups)
Lab (small groups)
D)S
D)S
Hannes, 1984?
Hannes, 1986
Liley and Kroon, 1995
D)S
ND
Cardwell et al., 1996
Field
D)S
DsS
Cardwell et al., 1996
Field
DsS
DsS
Cardwell et al., 1996
Lab (dyadic encounters)
D)S
D)S
Elofsson et al., 2000
Tilapia zilli
(Cichlidae)
Haplochromis burtoni
(Cichlidae)
Xiphophorus helleri
(Poeciliidae)
Oncorhynchus mykiss
(Salmonidae)
Onchorhynchus mykiss
(Salmonidae)
Salmo trutta
(Salmonidae)
Salvelinus fontinalis
(Salmonidae)
Salvelinus alpinus
(Salmonidae)
T, territorial; NT, non-territorial; D, dominant; S, subordinate. ), indicates significantly higher hormone levels; s, indicates no
significant differences in hormone levels; ND, not determined.
Wingfield et al., 1990). Moreover, since territorialydominant males have to defend their territories
it would also be expected that they will have
higher androgen levels than non-territorialysubordinate males, which do not have to defend their
social status.
In teleost fish we are aware of only one study
where the effects of experimental territorial intrusions on androgen levels have been tested. In a
natural population of the stoplight parrotfish (Sparisoma viride) Cardwell and Liley (1991) found
that peaks of androgens could be induced in
established territorial males by experimental intrusions of other males. Nevertheless, the prediction
that territorial intrusions increase androgen levels
can also be tested indirectly by comparing breeding
populations of the same species but with different
densities, since the probability of a territorial male
suffering a territorial intrusion should be higher in
more dense populations. This extended prediction
should be taken with caution since there may be
situations where the increase in population density
is accompanied by the expression of mechanisms
to avoid aggression. In any case, a positive correlation between density of breeding territories, the
number of agonistic interactions and higher levels
of androgens has already been demonstrated both
in birds and teleosts (birds: Ball and Wingfield,
1987; Beletsky et al., 1990, 1992; teleosts: Pankhurst and Barnett, 1993; Oliveira et al., 2001c).
There are more studies available on the relationship between social status and androgen levels in
male teleosts. As a general rule these studies show
that territorialydominant individuals have higher
androgen levels than non-territorialsysubordinates
(Table 1).
The causality of the interaction between androgen levels and territorialityydominance may be
viewed in two ways: (a) androgen levels are the
predictors of social status; or (b) social status itself
is the cause and not the consequence of higher
androgen levels. In trying to disentangle these two
hypotheses Oliveira et al. (1996) computed correlations between androgen levels and a social
dominance index before and after group formation
in the cichlid fish Oreochromis mossambicus. The
rationale behind this experiment was that if androgen levels are the determining factors of social
status acquisition then it would be expected that
androgen levels before group formation would be
good predictors of the social status that the individuals would acquire after group formation. In
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R.F. Oliveira et al. / Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
contrast, if androgen levels were a response to the
acquired social status it would be predicted that
only after group formation the correlation between
androgen levels and social status would be present.
Oliveira et al. (1996) found that the latter hypothesis was the one supported by the data, which
showed a lack of correlation between the androgen
levels (both T and KT) prior to group formation
and the social status achieved, but strong correlations between androgen levels (both T and KT)
measured after group formation and the acquired
social status.
Thus, the associations found between androgen
levels and social status in male teleosts may
potentially be explained by the challenge hypothesis, reflecting a more challenging social environment for territorialydominant males than for
non-territorialysubordinate ones. Moreover, androgens do not play an activational role in social
status acquisition. Further studies employing temporal correlations or induced social status reversal
will be needed to get a clear picture of the causal
link between androgens and social status in teleost
fish.
