Download Testosterone and sexual selection

Behavior*] Ecology VoL 8 No. 1: 108-112
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Testosterone and sexual selection
N. HUTgrnrth, M. Rameno&k* and J. Wbgfield
Universily of Washington, Department of Zoology, Box 351800, Seatde, WA 98195-1800, USA
In 1982, Hamilton and Zuk presented their theory that females choose males on the basis of health indicated through
the expression of secondary sex characters (Hamilton and
Zuk, 1982). The sex steroid hormone testosterone has received considerable attention as a proximate factor regulating
the development of some morphological characters that are
thought to evolve as a result of sexual selection (Hillgarth and
Wingfield, in press; Witschi 1961). However, the realization
that testosterone suppresses the immune system offers fundamental insight into the function of this complex interrelationship, especially in relation to parasite-mediated sexual selection (FoUtad and Karter, 1992). An apparent paradox remains to be resolved: Why is testosterone immunosuppressive?
What function could this serve, and what are the implications
for parasite-mediated sexual selection?
Wedekind and Folstad (1994) suggested that testosterone
and other androgens suppress parts of the immune system so
that limited energy or essential metabolites can be reallocated
for the full expression of a sexual ornament. If these ornaments are very costly then resources may need to be mobilized
from other sources as well. Sex steroid hormones such as testosterone may promote development of at least some secondary sex characters, while suppressing components of the immune system. These resources could then presumably be reallocated for the development of the sexual character. Although
this idea is intriguing, we suggest an alternative, testable hypothesis involving male fertility.
In vertebrates, spermatogenesis begins during early stages
of development but is arrested around birth with a proportion
of the germ cells in meiotic prophase but still diploid. Completion of meiosis and production of haploid spermatocytes
occurs at puberty, or during the breeding season, directed by
reproductive hormones including testosterone (Wartenberg,
1981). Once spermatocytes achieve haploidy they become antigenic. Because meiosis occurs long after the development of
the immune system, proteins associated with haploid state are
recognized as "foreign" (Sharpe, 1994; Turel and IipshuJtz,
1994). To avoid stimulation of immune response, these antigenic spermatocytes embed within the sertoli cells of the seminiferous tubules, which are protected to some extent by the
blood testis barrier (Sharpe, 1994; Turel and Iipshultz, 1994).
However, some lymphocytes pass through. Sperm antigens
may also pass out into the circulation (Lehmann and Emmons, 1989; Turel and Lipshultz, 1994).
Testosterone levels within the seminiferous tubules are
greatly elevated over plasma levels, presumably because of the
presence of androgen binding protein (Wingfield et aL, 1991)
and may exceed concentrations apparently needed for completion of spermatogenesis (Sharp, 1994). It has been suggastod that testosterone suppresses the production of antibodies (that can damage sperm) in response to sperm antigens
in the te'sticular area (Lehmann and Emmonj, 1989; Turel
and Iipshultz, 1994). Testosterone may inhibit production of
antisperm antibodies by stimulation of lymphocyte suppresser
cells (Lehmann and Emmons, 1989; Turel and Lipshultz,
1994) Thus it appears that testosterone is critical for both the
regulation of ipermatogenesis and suppression of auto-immune responses to antigenic sperm (lehmann and Emmons,
1989; Turel and Iipshultz, 1994). Lehmann and Muller
(1986) found a significant number of human males with decreased fertility had low levels of testosterone and high antisperm antibody titers circulating in the plasma. To test this
premise, antisperm antibody responses could be measured in
males with manipulated testosterone levels.
The relationship of testicular testosterone and local suppression of the immune system, which may overflow in varying
degrees into other areas of the organism, suggests that animals should keep circulating levels of testosterone to an absolute minimum. However, at least at temperate latitudes, testosterone has very important effects on morphology, physiology and behavior of some species (Bathazart, 1983; Wingfield,
1990; Witschi, 1961). This release of testosterone into the
blood for orchestration of these additional biological effects
may also mean that the immune system is potentially vulnerable to suppression throughout the organism. In the class
Aves, a review of a large number of investigations indicate that
males do indeed appear to maintain circulating testosterone
levels at a minimum (Wingfield et aL, 1990). Males of socially
monogamous species show surges of circulating testosterone
that are facultative responses to challenges from other males.
These surges maintain high levels of aggression during antagonistic interactions but are brief and last only minutes to
hours. Wingfield et al. (1990) concluded that a major cost of
these high levels of testosterone was an interruption of male
parental care typically seen in socially monogamous species.
