by Academician Yuri ALTUKHOV, Director of the N.I. Vavilov Institute of General Genetics, Russian Academy of Sciences
One sequel to human activity is this: dozens of thousands of natural species have disappeared from the face of the earth. Gone are hundreds of unique breeds of domestic animals and strains of crop plants. As competent people see it, the biosphere may lose as much as 10-15 percent of its present species diversity by the years 2010-2015. Besides environmental pollution and destruction of habitation media, there is yet another adverse factor at work, though perhaps not as conspicuous-man's economic activity with no regard for the genetic characteristics of particular species.
This problem, now studied in the last two decades, has an important sideline to it: a new scientific discipline, ecological genetics, or ecogenetics for short, has been born. It is chiefly involved with the conservation and rational use of gene pools (genofonds), that is the aggregate hereditary information passed from progenitors to offspring and accounting for such essential biological characteristics of populations and species as their numbers, productivity, life expectancy and resistance to disease. Although a great many works have been published on the subject, they make us no wise on the key questions: what to protect and how? The purpose of this article is to fill in the blank. The author also considers the consequences of anthropogenic (man-induced) effects on populational gene pools and outlines steps toward their conservation.
WHAT TO PROTECT?
Different biologists will answer this question differently. A "globalist" will say that all of the biosphere should be protected (and conserved for that matter); an "ecologist" will insist on the importance of ecosystems, while a "populationist" will zero in on the key significance of populations, or the well-established self- reproductive intraspecies groups of individuals. Each of them will be right but with one reservation: it is populations alone that are crucial for the existence and further development of life on earth, since they are the vehicles of the genetic continuity of generations.
Yet, unfortunately, populations are an object of direct external effects, be it hunting, fishing or timber harvesting. Aside from anthropogenic pressures of immense scope that invite natural disasters (like, for instance, the death of the Aral Sea with its flora and fauna), all types of human activity, especially game-shooting and fishing as well as the artificial reproduction of animals and fish, involve local populations. Gradually, step by step, such activities are extending to whole species, ecosystems and ultimately, to the entire biosphere. Consequently, no
Population structure hierarchy of the Pacific salmon (nerka) spawning in river systems of Asia and America. Regions: / - western Kamchatka; II - basin of the r. Kamchatka; Ill - eastern Kamchatka; IV - Cook Inlet (Alaska); V - river Skin basin (northern British Columbia); Vl - river Fraser basin (British Columbia); Vll - southern part of the American area.
1 - Palana; 2 - Khairyuzova; 3 - Bolshaya; 4 - Ozernaya; 5 - Kamchatka; 6 - Andrianovka; 7 - Kirganik; 8 - Kimitin; 9- Kitilgin; 10 - Avacha; 11 - Pakhacha; 12 - Kenai; 13 - Susitna; 14 - Kasilov; 15 - Skin; 16 - Fraser, upper reaches; 17 - Fraser, middle reaches; 18 - Fraser, lower reaches; 19 - Queenalt; 20 - Columbia. Samples correspond to individual local subpopulations, the elementary subdivisions of a species.
matter what stand a biologist might take - "globalist", "systemic ecological" or "populationist" - he could not bypass populations. So the answer to the question in the heading - What to protect? - could be this: it is intra-species groups of individuals that should be protected.
Let me stress: populations have a complex pattern and, like any level of biological integration, they possess an inner structure and corresponding functions. Many, if not all, species are endowed with a subpopulational structure. If we take the Homo sapiens species, it is subdivided into three large geographical races: the Europoid, the Mongoloid and the Negroid races; each of these, in turn, comprises a variety of diverse ethnic and subethnic groups. The same applies to the plant and animal kingdoms. Say, we can identify at least four hierarchical levels in the Pacific salmon ( nerka, or blueback salmon) which spawns in lacustrine basins on both sides of the northern Pacific. Exchanges of individuals through migration contribute to sustaining the ecological integrity of a species as a complex system.
The age structure, too, is important: any population is composed of both young individuals of reproductive age and old ones. Good reproduction is possible only if there is a definite correlation between these age groups, or what demographers call a "pyramid of life", with the younger age groups down, and the older ones up. Clearly, a broad-based pyramid corresponds to a growing population and that with a narrow base, when older age groups prevail, to a contracting population. For simple reproduction the death and the mortality rates should be in equilibrium.
