Coevolution between interspecific plant competitors?

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15 Summers, K. II9891 Anim Behav. 37, 797-805 16 Davies, N 6. and Halliday. T.R. t 19771 Nature 289,5b-58 17 Gibbons, M.M. and McCarthy, T K. (1986) 1. Zool. 209, 579-593 18 Robertson, 1.G.M 119891 Anim. Behav. 39, 639-645 19 Hamilton, W.D. and Zuk. M.Z. t 19821 Science 2 18,384-387 20 Hausfater. C., Gerhardt. H.C and Klump, G. ( 1990) Am. Zoo/. 30, 299-3 I I 21 Tinsley, R.C. I I9901 Am. Zoo/. 30, 313-324

Tke nrost intportanl aspecr 01 ~1r1 individual’s environment may 6c its individual neigh6ours; if so, microevolutionary selecriotr pressure could 6e dominated by the competitors. Since biotic differentialion and toevolution of plant populations is a developing field in which there is strorrg interest, it Clas provoked keen discussion. Trifolium repens represents a particularly suitable example for an overview of the advances and criticism voiced in his resea& field. The problem concerning the ecological function of interspecific competitors is how they persist together in the same place without one driving the other extinct. Selection to prevent competitive exclusion may lead to divergence in ecological requirements. This is equivalent to the character divergence that results in niche separation in animal competitors; in plants it has been termed selection for ecological combining ability. A further mechanism, the evolutionary equilibration in competitive abilities, was proposed by Aarssen i.2. The consequence of such a reciprocal process is that any evolutionary advantage of the initially better competitor may be nullified by the other, and so both have to evolve in order to keep their position in the community (unstable equilibrium) However, the generalization that diversity in plant communities is necessarily restricted by the requirements of plants for a limited number of nutrients (the starting point of Aarssen’s argument) was

Andreas Luescher is at the ETH-Zentrum, lnstitut fur Pflanzenwissenschaften. 8092 Ztirich. Switzerland. Pierre lacquard is at the Centre Louis Emberger ICNRSI. BP 5051.34033 IMontpellier Cedex. France.

22 Mitchell. S.L. t 19901 Evolution 44, 502-5 I9 23 Woodward, BD. 11987) Oecologia 73. 626-629 24 Woodward, B.D. f 1986) Am. Nat. 128. 58-65 25 Woodward, B.D.. Travis, I. and Mitchell, S. ( 19881 Evolution 42, 784-794 26 Waldman, 8. Am. Zoo/. lin press1 27 Ryan, M.I. and Rand, A.S. (19901 Evolution 44, 305-3 I4 28 Rand, A.S., Ryan, M.I. and Wilczynski. W Am. Zoo/. tin press1 29 Given, M.F. II9881 Behav. Ecol. Sociobiol.

22, 153-162 30 Robertson, 1.G.M. 11986) Anim. Behav. 34. 773-784 31 Green, A.I. II9901 Anim. Behav. 39, 620-638 32 Given, M.F. II9901 Copeia 1990, 863-867 33 Lopez. P.. Narins. P.M., Lewis, ER and Moore, J.W. II9881 Anim. Behav. 36. 1295-1308 34 Wagner, W.E., jr t 19891 Behav. Ecol. Sociobiol. 25. 429-436 35 Wagner, W.E., jr (19891 Anim. Behav. 38, 1025-1038

CoevoMonbetweenlntwqwxiic PlantCompetitors? Andreas Luescherand PierreJacquard contradicted by the resourcecompetition theory of Tilman3. Coevolution occurs when a trait in one species evolves in response to a trait in another species; it encompasses both specificity and reciprocity. If only one species diverges, coevolution has not occurred. The process cannot be viewed solely as an ecological effect, but must be seen as the result of genetic feedback between interacting species-. Connell’ discussed the existing evidence for the coevolution of competitors and judged it to be weak, adding that, in his opinion, coevolution is more likely to occur between populations on different trophic levels fpredators, parasites), which depend on each other and thus require coexistence. He also argued that competitors, instead of diverging during co-occurrence, may have evolved independently. As a result, when they later interact each species becomes established in that part of the site to which it is preadapted. Connell’ proposed a field experiment to test whether competition, rather than some other mechanism, caused the niche divergence of competitors and whether this divergence has a genetic basis. Connell’s publication marked the beginning of an acrimonious debate on the applicability of certain experimental designs and whether or not competition is an ecological and evolutionary forces’O.

