TREE vol. 4, no. 17, November 7989

( Trichostrong ylus tenuis) infes- tations in the caeca of grouse (Lago- pus lagopus) cause them to smell, which unfortunately attracts carni- vores. During incubation when nests are vulnerable, they feed little and become far less pungent. By ex- perimentally reducing parasite bur- dens, Hudson was able to show that hens’ probability of being found by dogs was definitely reduced, con- cluding that incubating birds are in- deed effective in lowering their chances of detection.

Predators and antipredator be- haviour were linked in other ways. My own work showed that even in top carnivores such as cheetahs (Acinonyx jubatus), behaviour is moulded by the threat of predation by lions (Panthera leo) and spotted hyaenas on cheetahs themselves. Although large carnivores are often thought to live in groups to increase foraging efficiency through cooper- ative hunting, little evidence actually supports this: both small groups of male cheetahs, and adolescents of both sexes that remain together as a group for several months after leav- ing their mother, form groups for other reasons. Those juveniles that remain together are able to lower their personal vigilance and are

harassed less often by dangerous predators.

Finally, film of topi (Damiliscus korrigum) on a lek, shown by Peter Jones (BBC, Bristol), provided a tan- talizing hint of the trade-offs that prey face in attempting to escape predation. During the morning hours, female topi in Masai Mara, Kenya were seen feeding in long grass where lions can easily hide, but at the onset of their midday rest period they moved away, up the slope to shorter grass where pred- ators are less easily concealed. While they were asleep, on the site of the male lek, solitary spotted hyaenas stalked them, probably surprising and killing eight individuals in this ways. Thus, one antipredator strat- egy has repercussions on other as- pects of behaviour: here, amount of time devoted to sleep and whether to sleep next to conspecifics. Under- standing prey behaviour in terms of predation risks that we rarely see, and measuring the indirect costs of predation”, are challenges that field biologists must now tackle.

Behavioural coevolution of pred- ators and prey certainly requires much more attention, but it is easy to see why the study of predation is so exciting when events are scaled up

to our own size. BBC rushes of 3000 kg killer whales (Or&us orca) catching 75 kg sealion pups (Otaria flavescens) conveyed the appalling fear of being attacked. Surfing in on huge breakers on the Argentinian coast, the whales grab unsuspecting youngsters as they cavort on the beach, take them out to sea, and then use them as a kind of football with their huge tails before devouring them. When, after three weeks of filming from the beach, the camera crew decided they needed additional shots from underwater, none of us dared ask further questions.

References 1 Caro, T.M. and FitzGibbon, C.D. in Natural Enemies: The Population Biology of Predators, Parasites and Diseases (Crawley, M.J., ed.), Blackwell Scientific Publications (in press) 2 Guilford, T. and Dawkins, MS. (1987) Anim. Behav. 35,1838-l 845 3 Elgar, M.A. (1989) Biol. Rev. 64, 13-33 4 FitzGibbon. CD. 11989) Anim. Behav. 37,508-510 5 Gosling, L.M. and Petrie, M. Anim. Behav. (in press) 6 Sih, A. (1987) in Predation: Direct and Indirect Impacts on Aquatic Communities (Kerfoot, W.C. and Sih, A., eds), pp. 203-224, University Press of New England

New Phenotypes from Symbiosis Richard Law

How DO NOVEL PHENOTYPES come about in evolution? The consensus in evolutionary biology has been that they generally stem from gradual phenotypic changes taking place within species’. This goes back to Charles Darwin himself, who stated*: ‘If it could be demonstrated that any complex organ existed which could not possibly have been formed by numerous, successive, slight modi- fications, my theory would absol- utely break down.’ From the study of symbioses, a view is emerging that major innovations can also come about by the bringing together of dissimilar organisms in symbiosis, giving one (or both) access to a ready-made suite of phenotypic traits of the other.