Likewise important is a correlation between the total number of a population (N t ) and a segment within it that passes genes to the next generation and designated therefore as the genetically effective number (N e ). Since individuals of the older and junior age groups are not implicated in reproduction, under natural conditions N e is below n( and depends much on the correlation of male and female individuals. This is the sex, or gender population structure. The two components are in equilibrium in most community of animals, for each individual must find a partner of the opposite sex to keep up reproduction. Yet the pattern is more complicated in subdivisions of a species, in elementary subpopulations, where the above correlation may be essentially different from a state of equilibrium, and the Ng value will be much lower. If averaged, it will be closer to the number of individuals within a sex minority, when the equilibrium is upset too badly. For example, at (with the number of males and females equal), N e will correspond to 100 individuals, while at the figure will be but 29.
Before touching on the genetic significance of these effects, let me
stress this point: animal species are also remarkable for a fine social structure which is manifest within local subpopulations. It is represented by reproductive communities in the form of harems, colonies, prides and other analogous groups distinguished for a nonrandom conjugal structure which averts inbreeding (the breeding of closely related individuals) and its negative aftereffects. For instance, long-tailed macaques found in the tropical forests of Sumatra live in small colonies, from 8 to 50 species each. While females always stay at their birthplace, males migrate from colony to colony; they can be dominant or subdominant (the contribution of the former to the gene pool of a successive generation attains to 80 percent). The nonrandom system of selective breeding also occurs among the Pacific salmon: females will mate with large males.
Interpopulation exchanges of individuals are not random either. This phenomenon was first discovered in experimental studies on the population system of the Drosophila fruit fly, a pet object of genetic research. One experiment involved the fly's population system. This system, as it turns out, consists of a large subpopulation ("continent") and several small peripheral subpopulations ("islands"), both interacting through exchange. The lower the number of the "islanders", the more "continentals" they will be getting. The same dependence was then detected among native populations of other species.
Considering this body of data, let us try and answer the key question: What to protect? Well, we should protect population systems which exist in several levels of hierarchy, each having an age-sex structure of its own; this one is ordered in time and in space, and is coupled to the natural dynamics of the numbers, productivity, succession of generations and its pace, resistance to disease and other things. Nature knows no other populations! The same applies crop and cattle farming: plant and animal breeds did not appear at random but were evolved gradually; they are related to one another some way by bonds of kinship reflecting the successive differentiation of ancestral gene pools, or genofonds.
This very term, "genofond", was introduced in 1925 by Dr. A. Serebrovsky, corresponding member of the USSR Academy of Sciences. Here is how he defined it: "A totality of all genes of a given animal species. I have called a genofond so as to stress the idea that in the genofond we have the same national wealth as we do in the reserves of petroleum, coal and gold hidden deep underground." I would add but one thing to this elegant and commonly accepted definition, namely: mineral deposits are in the category of non-renewable resources which, sooner or later, will be exhausted; population genofonds, on the contrary, are renewable and, therefore, are inexhaustible - in theoretical terms anyway. An adequate strategy should be mapped out for the successful reproduction of gene pools and populations they embrace. Fortunately - and this facilitates our objective - scientists can rely on the theoretical principles of population genetics which studies regularities underlying the conservation and transformation of population genofonds in time and in space. Proceeding accordingly, we come to the other key question: How to protect?
HOW TO PROTECT?
Population genetics, born as a branch of applied mathematics in the beginning of the 20th century, is concerned with the dynamics of hereditary information in successive generations. The measure of this information is what we call heterozygosity (heterozygosis), which means a diversity of genes inherited by offspring from their progenitors and accounting for interindividual differences within a population. For instance, on the sheaths of ladybugs we can see pigment patterns peculiar to each individual and passed down from generation to generation. And we can identify petilia, a common variety of aquarium fish, by a design on the tail of males. This is a token of polymorphism, or genetic diversity.
