3 0 2 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(00)01889-9 TREE vol. 15, no. 7 July 2000
O
ne thing I can honestly brag about is my early recognition of Hamilton’s immense importance. It led to some correspondence between us in the early 1960s on his classic works on kin selection1,2and senescence3, and my1966 book4manuscript. During my
sab-batical in Iceland in 1966 and 1967, I took time to visit him at the University of London Field Station at Silwood Park, UK and to enjoy his hospitality there. This was just two days after visiting David Lack at Oxford, UK. Thus, on this one brief trip I met two most pleasant and immensely important scientists of widely different ages. That the youthful Hamilton could be so far ahead of almost all living biologists on such important issues was mighty encouraging.
Over the next 14 years, we occasion-ally met at meetings and exchanged some more correspondence. Then, in the fall of 1980, I had a one-semester appointment at the University of Michigan while Bill was on the faculty there. He and I gave a graduate seminar on sexual selection and related topics. Two especially worthy students were Marlene Zuk, now Pro-fessor at the University of California (Riverside, USA), and David Quellar, now Professor at Rice University (Houston, TX, USA). To me they have been a heroine and a hero ever since, and Bill found Marlene a choice collaborator in explain-ing the importance of sexual reproduction and sexual selection5.
Bill and I had many interactions in the 1980s and 1990s, including a 1999 meet-ing on my campus at Stony Brook (New York, USA) on the evolutionary signifi-cance of sexuality. What I remember most about that meeting was his talk on the role of genetic recombination in pro-tecting offspring against pathogens that can quickly adapt to individuals of their parents’ genotypes. In it, he compared, using impressive slides, a strictly sexual tree species in its native habitat, beset by serious pathogens, and in a habitat on another continent where its pathogens had not been introduced. The pathogen-free specimens must have had about ten times the biomass and fecundity of those in their natural habitat, where pathogens exacted extreme fitness costs.
Many of Bill Hamilton’s important biological advances of the past half cen-tury are known to TREE readers, but I will exploit my present role to extol one
of my favorites, which is not often recog-nized as a major contribution. His Geom-etry for the Selfish Herd6proposed that
the main reason for gregarious behavior in animals is to maximize competition for the bad things in life. If there are sev-eral sheep in a meadow all staying close together except for one that wanders off by itself, which is most likely to be attacked by a wolf? If the wolf sees the loner first, it will probably be the victim. If the wolf sees one of the others first, each will have companions to compete for the wolf’s attention and, therefore, each will be a less likely victim, even without such benefits as alarm calls or collective alertness.
There are other bad things in life that gregariousness can mitigate. If I were in a room with a mosquito bearing the West Nile virus, I would feel safer as one of a large crowd than I would alone. People in modern wealthy nations tend to think that pathogens usually come from close contact with other human victims; how-ever, in a world full of pathogen vectors, such as mosquitoes, tsetse flies and ticks, the largest crowd could provide the safest environment.
A long list of Bill’s works might be recognized as crowning achievements, but my guess is that his 1964 kin-selection modeling1,2could be the most
widely admired and the most historically important. It was the most important for me, not only conceptually but also per-sonally, because my wife and I had pub-lished a clumsy treatment of a related topic, natural selection among nuclear families7. It was a relief to have our ideas
replaced by Bill’s simple proposal of selection among individuals for the adaptive use of cues indicative of kinship with any conspecific.
No real scientists ever agree on everything, and Bill and I had a brief con-flict last year at the Stony Brook confer-ence. I am not convinced that adaptation* by local pathogens to parental genotypes need be the major problem solved by sexuality. I think that the general unpredictability of offspring environ-ments is what provides the main advan-tage. This issue is most appropriately settled not by modeling or data gathering but by consulting authorities. For a reli-able insight on the significance of sexual-ity there are many appropriate authori-ties, but one that is especially clear is the
strawberry plant (Fragaria). Offspring that develop immediately in the parents’ environment, with pathogens adapted to those parents’ genotypes, will not be sexu-ally produced; whereas those that develop at variable times in the future, over a large range of habitats will be. The allocation of resources to sexual and asexual reproduction must be that which balances the twofold cost of meiosis by the advantage of genetic diversity among widely dispersed seeds.
Is sexual reproduction adaptive for a species such as ours, which reproduces asexually only by a rare and maladaptive polyembryony? Consider the fitness of a seemingly normal parthenogenetic woman who produces diploid ova ready to develop, but also consider her fitness with just a step in that direction, ova with 24 instead of 23 chromosomes? If a life cycle normally includes no asexual reproduction, as in nearly all vertebrates and insects and many plants, the sexual process might be a maladaptive histori-cal legacy from an early ancestor in which it was adaptive.
I dislike one aspect of Bill Hamilton’s career – its brevity. That he will no longer be solving basic biological problems is sad news for biology.
*Note added in proof
The latest issue of Evolution contains an important contribution on optimized tradeoffs between sexual and asexual reproduction8.
George C. Williams
Dept of Ecology and Evolution, State University of New York, Stony Brook, NY 11794, USA
(dcwilliams@ccmail.sunysb.edu)
References
1 Hamilton, W.D. (1964) The genetical evolution
of social behavior. I. J. Theor. Biol. 7, 1–16
2 Hamilton, W.D. (1963) The genetical evolution of social behavior. II. J. Theor. Biol. 7, 17–52
3 Hamilton, W.D. (1966) The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45
4 Williams, G.C. (1966) Adaptation and Natural
Selection, Princeton University Press
5 Hamilton, W.D. and Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites. Science 218, 384–387
6 Hamilton, W.D. (1971) Geometry for the selfish herd.J. Theor. Biol. 31, 295–311
7 Williams, G.C. and Williams, D.C. (1957) Natural
selection of individually harmful social adaptations among sibs with special reference to social insects. Evolution 11, 32–39
8 Burt, A. (2000) Sex recombination, and the
efficacy of natural selection – was Weisman right? Evolution 54, 337–351
