Genic Variation In Natural Populations Research Articles

A comprehensive study of genic variation in natural populations of Drosophila melanogaster. VII. Varying rates of genic divergence as revealed by two-dimensional electrophoresis.

Four sibling species from the melanogaster subgroup (Drosophila melanogaster, D. simulans, D. sechellia, and D. mauritiana) were studied for genetic divergence, by high-resolution two-dimensional protein electrophoresis (2DE) coupled with ultrasensitive silver staining. A total of eight tissues from larval and adult developmental stages representing both gonadal (germ-line) and nongonadal (somatic) tissues were analyzed for protein divergence between species. Close to 400 polypeptides (protein spots) were scored from each tissue and species, and protein divergence was measured on the basis of qualitative differences (presence/absence) of protein spots in pairwise species comparisons. The observed levels of genic divergence varied among tissues and among species. When larval hemolymph proteins (which are known to be highly polymorphic) were excluded, there was no evidence to suggest that either the larval or adult-stage proteins, as a whole, are more diverged than the other; variation between different tissues rather than between developmental stages appears to be the most significant factor affecting genetic divergence between species. The reproductive tissue (testis and accessory gland) showed more divergence than did the nonreproductive tissue; D. melanogaster testis (from both larvae and adult males) showed the highest level of divergence. In view of the previous observation that D. simulans, D. mauritiana, and D. sechellia show similar but significantly less reproductive isolation from each other than from D. melanogaster, the present results suggest a correlation between the levels of reproductive-tract-protein divergence and the degree of reproductive isolation in these species.

A comprehensive study of genic variation in natural populations of Drosophila melanogaster. VI. Patterns and processes of genic divergence between D. melanogaster and its sibling species, Drosophila simulans.

We present here an extensive set of data on allelic differences between homologous proteins of Drosophila melanogaster and its sibling species, Drosophila simulans, obtained by nondenaturing one-dimensional, and denaturing two-dimensional gel electrophoresis. The data suggest that, for these two species, (1) approximately 10% of protein-coding loci have no alleles in common in our sample, (2) the extent of genic variation at a locus (mean heterozygosity) within a species is not correlated with the extent of divergence (Nei's genetic distance) at that locus between species, and (3) significant heterogeneity of divergence rates exists for different structural/functional classes of loci. These results are discussed in the context of the dynamics of genetic variation within and between species.

A comprehensive study of genic variation in natural populations of Drosophila melanogaster. V. Structural–functional constraints on protein molecules and enzymes and the levels and patterns of variation among genes

Ever since isozyme-allozyme polymorphisms were detected there has been an incessant effort to relate the amount of observed protein variation to various aspects of molecular structure and function. Structural-functional constraints can limit the amount of overall genic variation, and the observed variation can be due to neutral mutation and random genetic drift, mutation-selection balance, or balancing selection. The present analysis of structural-functional constraints on gene-enzyme variation in natural populations of Drosophila melanogaster shows that while both subunit size and substrate group show significant effects on number of alleles and mean heterozygosity, only substrate group affects population structure significantly. Subunit structure (monomer vs. multimer), IUB enzyme class (e.g., transferase, lyase), and tolerance of null alleles showed no significant effect on level or pattern of variation. While partly interdependent, these results suggest that efforts should be made to distinguish between constraints arising from molecular structure and physiological function.

A comprehensive study of genic variation in natural populations of Drosophila melanogaster. IV. Mitochondrial DNA variation and the role of history vs. selection in the genetic structure of geographic populations.

Preliminary studies with restriction fragment length polymorphisms of mitochondrial DNA (mtDNA) in natural populations of Drosophila melanogaster revealed considerable variation in terms of nucleotide sequence and overall size. In this report we present data from more isofemale lines and more restriction enzymes, and explore the utility of the data in inferring a colonization history of this species. Size variation in the noncoding A + T-rich region is particularly plentiful, with size variants occurring in all restriction site haplotypes in all populations. We report here classes of small-scale mobility polymorphisms (apparent range of 20 bp) in specific restriction fragments in the coding region. The variation in one such fragment appears to be generated even more rapidly than in the noncoding region. On the basis of the distribution of restriction site haplotypes, the species range can be divided into three major regions along longitudinal lines: Euro-African populations are the most diverse and are taken to be oldest; Far East populations have a complex distribution of haplotypes; Western Hemisphere populations are the least diverse and are interpreted to be the youngest. The history inferred from mtDNA alone is remarkably similar to one based on several nuclear markers. The mtDNA haplotype distribution is also very different from that of allozymes in these same populations. We interpret this as further evidence that natural selection is still the most parsimonious explanation for the parallel latitudinal allozyme clines in this species.