In dyadic interactions of the swordtail fish
(Xiphophorus helleri) there was an association
between some aspects of aggressive behaviour and
high levels of androgens (Hannes, 1986). However, when androgen levels of dominant and of
subordinate males from a socially stable community tank were compared, a relationship between
dominance and androgens was not found (Hannes,
1984). Taken together these two studies are consistent with the suggestion that a causal relationship between androgens and the expression of
aggression is only present in periods of social
challenge. In conclusion, we would predict that
the association between androgen levels and social
status should only emerge at periods of social
instability and that in stable social groups androgen
levels become dissociated from social status.
spring. Therefore, the trade-off between territorial
aggressiveness and paternal care seems to be mediated by androgens. This is supported by observations in many monogamous bird species with male
parental care where the experimental increase of
testosterone in parental males suppresses paternal
behaviour and increases aggression (e.g. Silverin,
1980; Hegner and Wingfield, 1987b; Ketterson et
al., 1992). Moreover, several studies on the seasonal patterns of biparentalypaternal temperate
zone birds have shown higher androgen levels at
the beginning of the breeding season when territories are being established and when courtship is
more intense, than in the subsequent paternal
phases (e.g. Wingfield et al., 1987).
We have gathered published androgen data from
paternal teleost species in order to compare the
(mean) androgen levels at mating with those
during parenting phases (Table 2). For all the
species included androgen levels dropped during
parental care in agreement with the above-mentioned prediction. It may be argued that the drop
of androgen levels in the parenting phase is due
to physiological changes associated with the end
of sperm production. In fact, androgen levels also
drop after spawning in a male salmonid, which
provides no paternal care (e.g. Liley et al., 1986).
However, the trade-off seems to be present even
in species in which there is an overlap of the
mating and parenting phase as is the case in
blenniid species. Blenniids have exclusive paternal
care: the males get a first clutch of eggs in their
nests and, while guarding and fanning the eggs,
keep on courting females. Males that have recently
received a clutch in their nest and, thus, are
actively parenting have significantly lower androgen levels than other nest-holder males that did
not have a female spawning in their nests recently
(Oliveira et al., 2001b).
3. Trade-off between territoriality and paternal
care
A third prediction of the challenge hypothesis
is that male androgen patterns during the breeding
season should vary among species according to
the amount of social interactions the individuals
are exposed to. For example, in monogamous
species with high levels of paternal care androgen
levels may increase above the breeding baseline
only when males are challenged by other males or
by mating. At other times androgens should remain
at the breeding baseline in order to not interfere
A second prediction of the challenge hypothesis
is that male androgen levels above a breeding
baseline are incompatible with the expression of
paternal care. If high androgen levels occur in
response to frequent territorial or social challenges
the male had to cope with, the individual would
pay off by investing less time into care of off-
4. Mating systems and endocrine responsiveness
R.F. Oliveira et al. / Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
207
Table 2
Variation in circulating androgen levels (mean values) throughout the breeding season in male teleosts that display paternal care of
offspringa
Species (Family)
Phase
Syngnathus acus
(Syngnathidae)
Syngnathus typhle
(Syngnathidae)
Lepomis macrochirus
(Centrarchidae)
Chromis dispilus
(Pomacentridae)
M
P
M
P
M
P
M
Hypsypops rubicundus
(Pomacentridae)
Lipophrys pholis
(Blenniidae)
Parablennius sanguinolentus
parvicornis (Blenniidae)
Sarotherodon melanotheron
(Cichlidae)
Porichthys notatus
(Batrachoididae)
P
M
P
M
Testosterone
(ngyml)
15.2
6.4
3.2
2.0
24
7
4–6; 9b
-1; 1.5b
15b
9b
1.4
11-KT (ngyml)
Author
3.6
0.9
2.4
0.9
55a
14a
49b
Mayer et al., 1993
8b
22b
7b
2.5
Mayer et al., 1993
Kindler et al., 1989
Pankhurst, 1990
Barnett and Pankhurst, 1994
Sikkel, 1993
Oliveira and Canario, unpublished
P
M
0.8
15
1.5
6
P
M
8.1
22
2.1
ND
Specker and Kishida, 2000
ND
11.5
Knapp et al., 1999
P
M
1.9
0.1c
P
0d
Oliveira et al., 2001b
8.1e
0.8f
M, mating phase; P, parental phase.
a
Values obtained 1 day after spawning.
b
Values extrapolated from published graphs.
c
Median value.
d
No males had detectable values (assay sensitivity was approx. 0.2 ngyml).
e
Levels of males guarding nests containing only eggs.
f
Levels of males guarding nests with embryos.
with paternal care. Conversely, in males from
polygynous species androgen levels should be
elevated close to the physiological maximum
throughout the breeding season due to high levels
of male–male competition. Wingfield et al. (1990)
reviewed the available testosterone and aggression
data of 20 free-living passeriform species and their
results supported the interspecific predictions of
the challenge hypothesis. Males of polyandrous
and of monogamous species showed higher androgen responsiveness (increase from breeding baseline to maximum response) to social interactions
than males of polygynous species. More recently,
Wingfield et al. (2000) have increased the number
of bird species in their database (60 species) and
the resulting patterns remain the same.
