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Behavioral Ecology Vol. 12 No. 3: 264-266
© 2001 International Society for Behavioral Ecology
Hamilton Symposium |
Bill Hamilton, sexual selection, and parasites
Max-Planck-Institute of Limnology, Department of Evolutionary Ecology, August-Thienemann-Strasse 2, D-24306 Ploen, Germany
Address correspondence to M. Milinski. E-mail: milinski{at}mpil-ploen.mpg.de .
Darwin (1871
) first
introduced the idea that males with elaborate ornaments have a net benefit
because they are preferred as mates. Evidence for such preferences is now
abundant (e.g., Andersson,
1994). A more troublesome problem has been to understand the
evolution of female preferences for handicapped males. Until the early 1980s,
there were mainly two theories: (1) Fisher's
(1930) runaway process, which
predicts that the male character and the female preference could, through
genetic correlation in the offspring, advance together with ever-increasing
speed. This was "easy to see," as Fisher wrote, and therefore he
did not provide a formal proof. (2) Zahavi's
(1975) handicap principle: a
female prefers a male with a handicapping trait because this male must have
high viability (i.e. good genes), to be able to survive with the handicap.
Both hypotheses appeared to resist any theoretical proof that was based on
conventional population genetics. For example, the problem with all good genes
models is that if females prefer to mate with the males that have the good
genes for high viability, then these genes become quickly fixed in the
population and nothing will be revealed by the handicap except the handicap
itself. So females should stop preferring handicapped males.
In the early 1980s both hypotheses suddenly received support. Lande
(1981) and Kirkpatrick
(1982) showed with elaborate
genetic models that Fisher's runaway process can work [actually O'Donald
(1980) had paved the way]. But
it was Bill Hamilton and Marlene Zuk (1982; see also Hamilton,
1982) who proposed a new good
genes hypothesis that predicted substantial additive heritability for
viability genes ad infinitum. Hamilton and Zuk
(1982) suggested that genes for
resistance might have important effects on fitness and always remain
heritable. The interaction between host and parasite is unusual because it
produces cycles of coadaptation. These cycles can ensure a continual source of
fitness variation in genotypes.
Imagine a host and a parasite population in which individual hosts differ
in their resistance to different genotypes of the parasite. Some hosts are
resistant to parasite A, some to parasite B. If a female chooses a male that
is resistant to parasite A, when this is the more common parasite genotype,
she is obviously getting a selective advantage because her offspring will be
more likely to be resistant to the common disease. So the next host generation
may be more resistant to parasite A. Now parasite B can successfully infect
the host population, and females should prefer males that are resistant to B.
The process will be cyclical because new resistant genotypes that arise in the
host species will provoke the evolution of new parasite genotypes; these in
turn will provoke the evolution of new host genotypes; and so on ad infinitum.
This provides a plausible reason that a population may have substantial
additive heritability for disease resistance. Then a male who is unmistakably
outstanding in health and vigor offers females that mate with him an inherited
healthiness in their offspring that is well above average
(Hamilton and Zuk, 1982).
How do females detect the males that are resistant to the currently
predominating parasite? Hamilton and Zuk's
(1982) clever insight was that
the method a female uses should have much in common with those of a physician
checking eligibility for life insurance. The choosing animal should unclothe
the subject, weigh, listen, observe vital capacity, and take blood, urine, and
fecal samples. Instead, if a male can present an elaborate bright plumage,
produce a song that is energetically costly, and display with an exhausting
athletic behavior, it likely has the currently needed genes for resistance
because it so demonstrates that it is healthy.
In later generations, other resistance genes against other parasites need
to be detected. Again, females can use the same preference for elaborate
adornment to detect those males that are resistant to the new parasite.
Hamilton and Zuk (1982)
predicted for comparisons among species that species that show strongly
developed epigamic characters should be subject to a wider variety of
parasites. In species where disease is relatively unimportant, animals should
be less showy. Within a species, preferred mates should have the smallest
parasite burden; parasites should reduce the showy character, and females need
to see this character when they prefer parasite-free mates.
Hamilton and Zuk (1982)
provided a comparative test of blood parasites and showiness of many species
of North American birds. As predicted, they found a highly significant
association over species between incidence of chronic blood infections and
striking display characters. Several years later new comparative results from
other authors (e.g., Read,
1987; Ward, 1988)
supported the Hamilton-Zuk hypothesis. However, the following generation of
comparative tests did not (e.g., Read and
Harvey, 1989). Actually, there seemed to be cycles of supporting
and nonsupporting comparative studies. Taken together, it appears now that the
comparative evidence is equivocal.
It is certainly true that the Hamilton-Zuk hypothesis provoked a whole generation of behavioral ecologists to regard sexual selection and the potential role of parasites as the major topic for at least two decades of research. The five previous behavioral ecology conferences each had several sessions on mate choice. Sexual selection had been a minority topic during the time before the Hamilton-Zuk hypothesis.
In 1986, there was a Dahlem Workshop on "Sexual Selection: Testing
the Alternatives," which appeared to set the stage for research on
sexual selection for the years to come. All participants signed the cover of
the book (Bradbury and Andersson,
1987). However, Bill Hamilton's signature is difficult to detect:
modest as he always was, he is hiding in the bottom-right corner of the back
cover.
I found the Dahlem conference extremely stimulating, especially because I had been lucky to be in Bill's discussion group. Thereafter I worked next door to Bill at Oxford for half a year and found him always to be enthusiastic about the natural history of animals—and he was completely addicted to thinking of parasites!
