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Will hybrids of genetically modified crops invade natural communities?
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that was not even suspected a decade ago. Sarah Ann Woodin and Sara Lindsay (University of South Carolina, Columbia, SC, USA) discussed negative settlement cues in which larvae avoid sources of mortality, and Dan Rittschof et al. (Duke University Marine Laboratory, Beaufort, NC, USA)considered chemosensory capabilities in the context of other stimuli that larvae may experience.
Techniques for larval ecologists Larval ecology has always suffered from the technical difficulties of finding, sampling, identifying and observing microscopic animals adrift in the sea. Many papers at the meeting introduced innovative techniques for overcoming these logistical difficulties. Some were elegantly simple (for example, Douglas Shapiro et al. captured clouds of fish gametes in plastic garbage bags to estimate egg and sperm numbers released in isolated spawning events). Other methods required expensive, newly engineered gadgetry. Cheryl Ann Butman (Woods Hole Oceanographic Institution, Woods Hole, MA, USA) described a new automated plankton pump modelled after the old continuous plankton recorders that were sometimes towed behind freighters, half a century ago. Butman’s pump can be placed on or near the sea floor and
programmed to collect plankton samples at discrete intervals. Scott Gallager et al., also of Woods Hole Oceanographic Institution, demonstrated results from a new underwater video system (‘Video Plankton Recorder’) that can be towed through the water column for sampling the fine-scale distribution of zooplankton. Using this new sampling method, Gallager et al. were able to correlate larval distributions with discrete water masses and observe the natural postures and orientations of various larval forms. Both of these new sampling techniques hold much promise. Enzyme electrophoresis and various DNAtechniques have been used for some time to infer larval dispersal among geographically isolated adult populations. An elegant eight-year study presented by Christopher Todd and Walter Lambert (Gatty Marine Laboratory, St Andrews, UK) showed little genetic variation among populations of nudibranchs along a 1500 mile range, regardless of whether they developed directly or with dispersing larvae. Larval ecologists are now beginning to use molecular methods for identifying larvae. Presentations by Randy Olson et al. (University of New Hampshire, Durham, NH, USA)and by Mary Alice Coffroth (State University of New York, Buffalo, NY, USA) detailed successful at-
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tempts to identify species-specific markers by amplifying adult and larval DNA with the polymerase chain reaction (PCR). A novel technique of marking larvae with calcium-binding fluorescent stains was presented by Bob Rowley (University of Otago, Dunedin, New Zealand). With renewed emphasis on field studies and a new arsenal of methods at its disposal, the discipline of larval ecology stands poised for tremendous new developments. The next meeting, which will be renamed the Larval Biology Meeting to allow a broader scope, will be held in the summer of 1995. Craig M. Young Harbor Branch Oceanographic Institution, 5600 US Hwy I N, Fort Pierce, FL 34946, lSA.
References Underwood, A.J. and Fahweather, P.G. (1989) Trends Ecol. Euol. 4, 16-20 Olson, R.R. (1985) Eco/osy 66,30-39 Levin, L.A. (1990) Ophelia 32, 115-144 Young, CM. (1990) Ophelia 32, 1-48 Thorson. G.L. (1950) Biol. Reo. 25, l-45 Pennington, J.T. (1985) Biol. Bull. 169,417-430 Levitan, D.R. (1991) Biol. Bull. 181,261-268 Denny, M.W.and Shibata, M.F. (1989)Am. kt 134,859-889 Anon. (1992) Northwest Atlantic Implementation Plan. US CLOBECReport Number 6
Will hybridsof geneticallymodifiedcrops invadenaturalcommunities? Alan F. Raybould and Alan 1. Gray
D
espite close similarities in A perceived danger of genetic modification from wild taxa and many such the phenotypes of some of crops is that crop hybrids may not only species have been transferred to transgenic and nontransbecome more-pernicious weeds of new regions where they have genie crop.+, transgenics agriculture but that they may also become naturalized. Obligate are perceived as posing special become invasive of natural communities. cultigens are highly domesticated risks. First, genetically modified New information on the extent of crop species that have usually lost crops may be toxic to humans or hybridization and the characteristics of the ability to survive in natural livestock, but this could easily be modified crops is facilitating morehabitats and include most crop tested. A less predictable outcome accurate assessments of these risks. species that are the targets of is that the transgene could ‘escape’ genetic modification. Hybridizfrom agriculture and have an unation and introgression between Alan Raybould and Alan Gray are at the Institute of desirable impact on the environobligate cultigens and wild species Terrestrial Ecology, Furzebrook Research Station, ment’,‘. Escape can occur if the may remove deleterious (in natuWareham, Dorset, UK BH20 5AS. crop persists after harvest and ral habitats) crop traits, or add becomes a weed of cultivation, or traits from the wild species, that .. establishes feral populations outside agricultural land. allow these crops to escape from agriculture. Alternatively, the transgene may be transferred to another Crops and wild relatives growing nearby often have crop or a wild species by sexual hybridization, and the similar morphology. This is not necessarily evidence of hybrid (or the product of further introgression) may introgression, as under intense selection, such as hand become a weed. weeding, forms of the wild plants that mimic the crop are Crops can be divided into facultative and obligate favouredd. New work using molecular markers is now cultigens”. Facultative cultigens may not differ genetically resolving whether such morphological similarity is due to 0 1994. Elsevier Science I.td
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REVIEWS gene flow or to convergent evolution. The relatively few examples where introgression has been shown to be the cause are shown in Table 1. Where introgression has occurred, the products have tended to colonize agricultural or disturbed habitats (Table 1). However, if genetic modification of crops alters the probability of hybrid formation or the performance of hybrids, then natural and semi-natural habitats, as well as man-made habitats may be invaded by hybrids carrying the modification. Data are now accumulating that will allow predictions of the effect of genetic modification on such processes. Hybrid formation Genetic modification may affect hybrid formation either by changing the frequency with which it occurs, or by altering the range of species with which the crop is sexually compatible. Increasingly the evidence suggests that modification has little impact on either factor. In general, plant fertility is maintained following genetic modification, although there are instances where a particular transformation protocol has produced sterile plants. For example, genetically modified maize regenerated from protoplasts was sterile if the protoplasts were transformed by electroporatio+‘, but fertile if transformed by polyethylene glycoll3. Fertility problems in transgenics may, there fore, be due to particular combinations of transformation protocol and starting material rather than transformation per se. It is unlikely that sterile transgenics would be of commercial interest as they are unsuitable for breeding purposes. It may be assumed, therefore, that commercial transgenic crop varieties will show similar fertility to nontransgenics. One exception to this is crops specifically modified for male sterility. These crops are useful to breeders when they wish to avoid selfing or particular patterns of maternal inheritance. Several methods of producing male sterility in transgenic plants are now being introduced, including anther-specific expression of ribonuclease genesl4, antisense expression of flavonoid biosynthesis genes15, and nuclear expression of unedited mitochondrial genome sequence+. In the case of ribonuclease genes, fertility can be restored by crosses to plants transformed with the appropriate ribonuclease inhibitor genel7. Male sterility could also be used to prevent release of transgenic pollen in cases where the crop is highly interfertile with wild relatives.