This relationship between mating strategies,
degree of paternal care and androgen levels is
further supported by the fact that T implanted
males of a monogamous species became polygynous, deserting their mates (Wingfield, 1984b).
Moreover, males of polygynous species have longer periods of elevated testosterone levels, which
correspond to the mating phase (i.e. displaying,
mate-guarding, territoriality, etc.; Beletsky et al.,
1995).
In order to assess if this is a specific rule in
birds or if it also applies to other vertebrates, we
have been collecting the available published data
to compare the androgen responsiveness patterns
between teleost fish species. Below we will present
a preliminary analysis of our database at its current
status (Figs. 1 and 2). We have separated the
effects of the mating system from the effects of
the parenting system, which were combined in the
analyses mentioned above (Wingfield et al., 1990,
2000). The reason to separate the two factors is
twofold. First, in some species with which we are
208
R.F. Oliveira et al. / Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
Fig. 1. Androgen responsiveness of male teleost fish for different parental strategies obtained from a literature survey.
Androgen responsiveness was calculated as the ratio of the
maximum response over the breeding baseline. (a) Non-breeding baseline level; (b) breeding baseline level; (c) maximum
physiological response level (Wingfield et al., 1990). Numbers
refer to the following species: 1, Acipenser ruthenus (Mojazi
Amiri et al., 1996); 2, Oncorhynchus mykiss (Rouger and Liley, 1993); 3, Oncorhynchus nerka (Kubokawa et al., 1999); 4,
Salmo salar (Mayer et al., 1990b); 5, Salmo trutta (Cardwell
et al., 1996); 6, Salvelinus fontinalis (Cardwell et al., 1996);
7, Cyprinus carpio (Nikitina and Godovich, 1984); 8, Catostomus commersoni (Scott et al., 1984); 9, Ictalurus nebulosus
(Rosenblum et al., 1987); 10, Heteropneustes fossilis (Lamba
et al., 1983); 11, Fundulus heteroclitus (Cochran, 1987); 12,
Porychthys notatus (Knapp et al., 1999); 13, Gasterosteus aculeatus (Mayer et al., 1990a); 14, Syngnathus acus (Mayer et
al., 1993); 15, Syngnathus typhle (Mayer et al., 1993); 16,
Lates calcarifer (Guiguen et al., 1993); 17, Dicentrarchus
labrax (Prat et al., 1990); 18, Morone saxatilis (Mylonas et
al., 1997); 19, Lepomis macrochirus (Kindler et al. 1989); 20,
Stizostedion vitreum (Malison et al., 1994); 21, Pomatomus
saltator (MacGregor et al., 1981); 22, Pagrus major (Ouchi
et al., 1988); 23, Acanthopagrus butcheri (Haddy and Pankhurst, 1998); 24, Rhabdosargus sarba (Yeung and Chan,
1987); 25, Sparidentex hasta (Lone et al., 1991); 26, Cynoscion nebulosus (Thomas et al., 1982); 27, Oreochromis aureus
(Mol et al., 1994); 28, Oreochromis mossambicus (Oliveira et
al., 1996); 29, Sarotherodon melanotheron (Kishida and
Specker, 2000); 30, Chromis dispilus (Pankhurst, 1990); 31,
Acanthochromis polyacanthus (Haddy and Pankhurst, 1998);
32, Hypsypops rubicundus (Sikkel, 1993); 33, Sparisoma viridae (Cardwell and Liley, 1991); 34, Parablennius sanguinolentus parvicornis (Oliveira et al., 2001b); 35, Salaria pavo
(Oliveira et al., 2001a); 36, Scomberomorus cavalla (MacGregor et al., 1981); 37, Trichogaster trichopterus (Degani,
1993); 38, Pleuronectes americanus (Harmin et al., 1995); 39,
Pleuronectes platessa (Wingfield and Grimm, 1977); 40,
Rhombosolea tapirina (Barnett and Pankhurst, 1999).
less familiar it would be easier to treat the two
variables separately than trying to get a combined
score. Second, it would allow us to further disen-
tangle the specific contributions of each of the two
variables to the variation of androgen responsiveness in the different species.
