Mutations affecting fitness in Drosophila populations.

Summary

1. An understanding of the adaptive strategies of colonizing animal species depends upon an integration of population genetics and ecology, but behavioural components should not be ignored especially higher in the phylogenetic series than insects.



2. An ecologically marginal habitat from which colonists are derived can be regarded as one in which physical stresses of climatic origin tend to be variable and extreme, so that resources are unpredictable and short lived. Prerequisites for genetic analysis are therefore phenotypes relatable to the r K continuum of adaptive strategies. These can be called ‘ecological phenotypes’.



3. Ecological phenotypes include tolerances to environmental stresses, development time, and resource utilization variability. Such phenotypes enable distinctions to be made between colonizing species and non-colonists. For example, colonizing species have ecological phenotypes incorporating high resistance to physical stress, rapid development time, and the exploitation of an array of food resources. They are ecologically versatile generalists. This includes the use of ethanol as a resource in Drosophila.



4. There is a substantial literature on variation in central and marginal populations based upon gene and chromosome polymorphisms. Most data show a reduction of chromosome polymorphisms and of lethals and semilethals towards the margins, but no equivalent reduction in enzyme polymorphisms. Widespread species tend to have low levels of chromosome polymorphisms as in marginal populations, but enzyme polymorphism levels vary too much among species for meaningful interpretations. Since these are genotypic assessments not directly relatable to the field situation, the somewhat unsatisfactory nature of these data from the interpretative point of view is understandable. In addition, the fundamental issue is not the variability of the genome, but the nature and role of loci controlling ecological phenotypes.



5. Ecological phenotypes can be analyzed at the population level with isofemale strains as the starting material. In theory, genetic activity can then be localized to the chromosomal and even genic levels in a species such as D. melanogaster. Isofemale strain studies in D. melanogaster are interpretable in terms of the r K continuum, and so reflect adaptive strategies in nature.



6. It is highly likely that the genetic architecture of ecological phenotypes of marginal populations mainly comprises a few additive genes of relatively large effect. This is an architecture permissive of rapid adaptation to new habitats, provided that the appropriate genes are present. Discussions of speciation via the founder principle, a colonization event in itself, have invoked a similar explanation.

Adaptive strategies of colonizing animal species

The feeding- and breeding-sites of Drosophila obscura Fallén and D. subobscura Collin

The study of the first laboratory generation of isofemale lines ofDrosophila melanogaster, founded by wild flies collected in populations of various geographical origins, has shown that virgin females differ in their capacity to control egg deposition. This capacity to delay the ovulation process when no sexual partner is available is genetically determined. The present study shows that the frequency distribution of the various phenotypes varies progressively along a latitudinal cline from Afrotropical to European regions, or from neotropical to nearctic areas, while a few oriental populations appear off the cline. This variation in initial retention capacity, added to a similar variation in number of ovarioles conditioning a potential increase in fecundity for mated flies, induces variation in reactivity to insemination which may be an adaptation to a variable environment. Moreover, similar study of F1 virgin females from isofemale lines founded by wild flies collected in Spring, Summer and Autumn in two French populations over ten successive years revealed that seasonal genetic variations occur in this capacity to postpone egg-laying in case of non-insemination. The frequency of the different phenotypes follows cyclical seasonal variations. Long retention phenotypes are more frequent in Spring and Autumn samples, whereas short retention phenotypes, closer to the ancestral African type, are more common in Summer generations. This balancing selection temporarily modifies the genetic equilibrium of the population, enhancing its competitive ability. Temperature appears to be the primordial selective factor both in geographical and in seasonal variations.

Clinal and seasonal variations in initial retention capacity of virginDrosophila melanogaster females as a strategy for fitness

By means of the marker strain Va/Ba wild chromosomes O of Drosophila subobscura were extracted from eight natural populations situated on a north-south gradient from Sweden or Scotland to Tunesia. Lethal frequencies and viability effects of the wild chromosomes O were studied in homozygous and random heterozygous combinations. In accordance with results from other Drosophila species random heterozygotes were always more viable than homozygotes. The viability-determining polygene system proved, however, dominant to some degree. Geographic differences became apparent especially with respect to three different characteristics: (1) The lethal frequencies for chromosomes O from central populations are higher than for those from northern and southern marginal populations; (2) Mean viabilities of non-lethal homozygotes and random heterozygotes are lower for central than for marginal populations; (3) The increase of viability through heterozygosity is more pronounced in the northern populations than in the others. The differences are thought to be mainly due to differences in the adaptation strategy of marginal and central populations. The viability fitness components seem of more importance for the marginal populations while fertility components may be of greater weight under central conditions. The geographic variability of the viability polygene system is finally compared with that of other genetic traits in D. subobscura.

Wild O chromosomes of Drosophila subobscura from different geographic regions have different effects on viability

We have attempted to make quantitative comparisons between the genetic systems provoked by some neo-tropical environments and a European one. These comparisons permit certain clarifications regarding the comprehension of the genetic load and of the genetic “norm” in reference to particular ecological characteristics.