symbiosis as a source of evolution- ary innovation. Looking back over the history of life, we can see that there is at least one major event in which symbiosis most probably played a crucial part - the evolution of the eukaryotic ceil, through associations involving prokaryotes with aerobic respiration and with photosynthesis. A third cornerstone of this process -the evolution of the cellular motility apparatus from a spirochaete-like ancestor - remains more controversial, but the meeting was told of new evidence to support it (Greg Hinkle, Amherst; Lynn Mar- gulis). This included the identifi- cation of a tubulin-like protein in cer- tain spirochaetes and, of particular interest, the discovery of a 5 Mb DNA sequence at the site of the kinetosome in Chlamydomonas rein- hardtii. The latter was announced by David Luck and John Hall (Rocke- feller University, New York) at the American Cell Biology Meeting in San Francisco earlier this year, and has yet to be published.

part in another major event in evol- ution: the colonization of land by plants. David Lewis (Sheffield) ar- gued that the immobility of phos- phorus in terrestrial environments posed serious difficulties for the early (rootless) land plants, and sug- gested that the association with vesicular-arbuscular mycorrhizal fungi, which contributed to phos- phorus uptake, was a crucial event at the source of the great radiation of plants on land in the last 400 million years. Another union of photobionts and fungi - the lichen - has had far-reaching effects on the evol- ution of the Ascomycetes (Rose- marie Honegger, Zurich).

A recent meeting at the Rockefeller Foundation Study Center (Lake Como, Italy), organized by Lynn Mar- gulis (Amherst) and Ken Nealson (Milwaukee), considered the role of

Richard Law is at the Biology Dept, University of York, York YOl 5DD, UK.

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Symbiosis may also have played a

0 1989 Elsewer Science Publtshers Ltd lUKl0169-5347'89 $02 Oi;

The suggestion of symbiologists is, in effect, that the ‘gene pool’ for evolutionary innovation is not completely constrained by species boundaries. For instance, the set of phenotypes potentially available could be enriched by horizontal transfer of genes between species, a process that is clearly seen in bac- teria. Sorin Sonea (Montreal) envis- aged the bacterial cell as a symbiosis in which one large replicon - the bacterial chromosome - harbours a variety of smaller ones - plasmids, prophages - on a temporary basis.

TREE vol. 4, no. 11, November 1989

These small replicons readily trans- fer information from one kind of bacterium to another. That this is an effective source of new pheno- types is evident from the evolution of resistance to antibiotics, where plasmid-borne resistance genes have carried resistance from one bacterial taxon to another.

On the other hand, horizontal transfer of genes across the bound- aries of eukaryotic species is, with the exceptions of introgression and allopolyploidy, much more debat- able. The suggestion that flowers, fruits and storage organs of plants could have come about by transfer of genes from gall-forming insects and fungi (Kris Pirozynski, Ottawa) is speculative at the moment, as is the idea that some fungus-like traits of plants, such as haustoria and pollen tubes, could stem from incorpor- ation of fungal genes (Peter Atsatt, Irvine). Nonetheless,anextraordinary intracellular war, described by Lynda Goff (Santa Cruz), in which nuclei of parasitic red algae take over the cyto- plasm of their hosts, shows that at least one prerequisite, that of close proximity of the nuclei, can be met.

More usually, we find the separate identity of the symbiotic partners re- tained when at least one partner is eukaryotic (although there is the dilemma as to whether we would recognize the system as symbiotic were this not the case). For instance, Ken Nealson described a play of ex- quisite complexity between lumines- cent bacteria and nematodes in their combined attack on insect larvae. Early in life, the nematodes are free- living and simply feed on the bac- teria. They eventually stop feeding and harbour the bacteria internally while searching for an insect host. After entry into the host, the bacteria are released. Being very toxic, the bacteria kill the host and increase to a high population density in the host tissues, while releasing antibiotics that prevent invasion by other micro- organisms. At the same time, the nematode reproduces and the young feed on the bacterial culture. The bacteria produce a pigment that makes the carcass red in the day- time and in addition they make it luminescent at night; it is therefore highly visible, which possibly has the effect of attracting predators and bringing about dispersal of the young nematodes and bacteria.

