On the relation between heterozygosity and heterosis: an evaluation of the evidence from marine mollusks.
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Biomedical subjects
Publications and source records attributed to E Zouros.
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Electrophoretic surveys of two lizard species were used to test hypotheses that relate levels of enzyme variability to enzyme function (single-substrate versus multiple-substrate enzymes, regulatory versus nonregulatory enzymes). Anolis roquet behaviorally regulates its body temperature, but its congener A. gundlachi is passive to variations in the thermal environment. As a result, populations of A. gundlachi probably experience the thermal environment as temporally coarse-grained, whereas populations of A. roquet do not. We therefore predicted that A. gundlachi would exhibit greater enzyme heterozygosity than A. roquet and that different enzyme classes would contribute disproportionately to this interspecific difference. The data show (1) that A. gundlachi does have a higher heterozygosity and (2) that this difference appears to result from high levels of heterozygosity at loci coding for multiple-substrate enzymes. The dichotomy between regulatory and nonregulatory enzymes offers no explanation for the variability in heterozygosity among enzyme loci in these species.
An esterase duplication is described in the sibling species pair Drosophila mojavensis and Drosophila arizonensis. We present evidence for two separate structural loci mapping at a distance of less than 0.16 recombination units from each other. Alleles at the two loci have the same substrate specificities and form small amounts of interlocus heterodimers. One locus (Est-5) is functioning throughout the insect's life cycle and appears at high concentrations in the hemolymph and the fat body. Its duplicate (Est-4) functions only during the late larval stage and is concentrated mainly in the carcass. No null alleles at either locus were observed in population surveys. An examination of 12 other species from the repleta group, to which D. mojavensis and D. arizonesis belong, suggests that Est-5 is universally present, but the activity levels of Est-4 vary among species and may be totally absent in some species. Variation in the level of Est-4 activity does not closely follow the phylogenetic relationship.
In a larval esterase of Drosophila mojavensis there are alleles whose products preferentially hydrolyze alpha-naphthyl esters, whereas the majority of the alleles hydrolyze preferentially beta-naphthyl esters. In a collection of laboratory stocks alpha alleles have a frequency of 15%. Three different mobilities of alpha alleles were discovered, suggesting a polymorphism rather than a single mutation event. If substrate-preference polymorphisms are common among "multiple-substrate" enzymes (category II of Gillespie and Langley 1974), allozyme variation at these enzyme loci may well be maintained by balancing selection.
A method is presented for estimating relative mutation rates or relative effective population sizes, under the hypothesis of adaptively neutral allelic variation. This method was applied to seven surveys of electrophoretic variation. It was observed that electrophoretic mutation rates so obtained follow the gamma distribution and, in Drosophila, are positively correlated with the molecular weights of the enzymes subunits. The variance in mutation rate is larger under the step-wise model of electrophoretic mutation than under the infinite-alleles model. Rates for the most variable loci may exceed rates for less variable loci by a factor of 500. For completely invariant loci, this factor may be as high as 4 X 10(4), an observation suggesting that these loci are subject to purifying selection. In contrast to mutation rates, effective population sizes may vary at the most by a factor of ten. These results support the hypothesis that differences in the amount of electrophoretic variability among polymorphic loci may reflect differences in the rate by which electrophoretically detectable variation is generated in population.
When alleles are combined into few detectable classes, linkage correlations are underestimated most of the time. The probability that the linkage correlation will be underestimated is a function of the actual degree of correlation and the evenness of the allelic distribution, but is mainly determined by the distribution of alleles into distinguishable classes. With only two alleles per class this probability will usually be higher than 0.7. Also, the consistency in the sign of the linkage disequilibrium over many populations may escape detection. An increase of sample size by one order of magnitude or more may be required to compensate for the loss in detection power. It follows that the available electrophoretic studies of linkage correlations, although negative in their majority, do not suggest that epistatic interactions and linkage disequilibria are rare in natural populations.
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In species of repleta group of Drosophila about 70% of the electrophoretic variability is absorbed by the same chromosome which absorbs about 70% of the cytological variability of the group. However, this does not imply that inversions are actively involved in the maintenance of protein variation. A comparison of cytological and electrophoretic variation of homologous chromosomes points out that the amount of cytological polymorphism varies greatly over species of Drosophila while electrophoretic variation does not. This suggests that allelozymes do not constitute part of the coadapted complexes of genes characterizing the inversions. Rather, the amount of electropheptide molecule and is largely independent of factors such as background genotype and differences in the environment.
Gametic frequencies at four enzyme loci of the second chromosome of Drosophila mojavensis race B were obtained from six localities. The four loci were selected so that they code for functionally related enzymes; two code for esterases, one for xanthine dehydrogenase and one for acetaldehyde oxidase. In Drosophila the two latter enzymes are under the same regulatory control and their physiological functions might be related as well. Electrophoretic variants at the locicoding for these two enzymes were found not tobe in pair-wise linkage equilibrium. Other pair-wise combinations were in linkage equilibrium. It is argued that selectively maintained nonrandom associations may occur frequently between linked loci, the enzymatic products of which are functionally related, share common subunits or are under the same regulatory control.
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Gametic frequencies in one mainland and one island population of D. subobscura were obtained by means of extracting wild chromosomes and subsequently analyzing them for inversions and allozymes. The high degree of cytological heterogeneity which characterizes these populations is not reflected in the genetic data. Two cases of non-random association were observed among eighteen pair-wise comparisons involving gene alleles and inversions to which the locus is linked. In both cases exchange of alleles at the locus is completely suppressed by the inversions. Four cases of linkage disequilibrium were detected among eighteen pairs of loci; two of them could best be explained as transient associations generated by random drift. The results suggest that disequilibria among enzyme loci are not widespread in natural populations-Populations with a lower degree of chromosomal variation are genetically as variable as populations with a higher degree of chromosomal variation. This observation does not support the hypothesis that selection in marginal homokaryotypic populations is for specialized homozygous genotypes.
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The chromosomal determination of interspecific differences in mating behavior was studied in the interfertile pair, Drosophila arizonensis and Drosophila mojavensis, by means of chromosomal substitutions. Interspecific crossing over was avoided by crossing hybrid males to parental females, and identification of the origin of each chromosome in backcrossed hybrids was possibly by means of allozyme markers. It was found that male mating behavior is controlled by factors located in the PGM-marked chromosome (which, in other Drosophila species, is part of the X chromosome) and in the Y chromosome. The other chromosomes influence male sexual behavior through their interactions with each other and with the PGM-marked chromosome, but their overall effect is minor. Female mating behavior is controlled by factors located in the ODH-marked and AMY-marked chromosomes, with the other chromosomes exercising a small additive effect. Hence, the two sex-specific behaviors are under different genetic control. Cytoplasmic origin has no effect on the mating behavior of either sex. There appears to be no correlation between a chromosome's structural diversity (i.e., amounts of inversion polymorphism within a species or numbers of fixed inversions across species) and its contribution to sexual isolation. These findings are in general agreement with those from similar Drosophila studies and may not be specific to the species studied here.