In 1990, the first experimental intraspecific tests of the Hamilton-Zuk
hypothesis were published (Milinski and
Bakker, 1990; Møller,
1990; Zuk et al.,
1990). This was only the beginning of a movement that almost took
over many journals (Figure 1).
According to my subjective statistics (see
Andersson, 1994, for a balanced
view), most intraspecific tests supported the Hamilton-Zuk hypothesis. At the
present International Society for Behavioral Ecology Conference at
Zürich, there is at least 1 plenary talk, 77
short talks, and numerous posters on sexual selection. Immunology and
immunogenetics seem to be more important now than these fields were in
previous conferences. Suppose for a moment that Bill Hamilton had not existed.
Could one think of a behavioral ecology conference that presents a keynote
talk on "the origin and evolution of the vertebrate immune
system"?
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What did Bill Hamilton tell us about his more recent thoughts on sexual selection? The most recent paper, as far as I know, that he devoted entirely to mate choice was published in 1990 and was entitled "Mate Choice Near or Far." This paper was from a talk that he had given at a symposium on parasites and sexual selection. It is full of neat ideas; for example, he argues that in many monogamous species court-ship is such a lengthy affair that "it has come to seem to me unlikely that a bird needs to rely on looking for bright, tidy plumage or listening to momentary expressions of energy and co-ordination made in complex melodic song" (341). And later he says, "but if all this casts doubt on showiness for monogamous choice it leaves us with a dilemma: if not for monogamy, and yet still used for sexual display, what else is showiness for?" (341). And then he argues in a very entertaining way that he thinks that all the showiness is just for attracting extrapair copulations:
It now seems to me that it may be much more in regard to these events than in regard to seasonal pair bonding that bright coloration of males plays its part. The female who is dissatisfied with the seeming genetic quality of her mate probably has had no chance to perform any detailed assessment of other males in her vicinity; but she may well be able to appreciate the relative qualities of advertisements that are being broadcast through brilliant plumage and song from males at their territory posts on nearby trees.... It will be those supposed monogamists, where brightest males are contrasted to dull females, that reveal most "infidelity" by females and variable negligence of maternal care by males. (342)
There is another piece of his prose that is as entertaining as it is enlightening:
Searching for an island in the morass of possibilities that opens, one might at first seize on the top pair as inevitably stable: surely the female of that pair must have the male that she wants. But if "good genes" have begun to rule, even this is not so. While we easily imagine that the top male is distracted from guarding his nest by invitations from other females, what is it we expect his mate, the top female, to be doing? Is she likely to be working hard on her own to support her mate's brood? Surely not: the top female may be having plenty of invitations too. These come from the lowly males. They are sending hints to her that she is welcome to play cuckoo at their nests—with the proviso, of course, that she allows a copulation first. Their signals may be imagined to convey something like this. "Look how dull I am. How can you possibly doubt—I am your true working father. I and my mate (but quiet about her) will look after your eggs better than you can." In the light of this thought it becomes not even clear that a top male will want the absolutely top female to be his mate, or vice versa. (Hamilton, 1990
Bill Hamilton's view of mate choice had become rather sophisticated even 10 years ago.
Bill Hamilton has been a member of the advisory committee of our Max Planck Institute at Ploen. For this task he spent 4 days at our institute in December 1999. He was full of plans and ideas and so enthusiastic that he appeared to be able to go on forever. Many of us would not have done the kind of research which we did without Bill Hamilton's ideas. His memes will continue to keep us working at least for the next decades.
REFERENCES
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Bradbury JW, Andersson MB (eds), 1987. Sexual selection: testing the alternatives. New York: John Wiley & Sons.
Darwin C, 1871. The descent of man, and selection in relation to sex. London: John Murray.
Fisher RA, 1930. The genetical theory of natural selection. New York: Dover.
Hamilton WD, 1982. Pathogens as causes of genetic diversity in their host populations. In: Population biology of infectuous diseases (Anderson RM, May RM, eds). Berlin: Springer Verlag; 269-296.
Hamilton WD, 1990. Mate choice near or far. Am Zool 30: 341-352.
Hamilton WD, Zuk M, 1982. Heritable true fitness and
bright birds: a role for parasites? Science
218: 384-387.
Kirkpatrick M, 1982. Sexual selection and the evolution of female choice. Evolution 36: 1-12.
Lande R, 1981. Models of speciation by sexual
selection on polygenic traits. Proc Natl Acad Sci USA
78: 3721-3725.
Milinski M, Bakker TCM, 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344: 330-333.
Møller AP, 1990. Effects of a haematophagous mite on the barn swallow (Hirundo rustica): a test of the Hamilton and Zuk hypothesis. Evolution 44: 771-784.
O'Donald P, 1980. Genetic models of sexual selection. Cambridge: Cambridge University Press.
Read AF, 1987. Comparative evidence supports the Hamilton and Zuk hypothesis on parasites and sexual selection. Nature 328: 68-70.
Read AF, Harvey PH, 1989. Reassessment of comparastive evidence for Hamilton and Zuk theory on the evolution of secondary sexual characters. Nature 339: 618-620.
Ward PI, 1988. Sexual dichromatism and parasitism in British and Irish freshwater fish. Anim Behav 36: 1210-1215.
Zahavi A, 1975. Mate selection: a selection for a handicap. J Theor Biol 53: 205-214.[Web of Science][Medline]
Zuk M, Thornhill R, Ligon JD, 1990. Parasites and mate choice in red jungle fowl. Am Zool 30: 235-244.
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