The results confirm the interspecific predictions
that the androgen responsiveness is higher in males
from paternal species than in males from species
without male parental care (linear regression of
log10-transformed data: rs0.5; Fs4.7; d.f.s2;
Ps0.016; single effect of degree of paternal care:
tsy2.7; ns40; Ps0.011; Fig. 1). However, so
far, we have found no effect of the mating strategy
on male androgen responsiveness (ts0.5; ns40;
Ps0.605; Fig. 2). To verify if the divergence
between the results obtained for mating and parenting types was also present in birds but masked
by the fact that Wingfield et al. (1990, 2000) used
a compound measure of both variables, we reanalysed the available avian data from the literature
(73 species, Hirschenhauser and Oliveira, 2000).
This re-analysis showed that each of the two
variables did show a significant association with
male androgen responsiveness, in the same way as
when only the compound measure is used. Thus,
one major difference identified so far between
vertebrate taxa is that in teleosts, but not in birds,
the parenting system is determining the androgen
responsiveness of males rather than the mating
strategy. These results may still suffer from the
limited availability of specific mating and parenting systems, with promiscuity and paternal care
Fig. 2. Androgen responsiveness (Wingfield et al., 1990) of
male teleost fish with different mating strategies, as obtained
from a literature survey. For the definition of androgen responsiveness refer to legend of Fig. 1. Numbers indicate different
species (see also Fig. 1).
R.F. Oliveira et al. / Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
Fig. 3. Pairwise comparisons of male androgen responsiveness
(Wingfield et al., 1990) between closely related species with
different degrees of paternal investment among four teleost
families. Salmonidae: Salmo salar and Salvelinus fontinalis,
open squares; Blenniidae: Salaria pavo and Parabelnnius sanguinolentus parvicornis, filled triangles; Cichlidae: Oreochromis mossambicus and Sarotherodon melantheron, filled
circles; Pomacentridae: Acantochromis polyacanthus and
Chromis dispilus, filled squares. See Fig. 1 for the definition
of androgen responsiveness and for the references of the different species (indicated by the numbers).
dominating the available fish species as compared
with monogamy and biparental care among avian
species. We observed a relatively high variation
among polygynous and paternal teleost species,
however, the general pattern seems to be relatively
robust.
Both our analysis and the analysis of Wingfield
et al. (1990, 2000) suffer from the problem of a
potential phylogenetic bias in the data sets used,
for example the over-representation of species from
some groups as compared with more rarely studied
species from other groups, a problem which has
also been recognised by Wingfield et al. (2000).
As a first approach to solve this problem we have
employed pair-wise comparisons of androgen
responsiveness between closely related species that
differ in their matingyparenting styles (Fig. 3).
These preliminary results show that for all the
pairs considered so far, which include species from
four different families (salmonidae, blenniidae,
cichlidae, and pomacentridae), the results confirm
the prediction that in species with paternal care
male androgen responsiveness is higher than in
species with biparental or maternal care (Fig. 3).
209
Although the results obtained so far are clear,
the pairwise comparison method involves disadvantages, as the selection of the closely related
species to be compared may be arbitrary in multilineal evolutionary operation units (e.g. families
represented by more than two species). Therefore,
we are still gathering more data for this database
and a more definitive and inclusive analysis is in
progress. Since Wingfield’s (Wingfield et al.,
1990, 2000) survey of avian endocrine responses
to social interactions the challenge hypothesis has
inspired a number of more restricted studies on
specific groups or species (e.g. Emerson and Hess,
1996; Cavigelli and Pereira, 2000; Nunes et al.,
2000; Goymann et al., in press; but see Creel et
al., 1993), which in general support it. However,
a wider synthesis of the challenge hypothesis
across the different vertebrate taxa is still lacking.