Numerous studies have shown that, when a transgene is integrated as a single copy, its inheritance is mendelian, whereas transgenes integrated as multiple copies show complex inheritance and often reduced expressioni8. As breeders are almost certain to require simple patterns of inheritance and high expression of transgenes, the majority of releases will involve crops with a low copy number of the transgene showing mendelian segregation. The population genetics of traits encoded by transgenes may, therefore, be modelled using data on similar, naturally occurring, single gene traits. One of the most important determinants of the extent of hybridization is the movement of fertile pollen to a receptive stigma. Clearly, pollen production in the crop and stigma-ripening in the wild relative must be concurrent. If the phenology of a modified crop is different from the unmodified form, then the potential for hybridization will be changed. Several genetic modifications have produced alterations in flower developmentlgJ0, but these tend to be changes in structure, leading to morphologically abnormal flowers rather than the production of normal flowers with different flowering times. These experiments have used genes known to be involved in flower development, or promoters only activated in floral tissue. Transformation, in general, does not appear to alter flowering time; however, as flowering time is a multigenic trait there is a possibility that a transgene may integrate into, and disrupt the expression of, a gene involved in floweringtime determination. Assuming simultaneous flowering times, the extent of pollen movement will determine the potential for crop pollen to alight on the stigma of a wild relative. Pollen flow, in most cases, describes a highly leptokurtic distribution from the source plant, with most grains moving less than 2 m in herbaceous plant.9 (recent work confirms this for transgenic pollen22-24). However, to conclude from these data that hybridization between crops and wild plants can only occur over short distances is misleading. Investigations using genetic markers are revealing considerable variation in gene flow between discontinuous patches of plants. This variation is not necessarily related to the interpatch distance, and the amount of gene flow between patches can be substantial and occur over long distances’. For example, gene flow has been demonstrated over distances of 1000m or more in species of Ruphanus2~ and Curcurbiraa.
Table 1. Introgression between crops and wild species Crop
Crop relative
Evidence for hybridization
Habitat of hybrid
Refs
Beta vulgaris
Beta maritima a
Boltersb Nuclear and chloroplast RFLPs
Beet fields and field margins
56
Chenopodium quinoa
C. berlandieri
lsozymes
Roadsides and field margins
7
Curcurbia pepo
C. texana
lsozymes
Drainage ditches
8
Daucus carota ssp. sativus
Daucus carota ssp. carota
Bolters White roots
Carrot fields
9
Dryza sativa
‘Red rice’c
lsozymes
Rice fields
10
Zea mays
Teosinte spp.
lsozymes
Presence of Zea mays alleles in adjacent teosinte populations
11
aPlants were assumed to be B. maritima, although they may be weedy populations of B. vulgaris. bBolters are plants of normally biennial species which flower in the first year of growth. CThe status of ‘red rice’ in this study is unclear. It may be a feral population of cultivated rice or a closely related species, accidentally with the cultivated species.
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0. rufipogon, that was introduced
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REVIEWS Some transgenic phenotypes have more-or-less exact Accumulated evidence from many studies allows some equivalents in crops and wild species and may be advangeneralizations to be made about how the pollination mechanism and breeding system of a crop will affect both tageous in natural communities, whilst others are compollen transfer to wild relatives and also the subsequent pletely novel or are only found in plants that have been spread of genes in natural populations. Gene flow may subject to strong selection by human influence (herbicide occur over longer distances in outbreeders and wind-polli- resistance, for example). Knowledge of traits that are phenonated species, compared with inbreeders and insect-pollitypically similar to those of genetically modified crops nated plants. For example, isozyme and RFLP data indi- may allow the consequences of the escape of transgenes cate that on the Dorset coast (UK) wild populations of to be predicted with more confidence than in cases where Brassica oleracea, an insect-pollinated species, are gen- no wild equivalent is known. For example, there are many etically more highly structured than adjacent populations methods of producing disease resistance by transformof Be& maritima which is pollinated by wind (Raybould ation (Table 2). Data on the maintenance of disease reand Gray, unpublished). These generalizations should hold sistance polymorphisms in natural populations are now for transgenic crops22-24providing the period of viability accumulating50, and will be very valuable in predicting how of transgenic pollen is similar to nontransgenic pollen. transgenes conferring disease resistance might behave in Pollination is a major determinant of the rate of hybridnatural populations. ization, but the types of hybrid are determined by interThere are, however, important differences between specific incompatibility mechanisms. The genetics of these natural and transgenic resistance which need to be conmechanisms is still not clear. Unless interspecific incomsidered in models. First, transgenic resistances are often patibility is controlled by one or a small number of genes, based on genes derived from the pathogen and have no then transformation is unlikely to alter the cross-compatiexact natural counterpart. Second, in natural resistances bility of plants following transformation. genes are frequently expressed only in particular tissues Many intraspecific self-incompatibility (SI) mechanisms (seeds, for example) and/or at particular times (for instance are now well characterized genetically. Several species have after wounding). Many genes bestowing genetically modimechanisms based on a single (S-) locus with multiple fied resistance are expressed from the cauliflower mosaic virus 35s RNA promoter, which in most cases gives conalleles, and a match between the allele in the stigma and the pollen causes inhibition of pollen growth. Recently S- stitutive (continuous in all tissues) expression in plants. locus alleles have been cloned and have been transferred to, and correctly expressed Table 2. Examples of disease and pest resistances introduced into plants in, self-compatible species, by genetic modification although all plants have so far remained selfcompatible2”,2’. Transgenic Pathogen/Pests resistant host Resistance gened Transformation of a species possessing SI with an S-allele PVX/PW/PLRV Potato CP has also been achieved and Antisense to CP the plants became selfcompatRat 2’-5’ oligoadenylate synthetase ible? Introduction of Sl into CP TMV/ToMV Tomato self-compatible species will TGMV Tobacco Antisense to TGMV AL1 gene be useful to plant breeders, CMV Tobacco CMV satellite but it is not clear whether Sl Pseudomonas syringae pv. tabaci Tobacco Tabtoxin detoxification enzyme is involved in interspecific inBarley endosperm thionin compatibility, and, therefore, P. syringae pv. phaseolicola Tobacco Phaseolotoxln-reslstant ornithyl such modifications can be transcarbamylase expected to have little effect P. solanacearum Tobacco Cecropin B lytic peptide analogue on interspecific hybridization. Persistence and spread It is improbable that genetic modification will change the rate at which crops hybridize with wild relatives, or the range of species with which they are sexually compatible. Modification may, however, alter the fitness of hybrids and this might result in greater persistence, faster rates of spread or the ability to invade new habitats. Precise effects are difficult to predict as one must consider all stages of the plant’s life cycle and a variety of habitats, although it is possible to highlight some general principles based on the type of modification.