Many species, however, are outwardly uniform and monoform, something that renders their genetic analysis well-nigh impossible. Yet thanks to achievements of molecular biology, we can now study the genetics of any species by relying on latent differences inherited by individuals-the individual differences "recorded" in protein structures of the organism or within DNA. We detect them by mounting protein or DNA solutions of plant or animal tissues on neutral fine-porous gels within special apparatuses. The molecules of these substances are sorted out in an electric field according to the charge or other heredity-related characteristics (individuals within a population are different, and their differences are passed invariable by parents to progeny). Since the late 1960s, as electrophoretic techniques came into use, innate biochemical variability has been discovered in more than 2,000 species, from microorganisms to man. And in the past 15 years, hundreds of these species have been characterized according to DNA markers.
Microbiologists have thus discovered an immense scope of intraspecific hereditary diversity. About a third of the genes coding for protein synthesis are found to be polymorphous, with the level of individual heterozygosis approaching 10 to 12 percent. Applying these estimates to a genome (ca. 10 to 50 thousand structural units of heredity), we find that an "average" individual is heterozygotic in hundreds of its genes. This very characteristic-the information capacity of a genotype-is a vital biological parameter of the organism's adaptive capabilities. To get a grip on the problem, we cannot to without mathematical models of panmictic and subdivided populations. In the first case, individuals interbreed freely and under definite conditions (infinite numbers, absence of external effects and so forth), this population type remains stable in many generations. Yet this is but an abstraction: the point is that evolutionary factors are always at work to upset equilibrium. Take natural selection whereby some genotypes have more populous progeny than others, something that changes the genetic structure of a population. Or take genetic migration (gain or loss of genes) which likewise distorts this characteristic. We cannot rule out what is called a random genetic drift when the effective number of a population goes down and "errs" in the reproduction of the next generation's genofond. This causes an increasing inbreeding and, as a consequence, a loss of genetic diversity.
The intrapopulation inbreeding, however, can be redressed by genetic migrations. In that case a panmictic population changes to a subdivided population, that is a sum total of interacting subpopulations. It was the American biologist Sewall Wright who, back in the 1930s, made a crucial contribution in elaborating the theory of subdivided populations. Such systems are noted for steady genetic stability by virtue of mutual equilibration of evolutionary factors (say, genetic drift is neutralized by gene migration, and it cushions the effects of natural selection).
We can now see that in contrast to the simplest mathematical models, population systems are real natural objects with a history of their own. They took form in the course of ancestral genofond differentiation in generations and in areas of propagation, and they are represented by different hierarchical levels. These characteristics enable us to reconstruct the genetic picture of an ancestral parent population by averaging the characteristics of the extant subdivisions of a species.
It also follows from S. Wright's theory that the structure of a genofond (gene pool) of a particular population, its genetic diversity (H T ), is determined not only by intrapopulation (H S ) but also by interpopulations (G ST ) components of variability. The Japanese geneticist Masatoshi Net has studied the correlative statistics of these two components. Without going into particulars, I will only say that G ST is a measure of local differentiation: the greater the genetic differences among local groups of individuals, the higher this value will be. The intrapopulation components H S behaves respectively: it goes up when G ST is down and, contrariwise, it goes down if 0пар.т is up (since H S + G ST = 100% of H T ).
Should a subdivided population reproduce its genofond in successive generations steadily, that is the genofond differentiation and integration are in equilibrium, then a correlation of the intra- and inter-population components of genetic diversity would also remain steady on different hierarchical levels of a system. As shown by our studies, such kind of autoregulation does take place owing to the non-random structure of breedings.
This conclusion is of essential importance, for it validates the concept of a normal process ensuring an infinitely long life of a structured genofond. So our question - How to protect? - could be answered unambiguously. In the course of the commercial use and artificial reproduction of biological resources it's all-important to preserve the population structure of a species, a structure that regulates the evolutionally established correlation of the intra-
and intergroup components of its genetic diversity. But this "how- to" will be materialized only through an adequate, even-handed apportioning of economic activities with respect to every subpopulation.
To understand how man abides by this rule let's turn to native and cultivated species.
UNDER ANTHROPOGENIC PRESSING
Our studies of commercial fish population may respond best to the main goal of ecogenetics, and this is to understand what happens to the gene pools of commercial fish species and what should be done if events proceed by a bad scenario. As we found out, the genetic diversity of artificially sustained fish populations has shrunk compared with native ones. But there are more sides to this problem. We have also detected negative effects of increasing intrapopulation heterozygosis because of the all too big catches of large old males, 5 to 7 year olds.