GEOGRAPHIC VARIATION IN THE MILKFISH CHANOS CHANOS. I. BIOCHEMICAL EVIDENCE.

Since the first use of protein gel electrophoresis for the assessment of genic variation in natural populations (Lewontin and Hubby, 1966), a large number of plants and animals across many phylogenetic lines has been surveyed for electrophoretic variation. Results of these surveys and synopses of the related evolutionary hypotheses have been summarized in Lewontin (1974), Ayala (1976), and Nevo (1978). In reviewing these reports, it is apparent that one group of organisms has been generally overlooked: the marine fishes. For instance, many workers have examined the population structure of freshwater fishes (Avise and Selander, 1972; Avise and Smith, 1974; Echelle et al., 1975; Allendorf et al., 1976; Vrijenhoek et al., 1977; and others), yet there are virtually no data available for widely distributed marine fishes. In comparable studies of marine fishes, the work has dealt with diadromous fishes (Koehn and Williams, 1978; Utter et al., 1980), estuarine fishes (Johnson, 1975), or fishes from restricted geographic areas (Gorman et al., 1976; Gorman and Kim, 1977; Ward and Beardmore, 1977). In only one report were genetic differences assessed for a marine fish found in separate localities across the tropics, but this study remains unpublished (Soule, reference in Ehrlich, 1975). It is generally assumed that because of a planktonic larval stage, marine fish have a high potential for gene flow and hence may show little interlocality differentiation, but this topic remains unexplored. It would be interesting, therefore, to assess patterns of geographic differentiation of fish populations within and among archipelagos across an ocean basin. It has long been realized that small and/ or isolated populations may undergo considerable genetic changes. Semi-isolated populations of cavefish Astyanax mexicanus had reduced levels of electrophoretic variation relative to conspecific surface populations (Avise and Selander, 1972), and stream populations of Etheostoma radiosum, separated in different drainages of the same tributary, exhibited high levels of population differentiation (Echelle et al., 1975). In a marine habitat the epitome of isolation of an ichthyofauna is the Hawaiian inshore fish community. Randall (1976) estimates the level of endemism for the inshore fishes is 29%-the highest value for any oceanic island. Yet, there have been no electrophoretic estimates of the degree of isolation of the fishes in Hawaii. Thus, using electrophoretic data, the following questions were examined for the milkfish Chanos chanos: 1) What is the level of genic variation in this species and how does it change over large geographic distances? 2) What is the genetic population structure for a marine fish, such as Chanos, that has a planktonic larval stage? 3) What factors affect the observed pattern of geographic variation and how does the level of geographic differentiation compare to that of other species-terrestrial and marine? 4) How genetically isolated is the Hawaiian population of milkfish relative to other milkfish populations? Life history of milkfish. -Milkfish, Chanos chanos (Forskal), are tropical marine fish distributed throughout the Pacific 1 Hawaii Institute of Marine Biology Contribution No. 586.

Genic heterogeneity within electrophoretic "alleles" and the pattern of variation among loci in Drosophila pseudoobscura.

An investigation, similar to our previously reported xanthine dehydrogenase study, was undertaken to examine the extent of hidden genic variation at nine loci (five larval proteins, three esterases and one aldehyde oxidase) by sequential application of various electrophoretic criteria employing pH, gel concentration and buffer variation. Polymorphic loci appear to fall into two distinct groups: weakly polymorphic, including larval protein 6, 7, 8, 10 and 13 and esterase-1 and -6; and highly polymorphic, including esterase-5, Xdh and possibly Ao. Monomorphic loci may belong to a third group different from all polymorphic loci. Bogota, a geographical isolate that is reproductively isolated from the mainland population, was found to be genetically distinct at four of the ten loci examined in detail so far, including Xdh, whereas previously it was found to be genetically distinct at none. These results are discussed in the light of balancing selection, neutral and mutation-selection hypotheses of genic variation in natural populations.