Erwinia carotovora
Potato
Bacteriophage T, lysozyme
Rhizoctonia solani
Tobacco
Bean chitinase Barley ribosome-inactivating
Refs 29 30 31 32 33 34 35 36 37 38 39
protein
40 41
Botrytis cinerea
Tobacco
Grapevine stilbene synthase
42
Perenospora tabacina/ Phytophthora parasitica
Tobacco
Tobacco pathogenesis-related protein la
43
Tobacco hornworm
Tobacco
Bacillus thunngiens,s lCPb
51
Tobacco hornworm
Tomato
B. thuringiensis ICP
44
Cotton
B. thuringiensis ICP
45
Poplar
8. thuringiensis ICP
46
Striped stemborer/Leaffolder
Rice
8. thunngiensis ICP
47
Colorado beetle
Potato
8. thuringiensis ICP
48
Tobacco budworm
Tobacco
Cowpea trypsln Inhibitor
49
Cabbage looper/Beet Cotton bollworm
armyworm/
Forest tent caterpillar/Gypsy
moth
aAbbreviations: CMV, cucumber mosaic virus; CP, coat protein; TGMV, tomato golden mosaic virus; TMV, tobacco mosaic virus; ToMV, tomato mosaic virus: PLRV, potato leafroll virus; PVX, potato virus X; PVY, potato virus Y. blCP, insect control protein; occurs as several forms depending on the strain of 6. thuringiensis.
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REVIEWS This could be particularly important in the case of phytophagous insects which could be continuously exposed to defence compounds, and has implications for possible deleterious effects on nontarget insects, particularly if the gene escapes into a wild relative that is the sole foodplant of a particular species. The speed with which tolerance to the resistance mechanism might evolve may also have a bearing. Constitutive expression may be a shortlived concern, however, because plant-promoter sequences are now being isolated which confer tissue-specific and temporally specific expression of transgenes. For example, Williams et al.51 designed a chimaeric gene using the promoter from the tobacco PR (pathogenesis related) la gene, and coding sequences from the insect control proteingene from Bacillus thuringiensis. Tobacco plants transformed with this construct were resistant to feeding by tobacco hornworm larvae only after plants were treated with simple chemicals (such as salicylic acid) that induce PRla expression. Also, other workers have demonstrated expression of genes from wound-inducible promoters only following mechanical damage or feeding by insect&s. Modifications which confer a trait that has no wild equivalent and/or has no obvious beneficial effects, other than in agricultural environments, include herbicide and antibiotic resistances and the production of pharmaceuticals and industrial chemicals. The appropriate questions here are whether the possession of a transgene, in the absence of selection for that gene, imposes a cost on the plant (a ‘yield penalty’) or whether it has unforeseen effects leading to greater invasiveness. Evidence is increasing which suggests that plants possess spare metabolic capacity so the production of protein coded by a transgene in the absence of selection does not impose a cost to the plantlJ4. This means that such transgenes may behave as neutral genes in natural populations, and hence their spread can be modelled using data from markers such as isozymes and RFLPs which are also assumed to be neutral. Although there is good evidence that the direct effects of transgenes for traits such as herbicide resistance may be neutral with regard to fitness in natural environments, there is less information on whether unanticipated pleiotropic effects of these genes could be advantageous. Recent results from Crawley et a1.55, however, show no evidence for enhanced weediness in trans-
Box 1. The invasiveness of transgenic oilseed rape in natural habitats A plant will invade an area if its finite rate of increase, h, is >l, and it will become extinct if h
+ g(l-d>)F
where dI is the proportion of seed that dies in one full year; g is the proportion of seed that germinates in the spring of year one; d2 is the proportion of seed that dies in the winter between years one and two: and Fis the mean number of seed produced per seed that germinates. Crawley et a/.55 estimated these parameters for oilseed rape in three climatically different sites and four habitats within each site (wet versus dry, sunny versus shaded), giving 12 environments. In each environment experimental treatments were established involving the presence or absence of vertebrate grazers, invertebrate grazers, fungal pathogens and background perennial vegetation. Three lines of the same rape cultivar were used: transgenic herbicide resistant, transgenic antibiotic resistant and nontransgenic. In no instance was A for transgenics >h for nontransgenics. Also, h>l only occurred in treatments where vegetation was removed, showing the preference of rape for disturbed habitats.
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genie Brassica napus expressing herbicide or antibiotic resistances (Box 1). This experiment was performed with a crop plant rather than a hybrid, hence the ‘genetic baggage’ of the crop may have concealed any possible effects of the transgenes on invasiveness. Nevertheless, this is an important experiment and paves the way for future investigations of the fitness of genetically modified plants in nonagricultural environments. Conclusions Molecular markers are revealing the true extent of hybridization and introgression between crops and wild plants. There is now ample evidence that transformation should not affect the rate or extent of hybridization, hence the information on introgression of nontransformed crop genes gives a basis for assessing the potential for transfer of genetic modifications to wild relatives. The increasing sophistication of modifications, giving control of temporal and spatial expression of transgenes, will enable transformation to mimic naturally occurring phenotypes such as disease resistance, and information on the maintenance of resistance in natural populations will allow the modelling of the effects of these modifications should they be transferred to wild plants. With novel phenotypes, the performance of the gene in natural habitats and in several genetic backgrounds will need to be tested directly. Acknowledgements We would like to thank Dr Norman Ellstrand and two anonymous
reviewers
the original
manuscript.
