Proc. Assoc. Advmt. Anim. Breed. Genet. Vol12
A GENETIC DIVERSITY APPROACH TO CONSERVATION: GENETIC SIMILARITIES AND DIFFERENCES BETWEEN SPECIES
R H. Crozier
School of Genetics & Human Variation, La Trobe University, Bundoora, Victoria 3083 SUMMARY
The justifications given for biological conservation fall into three categories: moral, aesthetic, and utilitarian. Utilitarian reasons for conservation include the possible importance of high biodiversity in preserving ecosystem function and the occurrence of useful attributes in organisms, with bioprospecting being an example of commercial understanding of biodiversity as wealth.
Increasing estimates of the numbers of species on Earth raises the value of the natural world. A framework for the preservation of biodiversity is the maximisation of the genetic information content of the Earth’s organisms. This information content approach has to take account of the coding portions of the genome and differing numbers of genes between organisms. The numbers of species in ecosystems is the simplest measure of biodiversity, but phylogenetic measures taking into account the evolutionary distinctness of species are preferable, especially those using divergence information and not just tree topology. Technological advances already permit the automated genetical enumeration of bacterial communities, and will eventually allow the ready molecular characterization of the macrobiota.
Keywords: Genetic variation, nature conservation, resource conservation, genetic resources, species diversity.
THE ANATOMY OF THE GENOME
The genome, the total DNA in a set of chromosomes, varies widely in size between species. It is a truism that this variation in size, conveniently given in terms of the numbers of nucleotide base pairs, does not follow any simple notion of the complexity of the organisms concerned. For example, the diatom Navicolapelliculosa has 35,000 kilobase pairs (kb), humans have 3,400,OOO kb, and the protist Amoeba dubia has 670,000,OOO kb (Li and Graur, 1991). The situation is considerably (although not completely) clarified when one realises that much of the DNA in organisms is non-genie (i.e. does not produce a gene product), with the traction of the genome which is non-coding varying from less than 30% to almost all of it (Cavalier-Smith, 1985).
Organisms vary in the numbers of genes which they have. The free-living bacterium Mycophma genitalium manages with only 470 genes (Fraser et al., 1995) whereas humans have approximately 75,000 (Antequera and Bird, 1993). The simplest completely-sequenced eukaryote is a yeast, with 6,000 genes (Dujon, 1996). Loomis (Loomis, 1988) suggested that about 6,000 genes are required for the house-keeping functions of the cell, and that a further 2,500 gene products are essential for the development of a human. Clearly the difference between 8,500 and 75,000 is large, and represents considerable fine-tuning, as through the production of gene families via gene-duplication (Li and Graur, 1991). The concept of increasing complexity through
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Proc, Assoc. Advmt. Anim. Breed. Genet. Vol12 increasing the numbers of genes (Maynard Smith and Szathmary, 1995) fits well with the idea that gene duplication is the major creative agency in evolution.
The picture that a great many genes are held in common between organisms is correct, although whether to be impressed by the genes in common or the genes whose function is unknown (Dujon, 1996) is perhaps a matter of choice. It is premature, however, to conclude that biodiversity is unnecessary because by addition of suitable genes a common species could be used to recreate extinct relatives. Firstly, although the genes may be held in common in terms of similarity of function, there may be considerable and important sequence differences between them, i.e., allelic variation. Secondly, although for many characters the number of genes of significant effect is now known to be small, it would be very hard to identify which genes they are and then cleanly replace them to yield the desired result. Even when the number of genes underlying dramatic differences between related species is known to be small (Val, 1977), the molecular identification and transfer of the requisite alleles appears to be considerably beyond current technology.
BASIC REASONS FOR CONSERVATION
All reasons given for the preservation of biodiversity can be grouped under three headings, the moral (other species have an innate right to existence), aesthetic (although other species have neither an innate right to exist nor, in most cases, any economic value, they are nature’s works of art which we would be foolish to destroy) or utilitarian (other species are of actual or potential direct benefit to the well-being of humankind).