SUBSTRATE-SPECIFIC ENZYME VARIATION IN NATURAL POPULATIONS OF DROSOPHILA PSEUDOOBSCURA

By using a number of different alcohols as substrates, eight alcohol dehydrogenase loci were discovered in Drosophila pseudoobscura. Each of these loci can take more than one substrate. Several of these loci differed in their tissue specificities and activity patterns during development. The genic variation in natural populations was studied at four of these loci and three of them were polymorphic. A quantitative study of substrate-specific differences among alleles of the same locus produced negative results. This result appears to be typical of most studies done on this aspect. From this it was concluded that the substrate specificity of enzymes is not an important factor in determining the greater amount of genic variation at Group II loci than at Group I loci, as proposed by KOJIMA, GILLESPIE and TOBARI (1970). There are several observations which suggest a different explanation for the differences in the genic variability at Group I and Group II loci: (1) There are, on an average, more isozyme loci (loci with similar substrate specificity) for enzymes in Group II than in Group I; (2) The null alleles are far more common at Group II loci than at Group I loci; (3) There is significant heterogeneity in the number of alleles and the heterozygosities at loci within each of these two groups of enzymes; (4) Relatively higher levels of genic variation are observed at Group II loci even in populations which appear to be living in homogeneous environments; and (5) Some loci (e.g. esterases) are highly polymorphic in most species investigated by gel electrophoresis techniques. Based on these general observations, it is proposed that (1) the substrate-specific differences are between isozyme loci and not between alleles of a given locus, and (2) neutral alleles are proportionately far more common at loci at Group II than at loci in Group I, because the former is under less selection constraint than the latter.

Measurement of fitness at the esterase-5 locus in Drosophila pseudoobscura.

KNOWLEDGE of the amount of genic variation in natural populations is the first step towards understanding how such variation is maintained. The first systematic studies of the amount of genic variation in natural populations of Drosophila pseudoobscura were reported by HUBBY, LEWONTIN, and co-workers (HUBBY and LEWONTIN 1966; LEWONTIN and HUBBY 1966; PRAKASH, LEWONTIN and HUBBY 1969) who estimated that 40% of the loci are polymorphic and that on the average 12% of loci per individual are heterozygous in North American populations of the species. Similar estimates of heterozygosity have now been made for several organisms, including mice (SELANDER and YANG 1969) and humans (HARRIS 1969; LEWONTIN 1967). All these estimates indicate that the proportion of polymorphic loci in natural populations may be much greater than was previously supposed. Were these polymorphisms maintained primarily by heterosis operating independently at each locus, populations probably would not be able to tolerate the huge genetic load involved (see LEWONTIN and HUBBY 1966). SVED, REED and BODMER (1967) have attempted to solve this dilemma by postulating that there is a limit to maximum fitness because of gene interaction. Owing to the rarity of the maximally fit genotypes, the amount of reduction in the selective advantage of heterozygote over homozygote at individual loci is extremely small. KING (1967) proposed a different threshold model in which he assumed that a certain proportion of the population with the “worst combination of genes, environment, and luck” will be eliminated by natural selection. The effect of KING’S model is similar to that of SVED, REED and BODMER (1967) both in the sense that maximal fitness is approached asymptotically as heterozygosity increases, and that there are thousands of different genotypes with essentially the same fitness. According to these models a large number of polymorphic loci can be maintained without increasing genetic load to an excess. However, both hypotheses fail to explain the relatively small loss of fitness found when natural populations are inbred. The hypothesis of neutrality or very small selection coefficients of allozymes as proposed by KIMURA (1968) may be adequate to explain the maintenance of large amounts of polymorphism by assuming a rather high mutation rate, migration rate, and population size, but it does not appear to be an adequate explanation of