for suggesting
improvements
to
References Raybould, A.F. and Gray, A.J. (1993) J. Appt. Ecot. 30,199-219 Ellstrand, N.C. and Hoffmann, CA. (1990) Bioscience 40,438-442 Sukopp, H. and Sukopp, U. (1993) Experientia 49,21 l-218 Barrett, S.C.H.(1983) Icon. Bat. 37,255-283 Santoni, S. and BervillC,A. (1992) PIantMol.Riot. 20,578-580
Boudry, P., Miirchen, M., Saumitou-Laprade, P., Vernet, Ph. and van Dijk, H. Theor. Appt. Genet. (in press) 7 Wilson, H.D. and Manhart, J. (1993) Theor. Appl. Genet. 86,642-648 8 Kirkpatrick, K.J. and Wilson, H.D. (1988) Am. J. Rot. 75,519-527 9 Wijnheijmer, E.H.M.,Brandenburg, W.A. and Ter Borg, S.J. (1989) Euphytica 40,147-154 10 Langevin, S.A.,Clay, K. and Grace, J.B. (1990) Euolution 44,1000-1008 11 Doebley, J. (1990) Bioscience 40,443448 12 Rhodes, CA., Pierce, D.A.,Mettler, I.J., Mascarenhas, D. and Detmer, J.J. (1988) Science 240,204-207 13 Omirulleh, S. et at. (1993) Plant Mot. Riot. 21,415-428 14 Mariani, C., de Beuckeleer, M., Truettner, J., Leemans, J. and Goldberg, R. (1990) Nature 347, 737-741 15 van der Meer, I.M., Stam, M.E.,van Tunen, A.J., Mel, J.N.M. and Stuite, A.R. (1992) The Plant Cett 4,253-262 16 Hernoufd, M., Suharsono, S., Litvak, S., Araya, A. and Mouras, A. (1993) Proc. Nat1Acad Sci. USA 90,2370-2374 17 Mariani, C. et al. (1992) Nature 357,384-387 18 Grierson, D., Fray, R.G., Hamilton, A.J., Smith, C.J.S. and Watson, CF. (1991) Trends Biotechnol. 9, 122-123
19 Mizukami, Y. and Ma, H. (1992) Cell 71,119-131 20 Mandel, M.A.et al. (1992) Cell 71, 133-143 21 Levin, D.A. and Kerster, H.W. (1974) Evol. Biot. 7, 139-220 22 Tynan, J.L., Williams, M.K.and Connor, A.J. (1989) J. Cenet. Breed. 23 24 25 26 27 28
44,303-306 Umbeck, P.F. et at. (1991) J. Econ. Entomol. 84, 1943-1950 Morris, W.F., Kareiva, P.M. and Raymer, P.L. Ecol. Appl. (in press) Ellstrand, N.C. and Marshall, D.L. (1985) Am. Nat. 126,606-616 Nishio, T. et at. (1992) Sex. Plant Reprod. 5, 101-109 Murfett, .I.et al. (1992) Plant Cell 4, 1063-1074 Toriyama, K. et at. (1991) Theor. Appt. Genet. 81,769-776 TREE uol. 9, no. .3 March
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REVIEWS 29 Huisman, M.J., Cornelissen, B.J.C. and Jongedijk, E. (1992) Euphytica 63, 187-197 30 Kawchuk, L.M., Martin, R.R. and McPherson, J. (1991) Mol. Plant-Microbe Interact. 4,247-253 31 Truve, E. et al. (1993) Bio/Techno/ogv 11, 1048-1052 32 Nelson, R.S. et a/. (1988) Bio/Technology 6,403-409 33 Bejarano, E.R. and Lichtenstein, C.P. (1992) Trends Biotechnot. 10, 383-388 34 Harrison, B.D.. Mayo, M.A.and Baulcombe, B.D. (1987) Nature 328, 799-802 35 Anzai, H., Yoneyama, K. and Yamaguchi, I. (1989) Mol. Cen. Genet.
219,492-494 36 Carmona, M.J., Molina, A., Fernlndez, J.A., L6pez-Fando, J.J. and Garcia-Olmedo. F. (1993) P/ant 1 3,457-462 37 de la Fuente-Martinez, J.M., Mosqueda-Cano, G., Alvarez-Morales, A. and Herrera-Estrella, L. (1992) Bio/Techno/ogy 10, 905-910 38 Jaynes, J.M. et a[. (1993) P/ant .Sci.89,43-53 39 During, K., Porsch, P., Fladung, M. and Liirz, H. (1993) P/ant Mol. Biol. 15,281-293 40 Broglie, K. et a/. (1991) Science 254, 1194-1197
41 Logemann, J., Jach, C., Tommerup, H., Mundy, J. and Schell. J. (1992) Bio/Technology 10,305-308 42 Hain, R. et al. (1993) Nature 361, 153-156 43 Alexander, D. et al. (1993) froc. Nat/Acad. Sci. USA 90, 7327-7331 44 Delanney, X. et at. (1989) Bio/Technology 7, 126.5-1269 45 Perlak, F.J. et al. (1990) Bio/Technology 8, 939-943 46 McCown, B.H. et al. (1991) flunt Cell Rep. 9,590-594 47 Fujimoto, H., Itoh, K., Yamamoto, M., Kyozuka, J. and Shimamoto, K. (1993) Bio/Technotogy 11. 1151-1155 48 Adang, M.J. etal. (1993)flant Mol. Biol. 21. 1131-1145 49 Hilder, V.A.,Gatehouse, A.M.R.,Sheerman. SE.. Barker, R.F. and Boulter, D. (1987) Nature 300, 160-163 50 Parker, M.A. (1993) Hered@ 71,290-294 51 Williams, S. et al. (1992) Bio/Technology 10,540-543 52 SanchezSerrano, J.J., Keil, M., O’Connor, A., Schell. J. and Willmitzer, L. (1987) EMBOJ. 6,303-306 53 Thornburg, R.W.,Keman, A. and Molin,L. (1990)P/ant Physiol.92,500505 54 Hilder, V.A.and Gatehouse, A.M.R.(1991) Transgenic Res. 1,54-60 55 Crawley, M.J., Hails, R.S., Rees, M., Kohn, D. and Buxton, J. (1993) Nature 363,620-623
Cooperativebreedingin mammals Michael D. Jennions and David W. Macdonald
M
ost studies of cooperative breeding in vertebrates have been on birdslJ. This has led to the development of a concep tual framework which is generally assumed to be applicable to mammals. While most of the experimental and correlational tests have also been on bird+, new research on cooperative breeding in mammals provides an opportunity to investigate the generality of bird-based models.
Cooperative breeding in mammals covers a diversity of breeding systems. In all cases, however, individuals assist in the rearing of offspring other than their own. Recent research has highlighted some of the factors responsible for variation both within and between species. While it is possible to generalize about the selective pressures leading to cooperative breeding, doing so may obscure important contrasts between taxa. Of course, inclusive-fitness models explain the generalities of cooperative breeding, but differences in ecology, physiology and life history may result in distinctive processes operating in different taxa-data only likely to emerge from long-term field studies.
Is ‘helping’ beneficial for breeders? An important variable in co-
operative-breeding models is the influence of helping on breeder fitness, and correlational evidence is often used to calculate the magnitude of this effect. Positive relationships between the number of helpers and reproductive success have been recorded for some mammals Fable l), but others have failed to show this effect. However, relationships are potentially confounded by factors covarying with group size, like What is cooperative breeding? breeder experience or territory In the bird literature, cooperquality3Jl. This problem can be ative breeding is defined as a situaddressed through experimental ation where ‘more than a pair of Michael Jennions and David Macdonald are at the manipulation. In birds, by removindividuals exhibit parent-like Wildlife Conservation Research Unit, Dept of Zoology, ing helpers, two studies have [helping] behaviour towards University of Oxford, South Parks Road, Oxford, shown that helpers are beneficial, young of a single nest or brood’4. UK OX1 3PS. and a third that they have no disIn mammals, this type of behavcernible effect”. Experimental reiour has been recorded in numermovals have been carried out on two mammals - prairie ous taxa, ranging from rodents to elephants5J. Activities defined as ‘helping’ in mammals (see Box 1) include feed- voles (Micro&s ochrogasfer) and pine voles (Microtus pinetorwn)l*J3. In both species, philopatric juveniles groom ing, grooming, babysitting7, helping infants in distresss, assistance in thermoregulationg and allosucklinglo. In and brood young and assist in burrow maintenance. practice, ‘helping’ has been used to describe any activity Statistically significant differences in some reproductive variables were recorded (Table 2). Although suggestive of directed towards infants or their parents which is likely to increased life-time reproductive success for breeders benefit the recipients and increase breeding success (e.g. alarm calling or provisioning a pregnant female). By defi- with helpers, it remains to be shown that these effects translate into increased breeder fitness. nition, then, all animals which are social during the breedFurther experimental removals may clarify the situation, ing season are cooperative breeders. We suspect, however, but their results will need to be interpreted with caution. that workers are most interested in a subset of costly First, groupsize effects may be responsible for the increased helping behaviours - those which appear to decrease the donor’s direct fitness relative to that it would possess if it reproductive success of breeders in larger groups”. Many cooperatively breeding mammals are highly social, did not perform these activities (Box 2). TREE uoi.