Experimental procedures Plants are known to have a much more plastic phenotype than animals”; so if any character change is measured in the presence of a competitor this could merely be a phenotypic response to present competition without any genetic change having been induced by past competition. Consequently, character divergence cannot be measured in situ in plant populations and the evolutionary impact of competition (in the past1 must be estimated from competition experiments (in the present), which should give evidence that, after selection, competition between the two species is less severe than it was before. All existing experimental procedures are based on the assumption that when two species are collected where they occur separately fallopatryt and where they occur together (sympatry) they represent respectively pre- and postcontact populations (i.e. current separation in space aiso represents separation in timer. Competition experiments to test the importance of interspecific competition as a selecting force have been carried out with populations of white clover (Trifolium repensl in two different ways. First, there have been transplant experiments in the fieId12-14 where ramets of T. repens are sampled from sites dominated by one of several different grass competitors. 355

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After vegetative multiplication, the 7. repens ‘origins’ are replanted back into the original fsympatricf site and transplanted into all other lallopatric) sites. The pre-existing vegetation in the sites is either left or removed. The denuded plots serve as a control for local site effects other than the competitors. This kind of experiment can determine whether the T. repens population contains genetic variation that is correlated with its competitors. However, the reactions of the grass competitors provoked by the different T. repens origins are not tested. competition experSecondly, iments have been carried out under standard conditions. Rametsof both 7. repens and of the neighbouring grasses (different species or different genotypes of the same species) are sampled. After cloning, each grass origin is planted in competition with each clover origin, in all possible combinations (Box II. In such experiments the performance of both competitors is analysed”-I*. However, competition experiments need to be carried out undera range of standard conditions because the predictability of the performance under varied conditions is weak19. Further, a range of planting densities is required20, making this approach complex to carry out. Biotic differentiation and coevolution in white clover Turkington and HarperI indicated that the influence of a plant’s neighbours may be great enough to result in microevolution, and there has since been a great deal of research on the possible evolutionary differentiation of T. repens populations in relation to their grass neighbours’3-‘8.21.22. In the initial work of Turkington and Harper12, the 356

growth of T. repens ‘origins’ was observed in competition with different grass species, while the reaction of the grass species to the clover origins was not tested. The most striking result was a ‘principal diagonal effect’ (Box I) in which each clover type grew best when planted back into its site of origin. Local site conditions in the field clearly had an impact on T. repens growth, but in the greenhouse on standard soil the most significant diagonal effect was observed when T. repens origins were planted into sown swards of the grass competitors. Thus, it was argued that competition is the most probable explanation for the observed pattern, although local site conditions were also important. In 1989, Turkington’) published the results of a subsequent and much more rigorous transplantation experiment, following the procedure proposed by Connell’. This is the first paper to actually demonstrate a genetic shift in a population, a shift generated by competition. Unfortunately, the grass populations were not tested as rigorously as the clover; thus, the reciprocal event of coevolution is not demonstrated sufficiently. The reciprocal transplantation experiment of Gliddon and Trathanld is the sole reported instance where not only T. repens but also the coexisting grass competitor (Lolium perenne) were replanted into all possible sites. The genotypes of both species grew better when replanted back into their sites of origin than they did when transplanted to other sites. Since there were no denuded control plots in the different sites, the experiment was unable to distinguish between general site effects and possible local coevolution of neighbours. Therefore, Gliddon and TrathanlJ designed a competition experiment under standard conditions to investigate whether there was local specialization at the level of neighbouring plants of T. repens and L. perenne. Unfortunately, this experiment tested only the reaction of T. repens genotypes on the competition provoked by swards of different L. perenne genotypes and the reciprocal test of the performance of L. perenne in a 7. repensdominated environment was not included.