The results of our study of the Pacific salmon, nerka (blueback salmon), could well prove this point.* Its populations are noted for a peculiar social structure represented by three groups of fish implicated in spawning; these are two groups of males, small and large ones, and a group of medium-sized females. The small males (as a rule, three-year olds, known among Kamchatka denizens as kayurkas, and as jacks in Canada and the United States) do not occur as much frequently in natural shoals spared by commercial fishing. Yet their number is dramatically up in populations that are a target of systematic catches. A conspicuous example of that is a nerka school in Lake Dalny on Kamchatka - the biology of this colony has long been studied in detail. Whereas
in the 1930s the number of spawning fish breeders in the shoal approached 100,000, it went down to 2-5 thousand in the 1960s and 1970s, with the proportion of the kayurka fish among the sexually mature males up from 0.2 percent to 38 percent.
What is the cause of such dramatic changes? By and large, this is selective fishing that destroys the genetic structure of nerka shoals from generation to generation whereby large males are caught. Other spawning fish are caught on a regular basis (mostly 4-5 year-old females of middle-level heterozygosity) or even undercaught (small three-year-old males of maximum heterozygosity). Thus the proportion of large fish in the shoal falls, and the equilibrium of females and males is upset; the pubescence time becomes shorter, and so does the average life expectancy too and, as a
Variability of body length of the Pacific salmon (nerka) during spawning in one of the lakes of the Kamchatka Peninsula. Solid line, males; broken line, females.
* See: V. Zaselsky, "Shoals of Salmon - Model of Longevity", Science in Russia, No. 1, 1997 -Ed.
Genetic profiles of Russian hen breeds and of their protopopulation. Frequencies of genes encoding synthesis of blood and egg protein: 1 - ovalbumin; 2, 3, 4 - globulins; 5 - transferrin; 6 - albumin; 7, 8 - esterases. Gene frequency interval: 0-in the circle center, 1-on the perimeter. Lines connecting individual breeds with the protopopulation show estimates of their genetic relatedness distance from the ancestral gene pool.
consequence, the pace of generation changes is up. Simultaneously, the biomass and the population of the shoal is down, for small fish are less fertile. All this is proper not only to schools of Pacific salmon but also holds for other fish species, an object of commercial fishing.
The pattern is more complex where the artificial reproduction of biological resources is concerned. Comparing native populations of Atlantic salmon and trout, we come to deal with two absolutely different processes related to the redistribution of the intra- and intergroup components of genetic diversity. Salmon hatched at fisheries have a substantially higher level of inter-population differentiation but lower the level of intrapopulation polymorphism than the same fish under natural conditions. But it is quite the reverse for schools of salmon and trout nursed at hatcheries in Spain and France: we have a higher level of intrapopulation heterozygosis and obliteration of interpopulation distinctions. Salmons raised in hatcheries show a more intensive level of inbreeding due to a small number of male breeders; and in trout- breeding there is an intermixing of the genofonds of different maternal lines (distant breeding, or outbreeding). In either case the fry are in for a lower survival rate, and the shoal population goes down.
Thus the pattern of change induced by anthropogenic effects is of the same type by and large. This triggers adverse genetic processes and upsets the evolutionary correlation of the intra- and interpopulation components of genetic diversity. Both the downturn in heterozygosis and its excessive upturn are unfavorable for the normal functioning of a population system.
All these facts have made it possible to substantiate the concept of optimal genetic diversity as a vital condition for the welfare of populations. Knowing a correlation of the intra- and intergroup components of hereditary variability under the conditions of normal reproduction, we can develop practical recommendations towards rational economic use and conservation of the genofonds of native population systems.
This very approach works if applied to agricultural populations as well.
For example, in the past few decades about 60 strains of barley have been evolved and grown in Eastern Siberia. Our study of these strains has shown a considerable change in the heterogeneity of corresponding populations: represented by a mix of different genotypes before, they are now remarkable for a predominance of strains bred from separate genetic lines. As a result, the local, old-time strains display a substantially higher level of variability than the come-latelies. Small wonder: they, the newly evolved strains, descend from one or several plants.