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that was not even suspected a decade ago. Sarah Ann Woodin and Sara Lindsay (University of South Carolina, Columbia, SC, USA) discussed negative settlement cues in which larvae avoid sources of mortality, and Dan Rittschof et al. (Duke University Marine Laboratory, Beaufort, NC, USA)considered chemosensory capabilities in the context of other stimuli that larvae may experience.
Techniques for larval ecologists Larval ecology has always suffered from the technical difficulties of finding, sampling, identifying and observing microscopic animals adrift in the sea. Many papers at the meeting introduced innovative techniques for overcoming these logistical difficulties. Some were elegantly simple (for example, Douglas Shapiro et al. captured clouds of fish gametes in plastic garbage bags to estimate egg and sperm numbers released in isolated spawning events). Other methods required expensive, newly engineered gadgetry. Cheryl Ann Butman (Woods Hole Oceanographic Institution, Woods Hole, MA, USA) described a new automated plankton pump modelled after the old continuous plankton recorders that were sometimes towed behind freighters, half a century ago. Butman’s pump can be placed on or near the sea floor and
programmed to collect plankton samples at discrete intervals. Scott Gallager et al., also of Woods Hole Oceanographic Institution, demonstrated results from a new underwater video system (‘Video Plankton Recorder’) that can be towed through the water column for sampling the fine-scale distribution of zooplankton. Using this new sampling method, Gallager et al. were able to correlate larval distributions with discrete water masses and observe the natural postures and orientations of various larval forms. Both of these new sampling techniques hold much promise. Enzyme electrophoresis and various DNAtechniques have been used for some time to infer larval dispersal among geographically isolated adult populations. An elegant eight-year study presented by Christopher Todd and Walter Lambert (Gatty Marine Laboratory, St Andrews, UK) showed little genetic variation among populations of nudibranchs along a 1500 mile range, regardless of whether they developed directly or with dispersing larvae. Larval ecologists are now beginning to use molecular methods for identifying larvae. Presentations by Randy Olson et al. (University of New Hampshire, Durham, NH, USA)and by Mary Alice Coffroth (State University of New York, Buffalo, NY, USA) detailed successful at-
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tempts to identify species-specific markers by amplifying adult and larval DNA with the polymerase chain reaction (PCR). A novel technique of marking larvae with calcium-binding fluorescent stains was presented by Bob Rowley (University of Otago, Dunedin, New Zealand). With renewed emphasis on field studies and a new arsenal of methods at its disposal, the discipline of larval ecology stands poised for tremendous new developments. The next meeting, which will be renamed the Larval Biology Meeting to allow a broader scope, will be held in the summer of 1995. Craig M. Young Harbor Branch Oceanographic Institution, 5600 US Hwy I N, Fort Pierce, FL 34946, lSA.
References Underwood, A.J. and Fahweather, P.G. (1989) Trends Ecol. Euol. 4, 16-20 Olson, R.R. (1985) Eco/osy 66,30-39 Levin, L.A. (1990) Ophelia 32, 115-144 Young, CM. (1990) Ophelia 32, 1-48 Thorson. G.L. (1950) Biol. Reo. 25, l-45 Pennington, J.T. (1985) Biol. Bull. 169,417-430 Levitan, D.R. (1991) Biol. Bull. 181,261-268 Denny, M.W.and Shibata, M.F. (1989)Am. kt 134,859-889 Anon. (1992) Northwest Atlantic Implementation Plan. US CLOBECReport Number 6
Will hybridsof geneticallymodifiedcrops invadenaturalcommunities? Alan F. Raybould and Alan 1. Gray
D
espite close similarities in A perceived danger of genetic modification from wild taxa and many such the phenotypes of some of crops is that crop hybrids may not only species have been transferred to transgenic and nontransbecome more-pernicious weeds of new regions where they have genie crop.+, transgenics agriculture but that they may also become naturalized. Obligate are perceived as posing special become invasive of natural communities. cultigens are highly domesticated risks. First, genetically modified New information on the extent of crop species that have usually lost crops may be toxic to humans or hybridization and the characteristics of the ability to survive in natural livestock, but this could easily be modified crops is facilitating morehabitats and include most crop tested. A less predictable outcome accurate assessments of these risks. species that are the targets of is that the transgene could ‘escape’ genetic modification. Hybridizfrom agriculture and have an unation and introgression between Alan Raybould and Alan Gray are at the Institute of desirable impact on the environobligate cultigens and wild species Terrestrial Ecology, Furzebrook Research Station, ment’,‘. Escape can occur if the may remove deleterious (in natuWareham, Dorset, UK BH20 5AS. crop persists after harvest and ral habitats) crop traits, or add becomes a weed of cultivation, or traits from the wild species, that .. establishes feral populations outside agricultural land. allow these crops to escape from agriculture. Alternatively, the transgene may be transferred to another Crops and wild relatives growing nearby often have crop or a wild species by sexual hybridization, and the similar morphology. This is not necessarily evidence of hybrid (or the product of further introgression) may introgression, as under intense selection, such as hand become a weed. weeding, forms of the wild plants that mimic the crop are Crops can be divided into facultative and obligate favouredd. New work using molecular markers is now cultigens”. Facultative cultigens may not differ genetically resolving whether such morphological similarity is due to 0 1994. Elsevier Science I.td
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REVIEWS gene flow or to convergent evolution. The relatively few examples where introgression has been shown to be the cause are shown in Table 1. Where introgression has occurred, the products have tended to colonize agricultural or disturbed habitats (Table 1). However, if genetic modification of crops alters the probability of hybrid formation or the performance of hybrids, then natural and semi-natural habitats, as well as man-made habitats may be invaded by hybrids carrying the modification. Data are now accumulating that will allow predictions of the effect of genetic modification on such processes. Hybrid formation Genetic modification may affect hybrid formation either by changing the frequency with which it occurs, or by altering the range of species with which the crop is sexually compatible. Increasingly the evidence suggests that modification has little impact on either factor. In general, plant fertility is maintained following genetic modification, although there are instances where a particular transformation protocol has produced sterile plants. For example, genetically modified maize regenerated from protoplasts was sterile if the protoplasts were transformed by electroporatio+‘, but fertile if transformed by polyethylene glycoll3. Fertility problems in transgenics may, there fore, be due to particular combinations of transformation protocol and starting material rather than transformation per se. It is unlikely that sterile transgenics would be of commercial interest as they are unsuitable for breeding purposes. It may be assumed, therefore, that commercial transgenic crop varieties will show similar fertility to nontransgenics. One exception to this is crops specifically modified for male sterility. These crops are useful to breeders when they wish to avoid selfing or particular patterns of maternal inheritance. Several methods of producing male sterility in transgenic plants are now being introduced, including anther-specific expression of ribonuclease genesl4, antisense expression of flavonoid biosynthesis genes15, and nuclear expression of unedited mitochondrial genome sequence+. In the case of ribonuclease genes, fertility can be restored by crosses to plants transformed with the appropriate ribonuclease inhibitor genel7. Male sterility could also be used to prevent release of transgenic pollen in cases where the crop is highly interfertile with wild relatives.