It makes little sense to envisage these intimately intertwined life- styles as anything other than a symbiotic innovation. The same applies to the light organ symbioses of leiognathid fishes, which also in- volve luminescent bacteria (Margaret

McFall-Ngai, Los Angeles). Some phenotypic innovations are

simply not possible within the con- fines of a single gene pool. Russell Vetter (La Jolla) pointed out that the metabolic changes necessary to operate a chemoautotrophic sulphide-based metabolism are too complicated to arise de novo in eukaryotes. Yet chemoautotrophic animals do exist by virtue of sym- bioses with sulphur-oxidizing bac- teria. In the case of vestimentiferan worms of hydrothermal vents, the digestive system is absent and there is an obligate dependence on the bacteria to meet all energy require- ments.

How much symbionts can gain from their association is well illus- trated by a rice weevil/bacteria endosymbiosis described by Paul Nardon (Lyon). The bacteria in this symbiosis are found as permanent ‘organelles’ of the female germ line and as temporary inhabitants of cells around the larval gut, and are not capable of independent existence. For the weevil, the symbiosis brings five vitamins and some growth fac- tors which, although not essential, are associated with more rapid de- velopment, increased fertility and the capacity for flight. The substan- tially enhanced reproductive success of symbiotic weevils is apparent when they are introduced into an aposymbiotic population, for the symbiosis spreads rapidly through the population. Paul Nardon envis- aged the symbiotic phenotype as originally ‘acquired’ from the en- vironment and subsequently ad- justed by natural selection, and this led him to call for a more pluralistic view of evolution than that of the neo-darwinists. It would be in- teresting to know the degree to which innovations apparent in well- established symbioses such as this have remained unchanged from the original association or have come about during subsequent evolution generated by the interaction.

These systems illustrate how novel phenotypes can emerge from symbiosis without necessarily viol- ating the integrity of the gene pools of the partners. This does mean, though, that continuity of the pheno- type through the germ line of multi- cellular organisms is not assured. As John Maynard Smith (Sussex) pointed out, enclosure of the part- ners so that the success of each is bound to that of the other should be an important feature of such evol- ution; if this enclosure is retained from one generation to the next, then continuity of the phenotype may be achieved despite the separ-

ate genomes involved. It turns out that there are sometimes elaborate processes that bring endosymbiotic microorganisms into contact with the egg cells of their multicellular hosts. Such processes are evident among the bacterial endosymbionts of insects discussed by Werner Schwemmler (Berlin) and Toomas Tiivel (Tallinn); these endosym- bionts are always maternally in- herited.

As a population biologist listening to the description of symbiotic sys- tems, I found the record of sym- biotic innovation impressive. It is intriguing that a group of cell biol- ogists, working on systems outside the standard frame of reference of evolutionary biology, should be de- veloping this rather different per- spective of evolution. Their systems are subtle and easily overlooked; new ones continue to be found, such as the inhabitants of the renal sac of certain tunicates (Mary Beth Saffo, Santa Cruz), and bacteria- like organisms in vesicular-arbus- cular mycorrhizal fungi (Silvano Scannerini, Torino). As shown by an Amoeba/bacteria symbiosis (Kwang Jeon, Knoxville), new ones also continue to evolve. There is a need for evolutionary biologists to consider seriously the extent to which innovation in evolution has come about by symbiosis.

At the same time, I wonder about the relative likelihood of innovation from symbiosis and from changes within species. Within a population, the raw material for endogenous change is being continually gener- ated by mutation and recombination. The new materials for symbiotic change, on the other hand, depend on chance associations with other species; at present we have little reason to suppose that natural com- munities are organized in such a way that many new potential associates are available. (Is the microbial com- ponent of communities different?) The genetic system ensures that there is a good chance that an advan- tageous mutation will be inherited, whereas a symbiotic innovation may fall apart during reproduction of the partners. My hunch is that symbiotic innovation is relatively unusual in evolution, although potentially revol- utionary when it does happen.

References 1 May, E. (1960) in Evolution after Darwin (Vol. 1) (S. Tax, ed.), pp. 349-380, Chicago University Press 2 Darwin, C. (1859) The Origin of the Species by Means of Natural Selection (1st edn), Reprinted by Penguin