5. The adaptive value of androgen social modulation: androgens as mediators of the social
modulation of cognitive processes
So far we have presented data that in general
supports the predictions of the challenge hypothesis in teleost fish, suggesting that social modulation
of androgens is a widespread phenomenon in
vertebrates including teleost fish. One obvious
question that can be raised is why should animals
raise their androgen levels in socially challenging
environments?
One potential adaptive value of increased androgen levels during periods of social challenge would
be a positive effect of androgens on cognitive tasks
that would increase the probability of success of
animals in social interactions. Animals can use
information from previous interactions to adjust
their behaviour in subsequent social interactions
(e.g. winner–loser effect, Chase et al., 1994;
eavesdropping, Oliveira et al., 1998; audience
effects, Doutreland et al., 2001) and androgens are
good candidates to act as mediators of these effects
through modulation of cognitive mechanisms
underlying animal communication.
In other vertebrate taxa it is well established
that sex steroids play a major role in cognitive
processes such as social attention, learning, and
memory (see, e.g. Andrews, 1991; Cynx and
Nottebohm, 1992), and the neuroendocrine mechanisms underlying these processes are beginning
to be revealed. For example, androgen and oestrogen receptors and aromatase activity have been
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R.F. Oliveira et al. / Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
detected in the hippocampus of mammals and birds
(Gahr et al., 1993; Kerr et al., 1995; Weiland et
al., 1997; Saldanha et al., 1999), a brain area
known to be involved in relational memory processes (e.g. declarative memory, Eichenbaum et al.,
1992; Squire, 1992). Interestingly also in fish
androgen receptors have been found in the dorsolateral telencephalon (Gelinas and Callard, 1997)
which has recently been demonstrated to be
involved in spatial memory formation in goldfish
(Vargas et al., 2000).
We have recently tested the effects of androgens
on social attention in the Siamese fighting fish
(Oliveira and Carneiro, unpublished data). A tank
was divided in three parts: a large central compartment, and two smaller end compartments. A
male was placed in the central compartment and a
pair of males was placed in each of the end
compartments. The members of one of the pairs
were separated by an opaque partition and the
members of the other pair were separated by a
clear partition. Thus, in the former pair, males
were resting in their individual compartments
while in the latter pair, males were displaying to
their partner across the clear partition. This set-up
has been used in a previous experiment in which
it was shown that male Siamese fighting fish spend
more time observing the interacting pair and that
they use the information they have gathered while
eavesdropping in subsequent interactions with individuals they have observed fighting (Oliveira et
al., 1998). Thus, the time spent observing conspecifics was used as a measure of social attention.
The time that the focal male (placed in the central
compartment) spent observing the interacting pair
was significantly higher in T-treated fish than in
controls, suggesting an effect of T on social
attention. It could be argued that this difference
would be a result of increased aggressive motivation in the T-treated fish. However, T treated
subjects did not display higher levels of agonistic
behaviour towards the interacting pair than the
control group (Oliveira and Carneiro, unpublished
data). It is suggested that T may possibly promote
information gathering on the competitive abilities
of conspecific neighbours which they can use in
future interactions with their neighbours. Hence,
we predicted that even the endocrine system of
individuals that are not participating directly in a
social interaction but are exposed to it — bystanders that can be potential eavesdroppers — should
respond to the social environment.
To test this idea we conducted an experiment in
which a bystander fish (male O. mossambicus)
was allowed to observe through a one-way mirror
two conspecific neighbours fighting. As predicted
androgen levels of bystanders raised after observing fights, but not those of bystanders that were
observing conspecifics which were prevented from
fighting (Oliveira et al., 2001c). Thus, being
exposed to a socially unstable environment may
affect the androgen levels of males even if they
are not directly involved in the social interactions.
The adaptive value of elevated androgen levels in
spectators are suggested to be related to the fact
that androgens mediate the changes required for
increased awareness and readiness to a challenge,
which would be more probable to a bystander in
a socially unstable environment. Thus, androgens
should be viewed not only as sex steroids but also
as ‘competition’ hormones that respond to the
social environment and that prepare the individual
to face competitive contexts, in the same way that
corticosteroids are viewed as stress hormones.
6. Ultimate consequences of androgen social
modulation
The occurrence of social modulation of androgen levels has some potential implications at the
evolutionary level.