These reasons should be examined for the policies they imply in the light of the great increase in magnitude of the estimates of the number of species on the planet, with the estimate being 1.7 million in 1978 (Wilson et al., 1978) but 10 million in 1992 (May, 1992). Conservation biologists have to face the fact that if you have one dollar note, it will be extremely precious to you, but if you gain 9 more, then the first will be less valuable to you, and to sharpen the analogy, just as for species, each note is unique.
Under the moral view, the number of species is immaterial because, as do persons in a society of any population size, each species has a moral right to exist. This view is therefore attractive to conservationists of any intellectual persuasion, but they face the practical difficulty that rights are a human construct and have no objective reality other than those accorded by the popular will.
Moral rights for humans are themselves capable of drastically different interpretations, ranging from a call for the suppression of state power to give individuals untrammelled freedom (Nozick,
1984) to one for the increase of state power to enforce equality of outcomes @awls, 1971).
The aesthetic view can be expressed in E.O. Wilson’s @ers. comm.) terms, that it is wrong to burn Rembrandts to warm the house, however cold it gets. Living things are, to the conservationist, works of art, and should not be destroyed. However, arguments using this reason, as do those of the utilitarian view, face a problem with large estimates of the number of species. The intrinsic value of any one Rembrandt must decline as the total number of such works increases.
Proc. Assoc. Advmt. Anim. Breed. Genet. Vol12 The utilitarian view argues that other species are of direct value to humans either for specific products or for the preservation or productivity of the biosphere. Taking the second point first, particularly species-poor experimental (Naeem et al., 1994, 1995) or observational (Tihnan and Downing, 1994; Tihnan et al., 1996) plots show lower stability and productivity compared with more species-rich ones, but it seems problematic to extend this to highly diverse environments (Myers, 1996).
The products produced by particular species stand as a major benefit to humanity. Such products include possible new food plants (Beattie, 1995; Wilson, 1992) but more current effort is being expended in the field of bioprospecting for pharmaceutical products. Such activities are naturally of benefit to multinational companies (Turner, 1996) and, under recently international conventions, to species-rich countries (Iwu, 1996).
Bioprospecting enables us to examine the effects of increasing species numbers on the worth of species. The argument that the worth of individual species is reduced is not refuted, but the conclusion as to the total value of the world’s biota is changed. The more species there are, the higher is the value of the natural world for the production of natural products. Returning to our bank notes, if your piggy bank contains many bank notes, you should be more inclined to safeguard it rather than go looking for another. The economic value of biodiversity is in fact being recognised (Pearce and Moran, 1994), including the losses of plant species some of which would have produced useful products (Principe, 199 1).
The alternative to natural drug sources is the search of the chemical space (Ecker and Crooke, 1995). However the more plant species there are the more the more likely it is that some of these will present usefnl compounds. The usefulness of such compounds is that usually their value would not be imagined without their testing from natural products, and then their use is not themselves as drugs but as the lead to the deliberate elaboration of similar but more active compounds (Turner, 1996). This process thus resembles the ‘evolutionary algorithm’ approach to molecular design (Ebeling and Nadler, 1995), and in fact various authors stress that much bioprospecting is likely to be important as discovering the answers of other species to problems we are increasingly facing (Dobson, 1995; O’Brien, 1995). The best ‘evolutionary algorithm’ has been evolution itself.
SPECIES RICHNESS VERSUS GENETIC DISTINCTNESS
The commonest measure by ecologists of biodiversity is species richness, the number of species per habitat or perhaps a function of this (species diversity) taking into account the relative evenness of population size or biomass (Begon et al., 1990; Odum, 1989). Of these, species richness and not species diversity is the appropriate measure for conservation. But this measure takes no account of the distinctiveness of species (Williams et al., 199 1; Wilson, 1992), weighting one species the close relative of many more the same as one evolutionarily unique. For example, the New Zealand tuatara is widely recognised as of special merit for preservation (Daugherty et al., 1990; May, 1990), and it would then be illogical to acknowledge this and yet assert that each species is equally worth of preservation.