Population genetics in the American tropics. II. The comparative genetics ofDrosophila in european and neo-tropical environments

Our comparative genetic study with the second chromosome of Drosophila melanogaster from Hungary and Colombia (25) produced a quantitative appraisal of the detrimental, normal, subvital, and supervital loads. Results such as these lend support to the theory that the genetic characteristics of a gene pool reflect the ecological situation of the population. The most prominent and significant data in this direction were reported for populations of D. pseudoobscura on Mount San Jacinto in California (6,9,16), and of D. pseudoobscura and D. persimilis in Yosemite Park, California (7,8). These pioneering works and our present one detected changes in time. However, while Dobzhansky’s shifts were described in terms of the relative frequencies of various karyotypes for which they were found to be polymorphic, our present report deals with genetic modifications in viability similar to those found in Fusagasuga (26). The profound changes in the organization of the genetic architecture found in Fusagasuga were caused by recurrent cycles of rainfall-bound seasons in the area. Our analysis revealed surprising shifts in the mean viability of homozygotes. Furthermore, a suggestive correlation appeared between rain cycles and the genetic load observed. If maximum and minimum temperatures had been used to describe the climatogical situation, as was done in the past, we would not have detected anything consistent with the cyclic shifts in lethals and semilethals. Other work (27) revealed that even within 7 months significant shifts in the sterility content in the second chromosome of D. melanogaster from Fusagasuga could be effected by the cyclic rainfall-bound seasons. Testing for heterogeneity among homozygotes of the different temporal populations showed the coexistence of a high- and a low-sterility group. Further partitioning of X 2 in contingency tables revealed that through female sterility in the dry season and male sterility in the wet season the local demographic unit is altered. Still other works (21,22) have shown how even reforestation can produce profound genetic changes within a single area.

Population genetics in the American Tropics. IX. Rhythmic genetic changes that prove the adaptive nature of the detrimental load in Drosophila melanogaster from Caracolisito, Colombia.

Samples ofDrosophila melanogaster were taken each month over several years from a locality in Fusagasuga, Colombia. Temporal shifts in gene frequencies were found. These reflect important adaptive changes in the populations, and the kind of gene pool modifications that are necessary for the better occupation of local temporal niches.

Population genetics in the American tropics. IV. Temporal changes effected in natural populations ofDrosophila melanogaster from Colombia

Samples ofD. melanogaster have revealed fluctuations in sterility genes in Fusagasuga, Colombia, over a period of seven months covering a wet and a dry season. These samples were taken from a single locality in a circle of 10 m diameter within 20 min of collecting. The temporal shiftsin, gene frequencies found in male carriers fit the weather changes in that local niche. Our observations suggest that sterility genes may be part of an adaptive system which controls and modifies the effective population size.

Population genetics in the American tropics. V. The sterility content in the second chromosomes of Drosophila melanogaster from Fusagasugá, Colombia.

Cordeiro (1952) and Cordeiro and Dobzhansky (1954) have noticed that the same chromosome in different combinations can produce variable viability. Wallace and King (1952), Greenberg and Crow (1960), Hiraizumi and Crow (1960), and others have presented evidence to show that the drastic chromosomes were exerting average deleterious effects under heterozygous conditions. The works by Morton, Crow and Muller (1956) criticized mathematically by Li (1963a, b, c) and by Sanghvi (1963) emphasize a hypothesis which says that the general viability, mortality, or morbidity in outbred and inbred lines show a decrease in viability in heterozygous carriers for those deleterious genes. On the other hand, there are results by Masing (1938, 1939a), Berg (1942, 1943, 1944), and Wallace (1956, 1959, 1960, 1962) which indicate the existence of overdominance in Drosophila. Some authors, e.g., Berg (1942, 1943), have results which indicate that the appearance of lethals as deleterious, neutral, or heterotic in heterozygotes varied in different populations. Other authors, e.g., Wallace have suggested that chromosomes with deleterious effects on viability in homozygotes are often selectively advantageous when carried in heterozygous condition. In one of Wallace's papers (1962) he points out that most investigators have overlooked the fact that viability effects of lethal and semilethal chromosomes in heterozygous condition seem to depend upon the source of the homologous chromosome. The distribution of the genetic variants in various Colombian populations have already been presented (Hoenigsberg and de Navas, 1965). In the present article the authors have made some statistical analyses in or-

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1558-5646.1968.tb03450.x

L. A. Granobles

Papers

Population genetics in the American tropics. II. The comparative genetics ofDrosophila in european and neo-tropical environments

Population genetics in the American Tropics. IX. Rhythmic genetic changes that prove the adaptive nature of the detrimental load in Drosophila melanogaster from Caracolisito, Colombia.

Population genetics in the American tropics. IV. Temporal changes effected in natural populations ofDrosophila melanogaster from Colombia

Population genetics in the American tropics. V. The sterility content in the second chromosomes of Drosophila melanogaster from Fusagasugá, Colombia.

Population genetics in the american tropics iii. the genetic role of heterozygous individuals in various colombian populations of d. melanogaster.