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Competition experiments where both competitors were observed are reported by various authors. Evans et a/.21,22 compared the performance of natural combinations of 7. repens and L. perenne populations, which they collected as seed samples in alpine regions, with mixtures of the same T. repens samples and L. perenne ‘testers’ fcultivars S23 and Ba94621. All five white clover populations gave the highest yields when grown with their coexisting grass. The coexisting mixtures also yielded more grass in spring than the mixtures with the two tester cultivars. The total yield of the natural combinations was 8.5% higher over a four-year period. These results were interpreted as evidence of selection for ecological combining ability resulting in niche separation of the two competitors. In 1990, Hill*j proposed a strategy for breeding mixtures with increased ecological combining ability of one or both mixture components. Aarssen and Turkington”, however, found that natural-neighbour pairs of T. repens and L. perenne did not differ significantly in total yield from pairs of nonnatural neighbours. But the clover yield was highest in the natural-neighbour combinations, while the L. perenne yield was lowest. This suggests that natural selection, in the context of competition, may result in more balanced competitive abilities for contested resources rather than niche differentiation. But this could only be a purely phenotypic effect. Recently, Chanway et a1.16 and Thompson et a/J7 included as a third biotic element (besides the two plant competitors) the root nodule bacterium Rhizobium leguminosarum biovar. trifolii. Their results indicate that the significant effect of the grass competitor on clover yield may be modified by strains of R. leguminosarum. Chanway et al.l6 found that biotic specialization between L. perenne and T. repens genotypes became apparent when natural-neighbour combinations of the plants were inoculated with the matching R. leguminosarum isolate. The authors hypothesized that in earlier work the T. repens-L. perenne specificity was apparent because of contamination of the plant material with its matching R. leguminosarum

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strains. A new paper by Chanway et aLI demonstrates that, besides the symbiotic R. leguminosarum. asymbiotic Bacillus isolates (that had coexisted in the field with the plants) also have an impact on the competitive interactions between the plant species. The evidence available to date suggests that natural selection results in adaptation of T. repens to site effects, to interspecific competitors and also to soil microorganisms. Further, the results seem to support both existing theories (niche differentiation and more balanced competitive abilities) about the role played by selection in preventing competitive exclusion. Potential limitations of previous work The initial reports of Turkington and Harper’? and Evans and Hill I 1982. Report of the Eucarpia Fodder Crop Meeting, Aberystwyth I were criticized by Snaydonz4. He argued that the study by Evans and Hill (see also Refs 21, 22) demonstrated a pitfall in the coevolution interpretation, since in this work the five populations of T. repens were not grown with each of the five cooccurring populations of L. pefenne. Instead, each population was grown only with its own co-occurring L. perenne population and two ‘tester’ populations (two cultivars). As a result, coadaptation cannot be assessed. Similar reservations have to be voiced concerning the ‘crucial test of biotic differentiation’ of Turkington and Harper12, carried out on standard soil in the glasshouse, since they used grass swards established from commercial seed samples. Criticism would be appropriate if testing was for coevolution, but species adaptation of white clover can be assessed. Turkington and HarperI did not interpret their results as evidence for coevolution because the corresponding grass populations were not tested. They interpreted them as a ‘microevolutionary response of white clover’, adding that ‘it would be interesting to look for a similar effect among grasses’. Furthermore, they did not ignore the site effect, and discussed it in relation to soil microorganism populations (Rhizobium leguminosarum and mycorrhizal in the different sites. This was recently elaborated by Chanway et a/.‘6,iA.

Similar effects among grasses are perhaps not so easy to find, since grasses are most often the main component of grassland while white clover frequently occurs in a minority. Further, in most environments, grasses are known to be stronger competitors than white clover for important nutrients and light. As a result, white clover is known to show a marked response in dry-matter production and morphology to different light qualities generated by different grass species2’. Grasses may thus be an important factor in white clover’s environment, while, on the other hand, for a grass plant it might be more important to be a strong intraspecific competitor. Indeed, there is no published experiment that gives evidence for the adaptation of a grass to its clover competitor. A further problem concerns the danger of carry-over effects from the sampling sites in the field’6,2’. Since the plant material is sampled in different environments in the field, the genotypes could show differences that are due to their growth conditions in the past and not to their genome. Under common garden conditions, a significant variability due to the growth conditions at the sampling sites was observed, which disappeared two years later. Since, in the experiments on biotic specialization of T. repens, the preconditioning period never markedly exceeded four months, it is to be feared that some carry-over effects could have influenced the results. However, the long period over which the experiments were harvested and observed (about one year), minimizes the danger of important carry-over effects, and the more rigorous experimental design of Connel17,‘3 circumvents this problem. The main problem to overcome is how to find populations that represent the precontact state and can serve as controls for observations of present-day populations. The assumption that allopatric populations represent precontact populations was stressed in work with animals, and some criteria were defined to ensure that allopatric populations did in fact represent precontact populations28,29. If the allopatric population has split up into subpopulations (due to competi-