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Wilson (1992) specifically considered this question in the context of the possibility that, with speciation often a rapid process, a massive extinction event now could be tolerated if it was assumed that large reserves could be set apart in future and re-stocked with recently speciated species. Wilson noted that such organisms would be ‘trash species’, lacking the distinctness of those occurring today.
A contrary view should be mentioned, and that is that rare and unique species should be given lower conservation worth than common unendangered ones because the latter are liable to be able to speciate more rapidly and replenish the stock of species (Erwin, 1991; Linder, 1995). This view ignores the likely higher presentation of unique attributes of phylogenetically distinctive species, and the long-held conclusion of evolutionary biology that it is very hard to pick winners (Mayr, 1963).
It remains an unexamined question, however, how much more likely new distinctive products or other useful attributes are to occur in divergent species as against those close to species already well-known to have useful attributes. The method to test this is clear, if laborious, and is being carried out. Animal and plant breeders, however, are already convinced that distinctive breeds are particularly worth preserving (Brown and Schoen, 1994; Hall and Bradley, 1995).
METRICS FOR PRESERVING BIODIVERSITY
Wilson (Wilson, 1988, 1992) argues for the application of information theory to biodiversity, making the argument that the information in the world’s DNA should be maximised. This approach is very attractive, and initially at least appears highly tractable - the four bases lead to 2 bits of information per position (leaving aside the effects of base composition bias (Jermiin et al.,
1994)).
A number of refinements to the theory are needed, in the light of the fact that the information content of the DNA is being used as a predictor of the overall phenotypic diversity of organisms - what has been called ‘feature diversity’ (Faith, 1994b). Firstly, as briefly outlined above, much of the DNA of organisms is non-coding, and hence should not be included in the calculations.
Secondly, saturation is a universal feature of evolving systems, more serious for morphology than for DNA, and it is desirable if this can be taken into account. For example, in a study of mtDNA sequence divergence between Drosophila species, it was found that although the species were evolving at the same rate after a certain length of time they no longer diverged rapidly (DeSalle et al., 1987). Thirdly, species differ widely in the number of genes they have, eg almost 20% of the 470 genes of Mjcoplasma genitalium are absent from Haemophilus infuenzae (Fraser et al.,
1995), and this must affect their conservation worth (see below).
There are a number of reasons to prefer genetic diversity measures to morphological ones for estimating biodiversity, and one large drawback (considered at the end of this essay) that is more apparent than significant in the long term. Firstly, we seek a measure which will correlate with all features of an organism’s biology, not just those which are apparent to human observers, with all
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Proc. Assoc. Advmt. Anim. Breed. Genet. Vol12 their natural anthropocentric biases. DNA sequences provide such a source of data, at least potentially. Secondly, we seek a measure which readily and reliably converts into phylogenies, including estimates of the degree of divergence between organisms. Although molecular sequences present continuing problems in phylogeny estimation, they are now clearly vastly preferable to morphology (Russ0 et al., 1995).
Although other measures have been proposed, such as the use of topologies alone (Vane-Wright et al., 1991) higher taxa as a surrogate for species (Williams and Gaston, 1994), and satellite imagery analysis of landforms (Pressey et al., 1993), the evolutionary divergence between species or populations is emerging as the most useful measure of conservation worth (Crazier, 1992;
Crazier and Kusmierski, 1994; Faith, 1992, 1994a, 1994b; Krajewski, 1994; Weitzman; 1992, 1993). Among these authors, Weitzman has sought to integrate economic information with phylogeny to demonstrate the optimal approach, but other authors have concentrated on the phylogenetic distinctiveness. Crazier and Faith independently arrived at very similar measures:
Faith’s PD measure is an additive function of tree branch lengths whereas Crazier’s GD measure is a multiplicative measure designed to cope with saturation. Whether it is feasible to try and cope with saturation is a moot point at present, but in any case the two measures yield the same rank order of conservation worth of sets of species in all cases except a formulation of Faith’s measure which he does not generally use (Crazier and Kusmierski, 1994; Faith, 1994a). The two measures differ, however, in estimating the proportion of the total biodiversity being preserved. For these measures to be useful for management decisions, the bootstrap confidence limits on the relative worth of sets of species should be calculated; a program is being written to allow this.