First, the expression of androgen-dependent secondary sex characters, both morphological (e.g.
ornaments) and behavioural (e.g. courtship),
would be expected to be regulated according to
their resource holding potential (RHP sensu Parker,
1974, i.e. their ability to compete successfully with
other individuals for a given limited resource)
since males have their androgen levels shaped by
their social status and social environment. In a
social system in which male–male agonistic interactions are frequent, males that display characters
that do not correspond to their RHP may incur
heavy costs by provoking agonistic confrontations
that they will not be able to win. Thus, androgendependent ornaments and behaviours are expected
to be honest signals of male quality.
Second, by signalling their status both morphologically and behaviourally, dominant males may
reinforce their social status by a positive feedback
mechanism. Thus, small initial differences in RHP
may result in increasingly larger status differences.
This way social modulation of androgens may
R.F. Oliveira et al. / Comparative Biochemistry and Physiology Part B 132 (2002) 203–215
allow the evolution of an amplifier mechanism in
signals that are androgen-dependent.
Third, if the beneficial effects of androgens
could be separated from their detrimental effects,
they would be better mediators of the expression
of sexually selected traits. The dissociation of the
response of the different trait responses to androgens may be achieved by a local modification of
the number or the affinity of steroid receptors
present. This would allow a compartmentalisation
of the androgen effects on the phenotype (Ketterson and Nolan, 1994). Results compatible with
this compartmentalisation mechanism have been
observed in cichlid fish in which the relative size
of the genital papillae (an indicator of androgen
levels) was well correlated with the relative size
of the dorsal and anal fins, which are used in
male–male competition for mates and in courtship
displays towards females. In contrast, the relative
size of the genital papillae was not correlated with
the relative size of the caudal fin, whose role in
reproductive behaviours is constrained by its propulsive function (Oliveira and Almada, 1995,
1998).
Finally, if hormones play a mediating role
between the outcomes of social interactions and
the expression of male traits, this opens a way for
the evolution of a number of alternative life history
patterns. In fact, it is known that the social status
of a fish may affect a number of its life-history
traits such as sexual maturation (e.g. Xiphophorus
variatus, Borowsky, 1973, 1978; Astatotilapia burtoni, Fraley and Fernald, 1982), the adoption of
alternative male tactics (see Taborsky, 1994 for a
review), or even sex-change (see Shapiro, 1979
and Grober, 1998 for general reviews on the
subject). All these possibilities may allow compensatory responses to evolve so that subordinate
fishes minimise the disadvantages of their status
by adopting the life history pattern that makes the
best of their situation. For example, a smaller
subordinate individual may delay or suspend its
sexual maturation and, thereby, may divert more
resources to growth, subsequently overcoming its
relative size disadvantage. The same compensatory
principle has also been proposed both, for alternative mating tactics (e.g. Taborsky, 1994; Gon¸
calves
et al., 1996) and for socially controlled
mechanisms of sex-change (e.g. Warner, 1975;
Warner et al., 1975). This phenomenon may be
much more widespread among teleosts, as it is
much less conspicuous than sex change or the
211
adoption of sneaking tactics, and requires specific
ontogenetic studies for it to be revealed.
7. Conclusions
In summary we have presented data confirming
the occurrence of social modulation of androgen
levels in teleosts. Furthermore, the predictions of
the ‘challenge hypothesis’ (Wingfield et al., 1990)
regarding the effects of the mating system and of
the parenting style on androgen responsiveness
were confirmed, especially for the latter. Thus, the
‘challenge hypothesis’ (Wingfield et al., 1990),
which has been initially proposed for avian species, may emerge as a general principle in vertebrate endocrinology.
Acknowledgments
¸ ˜ para a
This work was funded by Fundacao
ˆ
Ciencia
e a Tecnologia (PraxisyPyBIAy10251y
1998). The authors wish to thank John Wingfield,
Vitor Almada and Albert Ros for stimulating
discussions on this topic. The following people
contributed either with data or with valuable information for the analysis: Alexis Dujmic, David
¸
¸
Goncalves,
Emanuel Goncalves,
Ned Pankhurst,
Ricardo Beldade, and Ricardo Matos.
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