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Fig. I. Resource partitioning in a hypothetical population that has split into subpopulations Each curve represents the resource utilization by a different subpopulation. Adding together the demands of all subpopulations produces the upper curve. The development of subpopulationscould have been induced by physical as well as biotic tactors working as selecting agents. To estimate allele frequencies in the original population of the species I before selection took place and divided it into subpopulationsl a representative sample of the different subpopulations has to be taken. Adapted tram Ref 30

tors or physical factors), as illustrated in Fig. I, we can estimate the genetic constitution of a precontact population from a representative sample of subpopulations. A real separation in time, however, can be found in fossils. There is some evidence for character shift in fossils of animals, but it is impossible to test experimentally the impact of such character shift on competition. In plant studies, however, an enormous advantage is conferred by the seeds that plants produce. In seeds lies the possibility of restoring to life earlier generations (‘fossils’) of the species and of testing their interactions with competitors. This, using preserved seed lots or seed samples extracted from the seed bank (provided that a prolonged ability to germinate is a trait of the species) provides a control against which to test whether evolutionary changes occur within populations. Conclusions The purpose of this article has been to review the evidence for the hypothesis that competition leads to interspecific coevolution. The results available to date are mainly related to the specific relationships between T. repens. a highly foraging modular organism. and fixed modular grasses. They suggest that natural selection results in adaptation of 7. repens to interspecific competitors land also to soil microorganisms and site effects). There is, however, no clear evidence whether the grass competitor has also evolved due to selection pressure from 7. repens. Hence, we should be conservative in using the word coevolution. Taking the described advantages of plants (immobility. clonabiiity 357

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and seed production) into account, the words of Bradshaw and Mortimer” are particularly pertinent: ‘It is a great pity that no further evidence is yet forthcoming for plants on a population basis, because direct experimental testing of niche differentiation in plants is so much simpler than in animals’. Acknowledgements The authors thank lohn Harper, Yan Linhart. john Connolly, Roy Turkington and an anonymous reviewer for very constructive comments on the manuscript, and lohn Thompson and Margaret Collinge for checking the English. We thank Eric Pianka for permission to reproduce the graph. This work was supported by the Swiss National Research Foundation.

References I Aarssen. L.W. I19831 Am. Naf. 122, 707-73 I 2 Aarssen. L.W. I19891 Oikos 56, 386-401 3 Tilman. D. (1988) P/ant Strategies and the Dynamics and Structure of Plant Communifies. Princeton University Press 4 lanzen, D.H. I19801 Evolufion 34,61 IL612

5 Futuyma. D.I. and Slatkin, M. I19831 in Coevolution Ifutuyma, D.I. and Slatkin. M., edsl. pp. l-l 3, Sinauer Associates 6 Roughgarden, I. 11983) in Coevolution Ifutuyma. D.I. and Slatkin. M., edsl. pp. 33-64, Sinauer Associates 7 Connell.I.H.11980~0ikos35. 131-138 8 Roughgarden, I. (19831 Am. Nat. 122. 583-60 I 9 Schoener. T.W. II9831 Am. Nat 122, 240-285 IO Connor, E.F. and Simberloff, D.S. I I9861 Am. Sci. 74, 155-162 II Sultan. S.E 119871 Eva/. Biol. 21. 127-178 I2 Turkington. R. and Harper, I.L. 119791 1. Ecol. 67, 245-254 I3 Turkington. R. II9891 1. Ecol. 77. 717-753 I4 Cliddon, C. and Trathan. P. II9851 in Structure and Functioning of Plant Populations IVol II) (Haeck. 1. and Woldendorp, I.W.. edsl, pp. 161-169. NorthHolland Publishing Company 15 Aarssen, L W. and Turkington. R. (19851 1. Ecol. 73.605614 I6 Chanway. C.P.. Hall. F.B. and Turkington. R. (I9891 1. Ecol. 77, 1150-I 160 I7 Thompson, I.D.. Turkington. R and Hall, F.B II9901 Can. 1. Bot. 68, 296-303 I8 Chanway. C.P. Hall. F.B. and Turkington, R. I I9901 Can 1. Bot. 68, I 126-l I30 I9 Mehrhoff. L.A. and Turkington, R. 119901