Numerous studies have shown that, when a transgene is integrated as a single copy, its inheritance is mendelian, whereas transgenes integrated as multiple copies show complex inheritance and often reduced expressioni8. As breeders are almost certain to require simple patterns of inheritance and high expression of transgenes, the majority of releases will involve crops with a low copy number of the transgene showing mendelian segregation. The population genetics of traits encoded by transgenes may, therefore, be modelled using data on similar, naturally occurring, single gene traits. One of the most important determinants of the extent of hybridization is the movement of fertile pollen to a receptive stigma. Clearly, pollen production in the crop and stigma-ripening in the wild relative must be concurrent. If the phenology of a modified crop is different from the unmodified form, then the potential for hybridization will be changed. Several genetic modifications have produced alterations in flower developmentlgJ0, but these tend to be changes in structure, leading to morphologically abnormal flowers rather than the production of normal flowers with different flowering times. These experiments have used genes known to be involved in flower development, or promoters only activated in floral tissue. Transformation, in general, does not appear to alter flowering time; however, as flowering time is a multigenic trait there is a possibility that a transgene may integrate into, and disrupt the expression of, a gene involved in floweringtime determination. Assuming simultaneous flowering times, the extent of pollen movement will determine the potential for crop pollen to alight on the stigma of a wild relative. Pollen flow, in most cases, describes a highly leptokurtic distribution from the source plant, with most grains moving less than 2 m in herbaceous plant.9 (recent work confirms this for transgenic pollen22-24). However, to conclude from these data that hybridization between crops and wild plants can only occur over short distances is misleading. Investigations using genetic markers are revealing considerable variation in gene flow between discontinuous patches of plants. This variation is not necessarily related to the interpatch distance, and the amount of gene flow between patches can be substantial and occur over long distances’. For example, gene flow has been demonstrated over distances of 1000m or more in species of Ruphanus2~ and Curcurbiraa.
Table 1. Introgression between crops and wild species Crop
Crop relative
Evidence for hybridization
Habitat of hybrid
Refs
Beta vulgaris
Beta maritima a
Boltersb Nuclear and chloroplast RFLPs
Beet fields and field margins
56
Chenopodium quinoa
C. berlandieri
lsozymes
Roadsides and field margins
7
Curcurbia pepo
C. texana
lsozymes
Drainage ditches
8
Daucus carota ssp. sativus
Daucus carota ssp. carota
Bolters White roots
Carrot fields
9
Dryza sativa
‘Red rice’c
lsozymes
Rice fields
10
Zea mays
Teosinte spp.
lsozymes
Presence of Zea mays alleles in adjacent teosinte populations
11
aPlants were assumed to be B. maritima, although they may be weedy populations of B. vulgaris. bBolters are plants of normally biennial species which flower in the first year of growth. CThe status of ‘red rice’ in this study is unclear. It may be a feral population of cultivated rice or a closely related species, accidentally with the cultivated species.
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0. rufipogon, that was introduced
TREE 001. 9, no. 3 March
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REVIEWS Some transgenic phenotypes have more-or-less exact Accumulated evidence from many studies allows some equivalents in crops and wild species and may be advangeneralizations to be made about how the pollination mechanism and breeding system of a crop will affect both tageous in natural communities, whilst others are compollen transfer to wild relatives and also the subsequent pletely novel or are only found in plants that have been spread of genes in natural populations. Gene flow may subject to strong selection by human influence (herbicide occur over longer distances in outbreeders and wind-polli- resistance, for example). Knowledge of traits that are phenonated species, compared with inbreeders and insect-pollitypically similar to those of genetically modified crops nated plants. For example, isozyme and RFLP data indi- may allow the consequences of the escape of transgenes cate that on the Dorset coast (UK) wild populations of to be predicted with more confidence than in cases where Brassica oleracea, an insect-pollinated species, are gen- no wild equivalent is known. For example, there are many etically more highly structured than adjacent populations methods of producing disease resistance by transformof Be& maritima which is pollinated by wind (Raybould ation (Table 2). Data on the maintenance of disease reand Gray, unpublished). These generalizations should hold sistance polymorphisms in natural populations are now for transgenic crops22-24providing the period of viability accumulating50, and will be very valuable in predicting how of transgenic pollen is similar to nontransgenic pollen. transgenes conferring disease resistance might behave in Pollination is a major determinant of the rate of hybridnatural populations. ization, but the types of hybrid are determined by interThere are, however, important differences between specific incompatibility mechanisms. The genetics of these natural and transgenic resistance which need to be conmechanisms is still not clear. Unless interspecific incomsidered in models. First, transgenic resistances are often patibility is controlled by one or a small number of genes, based on genes derived from the pathogen and have no then transformation is unlikely to alter the cross-compatiexact natural counterpart. Second, in natural resistances bility of plants following transformation. genes are frequently expressed only in particular tissues Many intraspecific self-incompatibility (SI) mechanisms (seeds, for example) and/or at particular times (for instance are now well characterized genetically. Several species have after wounding). Many genes bestowing genetically modimechanisms based on a single (S-) locus with multiple fied resistance are expressed from the cauliflower mosaic virus 35s RNA promoter, which in most cases gives conalleles, and a match between the allele in the stigma and the pollen causes inhibition of pollen growth. Recently S- stitutive (continuous in all tissues) expression in plants. locus alleles have been cloned and have been transferred to, and correctly expressed Table 2. Examples of disease and pest resistances introduced into plants in, self-compatible species, by genetic modification although all plants have so far remained selfcompatible2”,2’. Transgenic Pathogen/Pests resistant host Resistance gened Transformation of a species possessing SI with an S-allele PVX/PW/PLRV Potato CP has also been achieved and Antisense to CP the plants became selfcompatRat 2’-5’ oligoadenylate synthetase ible? Introduction of Sl into CP TMV/ToMV Tomato self-compatible species will TGMV Tobacco Antisense to TGMV AL1 gene be useful to plant breeders, CMV Tobacco CMV satellite but it is not clear whether Sl Pseudomonas syringae pv. tabaci Tobacco Tabtoxin detoxification enzyme is involved in interspecific inBarley endosperm thionin compatibility, and, therefore, P. syringae pv. phaseolicola Tobacco Phaseolotoxln-reslstant ornithyl such modifications can be transcarbamylase expected to have little effect P. solanacearum Tobacco Cecropin B lytic peptide analogue on interspecific hybridization. Persistence and spread It is improbable that genetic modification will change the rate at which crops hybridize with wild relatives, or the range of species with which they are sexually compatible. Modification may, however, alter the fitness of hybrids and this might result in greater persistence, faster rates of spread or the ability to invade new habitats. Precise effects are difficult to predict as one must consider all stages of the plant’s life cycle and a variety of habitats, although it is possible to highlight some general principles based on the type of modification.