Another approach using phylogenetic information is the Evolutionarily Significant Unit, or ESU (Baverstock et al., 1993; Legge et al., 1996; Moritz, 19944 1994b; Vogler and DeSalle, 1994;
Vogler et al., 1993). An ESU is a clade recognised from dendrogram topology, and distance information is not used except in the value judgement as to whether a monophyletic set of populations is sufficiently different from another such set to be termed an ESU. The measure can be thought of as aimed at the intraspecies level, although it is also thought of in part as a replacement for species because of the difficulties in defining these (Mallet, 1995). The population-level significance of this approach is as an indicator of gene flow between the populations, but it is also true that, apart from the lack of use of distance information, the ESU approach would tend to give higher priority to more distinctive populations.
INTRINSIC INEQUALITY OF SPECIES
As mentioned above, species differ in the number of genes they have. These differences have been plausibly linked to changes in complexity during evolution (Bird and Tweed@ 1995; Bird, 1995; Maynard Smith and Szathmary, 1995; Szathm&y and Maynard Smith, 1995). An organism with more genes should therefore have, other things being equal, a higher conservation worth than one with fewer genes. Would then a mammal be mtrinsically be worth 80,000/6,000 = 13 times more for conservation than a yeast? Given that we are concerned with preserving the instructions for biodiversity rather than just biodiversity itself, this seems the correct approach, with the caveat that the true factor might reasonably be expected to be less given that usually more gene-rich
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Proc. Assoc. Advmt. Anim. Breed Genet. Voll2 species have gained their additional genes via gene duplication (Ohno, 1970; Zhang and Nei, 1996). Naturally, of course, other things will not be equal, and the degree of phylogenetic distinctness of yeasts would be expected to preserve them against sacrifice in favor of an endangered rodent, for example.
FINAL PERSPECTIVES
Morphological systematists might naturally argue that molecular genetic diversity, as the basis for an information preservation approach, is impractical on the grounds that the collection of the necessary information is too expensive and too slow. At present, this is correct for most portions of the macrobiota. For large organisms, the genetic diversity approach will for some time be limited to setting conservation priorities for particular groups for their own intrinsic perceived interest or as indicator groups. In general terms, one could prioritise the information necessary for conservation decisions: species richness as a fast step, branching pattern if available, and full phylogenetic information if possible. However, the advance of technology is rapid and already for microorganisms it is becoming routine to acquire all this information in the same automatable operation. The approach began long ago with the discovery that reverse transcriptase could be used for direct sequencing of RNA (Pace et al., 1985), but has been greatly facilitated with the appearance of the polymerase chain reaction. Numerous bacterial communities are being surveyed without need for cultivating organisms, not only free-living forms (Bruce et al., 1995;
Giovannoni et al., 1996; Holben and Harris, 1995; Pedersen et al, 1996; Pedrbs-Ali6, 1993;
Porteous et al., 1994; Risatti et al., 1994; Weidner et al., 1996) but those in termite guts (Berchtold and Konig, 1996; Ohkuma and Kudo, 1996; Ohkuma et al., 1996). The prospects are that this approach, of total ecosystem inventory, will be applicable first to small soil-dwelling metazoa, fungi and plant roots, and then form a basis for studying other levels. Until then, a research need is to determine the extent to which microorganism diversity reflects that of the macrobiota with which it is associated.
ACKNOWLEDGMENTS
I thank the Australian Research Council and La Trobe University for supporting my work in evolutionary genetics, Mark Westoby for discussions on the information content approach, Mike Clarke for information on species diversity, and Robert M Kusmierski for constructive criticisms of the manuscript.
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