In contrast, males of socially polygynous species tend not to
express parental care and maintain high levels of circulating
testosterone for long periods (days to weeks). In light of its
debilitating effect on the immune system, a second cost of
high testosterone and risk of infection should now be considered. Several predictions can now be made in relation to temporal patterns of testosterone mating systems and sexual selection. We would predict that the immune system shows
greater seasonal suppression in polygynous species than in
monogamous species. Conversely, if socially polygynous males
have evolved a certain degree of immunological tolerance to
high circulating levels of testosterone, then we would predict
that increased male/male aggression and elevated secretion
of testosterone in socially monogamous males would result in
more deleterious effects on the immune system than in polygynous males. These predictions are testable and may help
explain and resolve some of the paradoxes of testosterone
patterns, development of some androgen sensitive secondary
sex characters, and parasite-mediated sexual selection.
It is dear diat to be fertile males require testosterone levels
sufficient to promote spermatogenesis and to counteract
sperm antigenicity within the testis. This androgen-mediated
immunosuppression may be more broad-reaching if testosterone is released into the blood. Males then become even more
vulnerable to parasites unless they have genetic resistance to
infection or the effects of immunosuppressive agents such as
testosterone (Harder et aL, 1994). Parasite resistance could
be expressed through the full develepaom ef socondary sex
characters as suggested by Hamilton and Zuk (1982), but
equally important, androgen-dependent traits may also be expressing male fertility status. Evolutionary biologists have
struggled to envision a way by which females could evaluate
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male fertility directly (Birkhead and Mailer, 1992; Mailer,
1994). The ability to do so could provide strong selection pressure for female choice (Mailer, 1994). This could be expressed in an androgen-dependent secondary sex trait providing a testable mechanism whereby females could detect not
only resistance to disease and overall male quality, but also
fertility status.
We feel that the concept (similar to Folstad and Skarstein's
ideas presented in this volume) of testosterone as an immunosuppressor of the auto-immune responses to sperm is an
alternative to Wedekind and Folstad's (1994) reallocation hypothesis. While these hypotheses are obviously not mutually
exclusive, we think the testosterone-andsperm antibody interaction is a more viable explanation for the general immunosuppressive properties of testosterone as well as indicating a
possible mechanism whereby females may assess male fertility
accurately. Experimental tests are now possible and raise many
exciting possibilities.
We would like to thank I. Folitad and two anonymous reviewen for
their useful comment*. N.H. was supported by a NATO Fellowship,
and J.CW. was supported by National Science Foundation grana OPP9300771 and 1BN-94008013.
Received 25 September 1995; revised 1 February 1996; accepted 3
February 1996.
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Is male germ line control creating
avenues for female choice?
hrar Folstad and Frode Sksntem
Department of Ecology/Zoology, University of Trams*, 9037 TromM,
Norway
Theories of sperm competition and die evolution of secondary sexual characters may have a common denominator in a
male trade-off between immune activity and ejaculate quality.
Sperm cells are non-self to die male and therefore targets of
immunological attacks in the reproductive tract Consequently, sperm cells, and eventually ejaculate quality, are influenced
by a male's ability to down-regulate immune responses during
the production df ejaculates, a process potentially regulated
by immunosuppressive gonadal hormones. The possibility for
unconstrained immunosuppression during spermatogenesis
will be decreased by parasitic infections, which thus can interfere with ejaculate quality. Males with genetic resistance
against parasites will have a higher potential for elevated levels
of immunosuppressive androgen hormones compared to nonresistant males. Therefore, parasite resistant males may be at
an advantage during spermatogenesis and consequently have
high-quality ejaculates. This logic suggesting that parasites
may impose costs on sperm production has implications for
both sperm competition theory and the current understanding of the evolution of sexually selected characters under androgen control (Folstad and Skarstein, 1995). We suggest that
females may obtain heritable parasite resistance for their offspring by exploiting a male trade-off, evolutionary rooted in
male need for germ line control.
Several aspects of vertebrate reproduction are under immunological control (Naz, 1993) and it is also well-documented that sperm are influenced by immune reactions as
they are not recognised as self hi a males reproductive tract
(e.g., Friberg, 1982; Hogarth, 1982; Roitt et aL, 1993). Because
spermatogenesis is initiated at puberty, after die definition of
self, a plethora of haploid sperm surface proteins are recognised as non-self by the male immune system (c£, Bigazzi,
1987; Turek and lipshultz, 1994). However, die exposure of
sperm antigens to die immune system is reduced by the bloodtestes barrier (e.g., Hadley, 1988; Hogarth, 198% Setchell et
aL, 1994). This barrier limits movement of sperm antigens out
of die testes and the ingress of blood-borne immune components into the interior of die testes, thus creating an immunologically privileged site. Moreover, cell and hormonemediated mechanisms behind die barrier protect sperm from
immune reactions (Mashburn and Kutteh, 1994), and lymphocyte activity can additionally be down-regulated by sperm
and seminal fluid (Sates and Erickson, 1975). The blood-testes barrier is formed at puberty, during die carry stage of the
first meiotic divisions, and in seasonal breeders shows a seasonal performance corresponding with spermatogenesis
(Setchell et al., 1994). In sum, these physiological mechanisms
at least partly shelter spennatogenesis from immunological interference in the male reproductive tract.