Erwinia carotovora
Potato
Bacteriophage T, lysozyme
Rhizoctonia solani
Tobacco
Bean chitinase Barley ribosome-inactivating
Refs 29 30 31 32 33 34 35 36 37 38 39
protein
40 41
Botrytis cinerea
Tobacco
Grapevine stilbene synthase
42
Perenospora tabacina/ Phytophthora parasitica
Tobacco
Tobacco pathogenesis-related protein la
43
Tobacco hornworm
Tobacco
Bacillus thunngiens,s lCPb
51
Tobacco hornworm
Tomato
B. thuringiensis ICP
44
Cotton
B. thuringiensis ICP
45
Poplar
8. thuringiensis ICP
46
Striped stemborer/Leaffolder
Rice
8. thunngiensis ICP
47
Colorado beetle
Potato
8. thuringiensis ICP
48
Tobacco budworm
Tobacco
Cowpea trypsln Inhibitor
49
Cabbage looper/Beet Cotton bollworm
armyworm/
Forest tent caterpillar/Gypsy
moth
aAbbreviations: CMV, cucumber mosaic virus; CP, coat protein; TGMV, tomato golden mosaic virus; TMV, tobacco mosaic virus; ToMV, tomato mosaic virus: PLRV, potato leafroll virus; PVX, potato virus X; PVY, potato virus Y. blCP, insect control protein; occurs as several forms depending on the strain of 6. thuringiensis.
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REVIEWS This could be particularly important in the case of phytophagous insects which could be continuously exposed to defence compounds, and has implications for possible deleterious effects on nontarget insects, particularly if the gene escapes into a wild relative that is the sole foodplant of a particular species. The speed with which tolerance to the resistance mechanism might evolve may also have a bearing. Constitutive expression may be a shortlived concern, however, because plant-promoter sequences are now being isolated which confer tissue-specific and temporally specific expression of transgenes. For example, Williams et al.51 designed a chimaeric gene using the promoter from the tobacco PR (pathogenesis related) la gene, and coding sequences from the insect control proteingene from Bacillus thuringiensis. Tobacco plants transformed with this construct were resistant to feeding by tobacco hornworm larvae only after plants were treated with simple chemicals (such as salicylic acid) that induce PRla expression. Also, other workers have demonstrated expression of genes from wound-inducible promoters only following mechanical damage or feeding by insect&s. Modifications which confer a trait that has no wild equivalent and/or has no obvious beneficial effects, other than in agricultural environments, include herbicide and antibiotic resistances and the production of pharmaceuticals and industrial chemicals. The appropriate questions here are whether the possession of a transgene, in the absence of selection for that gene, imposes a cost on the plant (a ‘yield penalty’) or whether it has unforeseen effects leading to greater invasiveness. Evidence is increasing which suggests that plants possess spare metabolic capacity so the production of protein coded by a transgene in the absence of selection does not impose a cost to the plantlJ4. This means that such transgenes may behave as neutral genes in natural populations, and hence their spread can be modelled using data from markers such as isozymes and RFLPs which are also assumed to be neutral. Although there is good evidence that the direct effects of transgenes for traits such as herbicide resistance may be neutral with regard to fitness in natural environments, there is less information on whether unanticipated pleiotropic effects of these genes could be advantageous. Recent results from Crawley et a1.55, however, show no evidence for enhanced weediness in trans-
Box 1. The invasiveness of transgenic oilseed rape in natural habitats A plant will invade an area if its finite rate of increase, h, is >l, and it will become extinct if h
+ g(l-d>)F
where dI is the proportion of seed that dies in one full year; g is the proportion of seed that germinates in the spring of year one; d2 is the proportion of seed that dies in the winter between years one and two: and Fis the mean number of seed produced per seed that germinates. Crawley et a/.55 estimated these parameters for oilseed rape in three climatically different sites and four habitats within each site (wet versus dry, sunny versus shaded), giving 12 environments. In each environment experimental treatments were established involving the presence or absence of vertebrate grazers, invertebrate grazers, fungal pathogens and background perennial vegetation. Three lines of the same rape cultivar were used: transgenic herbicide resistant, transgenic antibiotic resistant and nontransgenic. In no instance was A for transgenics >h for nontransgenics. Also, h>l only occurred in treatments where vegetation was removed, showing the preference of rape for disturbed habitats.
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genie Brassica napus expressing herbicide or antibiotic resistances (Box 1). This experiment was performed with a crop plant rather than a hybrid, hence the ‘genetic baggage’ of the crop may have concealed any possible effects of the transgenes on invasiveness. Nevertheless, this is an important experiment and paves the way for future investigations of the fitness of genetically modified plants in nonagricultural environments. Conclusions Molecular markers are revealing the true extent of hybridization and introgression between crops and wild plants. There is now ample evidence that transformation should not affect the rate or extent of hybridization, hence the information on introgression of nontransformed crop genes gives a basis for assessing the potential for transfer of genetic modifications to wild relatives. The increasing sophistication of modifications, giving control of temporal and spatial expression of transgenes, will enable transformation to mimic naturally occurring phenotypes such as disease resistance, and information on the maintenance of resistance in natural populations will allow the modelling of the effects of these modifications should they be transferred to wild plants. With novel phenotypes, the performance of the gene in natural habitats and in several genetic backgrounds will need to be tested directly. Acknowledgements We would like to thank Dr Norman Ellstrand and two anonymous
reviewers
the original
manuscript.