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1. Ecol. 78. 745-756 20 Connolly. I. II9881 Trends Ecol. Evol. 3, 24-26 21 Evans. D.R.. Hill. I.. Williams, T.A. and Rhodes, I. II9851 Oecologia 66, 536-539 22 Evans, D.R., Hill. I., Williams, T A. and Rhodes, I. I I9891 Theor. Appl. Cenet. 77, 65-70 23 Hill. I ( 19901 Theor. Appl. Cenet. 79, 168-176 24 Snaydon. R.W. II9851 in Structure and Functioning of P/ant Populations IVol II I IHaeck. I. and Woldendorp, I.W.. edsl, pp. 127-l 57, North-Holland Publishing Company 25 Thompson, L. and Harper, I.L. II9881 Oecologia 75, 343-347 26 Evans. R C. and Turkington. R. I I9881 New Phytol 109. 369-376 27 Turkington. R. II9891 1. Ecol. 77, 734-746 28 Grant. P R. l I9721 Biol. 1. Linn. Sot. 4, 39-68 29 Arthur. W. II9821 Adv Ecol. Res. 12. 127-187 30 Pianka. E.R. II981 I in Theoretical Ecology, 2nd edn IMay. R.M ed.1. pp. 167-196. Blackwell 31 Bradshaw. T. and Mortimer. M. II9861 in Community Ecology. Pattern and Process {Kikkawa. I and Anderson. D.I., edsl, pp. 309-34 I, Blackwell

SINES: ShortInterspersed Repeated Elements of theEukaryotic Genome Norihiro Okada Muth of lhc eukaryotic genonre is composed of a variely of repetitive sequences. Anlongst these, there are Iwo kinds o/retroposons (sequence elements derived from tlonviral cellular RNA): SINES (short interspersed elements I and LI N Es (lorIg interspersed elements). Amplificalion of SIN Es occurs in a single germ cell, and the members of SI N Es spread and become fixed in populalions through genetic drip. SINEs (fin be regarded as phylogenetic landma&s: Ihey are specific lo one species, a few species, a genius or in some cases a family, indicatirlg a specific lime of ampli/icalion durirrg evolution. Recent studies concerning the structure and origirl o/ many SINES revealed that refroposons are nlorc widcspread in animal genomes than was previously fhoughl. In higher eukaryotes, proteincoding genes constitute at most 10% of the genome, the rest being composed of a variety of repetitive seNorihiro Okada is at the Institute of Biological ences, University of Tsukuba. Tsukuba lbataki lapan.

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quences. Repetitive sequences in eukaryotic genomes are classified into two groups: tandemly repeated sequences and dispersed sequences. Dispersed sequences have been furtherclassified into two categories based on size: long interspersed elements (LINES), which include LI sequences, and short interspersed repetitive elements (SINES), such as the primate Alu and the rodent type I or 2 families’. Tandemly repeated sequences are generated by gene duplication at the DNA level, and many different mechanisms of gene duplication have been proposed to date, such as unequal cross-over, slippage of DNA synthesis, the ‘onion skin’ model and the ‘rolling circle’ mode12. For dispersed repeated sequences, another mechanism called retroposition3,J has recently been characterized, in which information in nonviral cellular RNA can flow back into the genome via cDNA (complementary DNA) intermediates. Retroposition creates 0

additional sequence combinations through dispersal of genetic information, and can shape and reshape eukaryotic genomes in many different ways.‘. The precise mechanism of retroposition is still unknown. The only agreement is that the generation of retroposons must involve a reverse transcriptase that copies nonviral cellular RNA to cDNA. The source of the reverse transcriptase, how cDNA synthesis is primed, and how the single-stranded cDNA becomes double-stranded DNA or is integrated into the genome, remain to be elucidated3,“. In this article, I will focus on several new topics of the generation and propagation of SINES, which have not been emphasized in previous reviews. Many SINES are derived from transfer RNA The first SINE to be well characterized was the human Alu family5-R. This family is made up of about 500000 copies of an approximately 300 bp DNA and thus constitutes about 5% of the human genome. On average, there is about one Alu el-

1991 Elsewcr Scence PuM?hcrs

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