The same trend of genetic diversity loss in time is clearly seen in hen populations. Today only 4 to 7 breeds of hen out of more than a thousand known worldwide are used commercially. Here in Russia about 30 hen breeds, out of a total of 80 old ones, are gone, which has led to a drop of genetic resources in the hen breed makeup by 37.5 percent in the last 50 years. Taking the genetic characteristics of 47 hen breeds raised here in Russia and abroad, we obtained the structure of a hypothetical "progenitor" ancestral population and, proceeding from it, drew genetic "profiles" of 14 home breeds. And what we saw was this: some of them had a unique structure, while the others were similar to that protopopulation. Five populations belong to the first group, and these are the Orlovskaya, Pervomayskaya, Russkaya White, Leningradskaya White and Moskovskaya breeds; the rest nine are in the other group. Here's another important fact: the home synthetic breeds that are close to the ancestral population show a higher level of intrapopulation heterozygosis (H S =0.213) and low interpopulation variability (G ST =0.0975) compared with those distant from it (H S =0.183; G ST =02311). That's the way it should be by statistics. However, close genetic related-ness to the "progenitor" population results in narrow "specialization", so to speak: nearly all of the nine breeds are meat-and-egg hens, while the distantly related breeds are either better egg-layers (Russkaya White, Moskovskaya breeds) or meat producers (Leningradskaya White).
A rather high degree of interpopulation genetic differentiation and, simultaneously, a lower level of heterozygosis - something that is characteristic of the group of specialized breeds-clearly indicate that selection entails a loss of intrapopulation genetic diversity. The reverse trend - higher heterozygosis and loss of pedigree individuality - is proper to the group of nonspecialized breeds. These are obviously the same unfavorable genetic processes induced by human activity in native populations.
As new strains and breeds are selected according to productivity characters, it often happens that alongside useful characters, those of harmful, untoward nature are also brought in (this is done inadvertently, sure). We can see that in the example of the sunflower strains said to be yielding superhigh amounts of oil. But actually these plants did not prove disease-resistant. The point is that together with high oil-yielding genes, these strains also took in late-maturing genes. And thus the sunflower seed matured by the autumn time, in a rainy period, when the root rot sets in.
Such mistakes can be avoided if novel methods of selection and seed production-certified and patented methods - are used. They allow to combine targeted selection by productivity characters with stabilizing selection by adaptability characters, that is obtain high- yield populations resistant to unfavorable external effects. Due to this, we in this country have been raising the early-maturing sunflower strain Yenisei that gives stable crops and, besides,
is adjusted to machine harvesting. Recently we at our Institute have created new productive varieties of sunflower and tomato plants that merited a Gold Medal at the First International Salon of Innovations and Investments held in Moscow in 2001.*
I hope I have shown how work in ecogenetics allows to substantiate the principles of optimal use of native and artificially evolved populations; we cannot neglect these principles if we want rational uses of the planet's biological resources.
The problem of their conservation needs closest attention, for the evolutionally established levels of intraspecies hereditary diversity are violated not only by all kinds of trades like hunting or fishing - this also happens during what looks like the well-intended job of selection and breeding, or in the course of artificial reproduction of fish shoals in nursing ponds. Whenever some genotypes are withdrawn out of proportion or when other genotypes are underutilized - or else are reproduced unevenly - such instances touch off untoward processes bringing down the vitality of populations. In order to keep their system organization intact and the correlation of their intra- and interpopulation hereditary variability at an optimum, it is essential to alter the strategy of Man/Nature interaction.
Besides the job of preserving the genetic diversity of the still extant population systems in the process of their consumption and artificial reproduction (by sustainable use of natural resources), it is also important to restore population systems already out of balance and create new systems in regions wherever appropriate natural, historical and economic conditions are on hand. Materializing these approaches, we shall be contributing to the stability of the Man/Biosphere system for many and many generations to come.
This work has received financial support from the Russian Foundation of Basic Research (Project No. 99-04-48591).
* See: Ya. Renkas, "Russian Know-How", Science in Russia, No. 3, 2001. - Ed.