for suggesting
improvements
to
References Raybould, A.F. and Gray, A.J. (1993) J. Appt. Ecot. 30,199-219 Ellstrand, N.C. and Hoffmann, CA. (1990) Bioscience 40,438-442 Sukopp, H. and Sukopp, U. (1993) Experientia 49,21 l-218 Barrett, S.C.H.(1983) Icon. Bat. 37,255-283 Santoni, S. and BervillC,A. (1992) PIantMol.Riot. 20,578-580
Boudry, P., Miirchen, M., Saumitou-Laprade, P., Vernet, Ph. and van Dijk, H. Theor. Appt. Genet. (in press) 7 Wilson, H.D. and Manhart, J. (1993) Theor. Appl. Genet. 86,642-648 8 Kirkpatrick, K.J. and Wilson, H.D. (1988) Am. J. Rot. 75,519-527 9 Wijnheijmer, E.H.M.,Brandenburg, W.A. and Ter Borg, S.J. (1989) Euphytica 40,147-154 10 Langevin, S.A.,Clay, K. and Grace, J.B. (1990) Euolution 44,1000-1008 11 Doebley, J. (1990) Bioscience 40,443448 12 Rhodes, CA., Pierce, D.A.,Mettler, I.J., Mascarenhas, D. and Detmer, J.J. (1988) Science 240,204-207 13 Omirulleh, S. et at. (1993) Plant Mot. Riot. 21,415-428 14 Mariani, C., de Beuckeleer, M., Truettner, J., Leemans, J. and Goldberg, R. (1990) Nature 347, 737-741 15 van der Meer, I.M., Stam, M.E.,van Tunen, A.J., Mel, J.N.M. and Stuite, A.R. (1992) The Plant Cett 4,253-262 16 Hernoufd, M., Suharsono, S., Litvak, S., Araya, A. and Mouras, A. (1993) Proc. Nat1Acad Sci. USA 90,2370-2374 17 Mariani, C. et al. (1992) Nature 357,384-387 18 Grierson, D., Fray, R.G., Hamilton, A.J., Smith, C.J.S. and Watson, CF. (1991) Trends Biotechnol. 9, 122-123
19 Mizukami, Y. and Ma, H. (1992) Cell 71,119-131 20 Mandel, M.A.et al. (1992) Cell 71, 133-143 21 Levin, D.A. and Kerster, H.W. (1974) Evol. Biot. 7, 139-220 22 Tynan, J.L., Williams, M.K.and Connor, A.J. (1989) J. Cenet. Breed. 23 24 25 26 27 28
44,303-306 Umbeck, P.F. et at. (1991) J. Econ. Entomol. 84, 1943-1950 Morris, W.F., Kareiva, P.M. and Raymer, P.L. Ecol. Appl. (in press) Ellstrand, N.C. and Marshall, D.L. (1985) Am. Nat. 126,606-616 Nishio, T. et at. (1992) Sex. Plant Reprod. 5, 101-109 Murfett, .I.et al. (1992) Plant Cell 4, 1063-1074 Toriyama, K. et at. (1991) Theor. Appt. Genet. 81,769-776 TREE uol. 9, no. .3 March
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219,492-494 36 Carmona, M.J., Molina, A., Fernlndez, J.A., L6pez-Fando, J.J. and Garcia-Olmedo. F. (1993) P/ant 1 3,457-462 37 de la Fuente-Martinez, J.M., Mosqueda-Cano, G., Alvarez-Morales, A. and Herrera-Estrella, L. (1992) Bio/Techno/ogy 10, 905-910 38 Jaynes, J.M. et a[. (1993) P/ant .Sci.89,43-53 39 During, K., Porsch, P., Fladung, M. and Liirz, H. (1993) P/ant Mol. Biol. 15,281-293 40 Broglie, K. et a/. (1991) Science 254, 1194-1197
41 Logemann, J., Jach, C., Tommerup, H., Mundy, J. and Schell. J. (1992) Bio/Technology 10,305-308 42 Hain, R. et al. (1993) Nature 361, 153-156 43 Alexander, D. et al. (1993) froc. Nat/Acad. Sci. USA 90, 7327-7331 44 Delanney, X. et at. (1989) Bio/Technology 7, 126.5-1269 45 Perlak, F.J. et al. (1990) Bio/Technology 8, 939-943 46 McCown, B.H. et al. (1991) flunt Cell Rep. 9,590-594 47 Fujimoto, H., Itoh, K., Yamamoto, M., Kyozuka, J. and Shimamoto, K. (1993) Bio/Technotogy 11. 1151-1155 48 Adang, M.J. etal. (1993)flant Mol. Biol. 21. 1131-1145 49 Hilder, V.A.,Gatehouse, A.M.R.,Sheerman. SE.. Barker, R.F. and Boulter, D. (1987) Nature 300, 160-163 50 Parker, M.A. (1993) Hered@ 71,290-294 51 Williams, S. et al. (1992) Bio/Technology 10,540-543 52 SanchezSerrano, J.J., Keil, M., O’Connor, A., Schell. J. and Willmitzer, L. (1987) EMBOJ. 6,303-306 53 Thornburg, R.W.,Keman, A. and Molin,L. (1990)P/ant Physiol.92,500505 54 Hilder, V.A.and Gatehouse, A.M.R.(1991) Transgenic Res. 1,54-60 55 Crawley, M.J., Hails, R.S., Rees, M., Kohn, D. and Buxton, J. (1993) Nature 363,620-623
Cooperativebreedingin mammals Michael D. Jennions and David W. Macdonald
M
ost studies of cooperative breeding in vertebrates have been on birdslJ. This has led to the development of a concep tual framework which is generally assumed to be applicable to mammals. While most of the experimental and correlational tests have also been on bird+, new research on cooperative breeding in mammals provides an opportunity to investigate the generality of bird-based models.
Cooperative breeding in mammals covers a diversity of breeding systems. In all cases, however, individuals assist in the rearing of offspring other than their own. Recent research has highlighted some of the factors responsible for variation both within and between species. While it is possible to generalize about the selective pressures leading to cooperative breeding, doing so may obscure important contrasts between taxa. Of course, inclusive-fitness models explain the generalities of cooperative breeding, but differences in ecology, physiology and life history may result in distinctive processes operating in different taxa-data only likely to emerge from long-term field studies.
Is ‘helping’ beneficial for breeders? An important variable in co-
operative-breeding models is the influence of helping on breeder fitness, and correlational evidence is often used to calculate the magnitude of this effect. Positive relationships between the number of helpers and reproductive success have been recorded for some mammals Fable l), but others have failed to show this effect. However, relationships are potentially confounded by factors covarying with group size, like What is cooperative breeding? breeder experience or territory In the bird literature, cooperquality3Jl. This problem can be ative breeding is defined as a situaddressed through experimental ation where ‘more than a pair of Michael Jennions and David Macdonald are at the manipulation. In birds, by removindividuals exhibit parent-like Wildlife Conservation Research Unit, Dept of Zoology, ing helpers, two studies have [helping] behaviour towards University of Oxford, South Parks Road, Oxford, shown that helpers are beneficial, young of a single nest or brood’4. UK OX1 3PS. and a third that they have no disIn mammals, this type of behavcernible effect”. Experimental reiour has been recorded in numermovals have been carried out on two mammals - prairie ous taxa, ranging from rodents to elephants5J. Activities defined as ‘helping’ in mammals (see Box 1) include feed- voles (Micro&s ochrogasfer) and pine voles (Microtus pinetorwn)l*J3. In both species, philopatric juveniles groom ing, grooming, babysitting7, helping infants in distresss, assistance in thermoregulationg and allosucklinglo. In and brood young and assist in burrow maintenance. practice, ‘helping’ has been used to describe any activity Statistically significant differences in some reproductive variables were recorded (Table 2). Although suggestive of directed towards infants or their parents which is likely to increased life-time reproductive success for breeders benefit the recipients and increase breeding success (e.g. alarm calling or provisioning a pregnant female). By defi- with helpers, it remains to be shown that these effects translate into increased breeder fitness. nition, then, all animals which are social during the breedFurther experimental removals may clarify the situation, ing season are cooperative breeders. We suspect, however, but their results will need to be interpreted with caution. that workers are most interested in a subset of costly First, groupsize effects may be responsible for the increased helping behaviours - those which appear to decrease the donor’s direct fitness relative to that it would possess if it reproductive success of breeders in larger groups”. Many cooperatively breeding mammals are highly social, did not perform these activities (Box 2). TREE uoi.
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