Constantina Rodriguez

The evolutionary history of Drosophila buzzatti. XXVI. Macrogeographic patterns of inversion polymorphism in New World populations

Inversion polymorphisms in the second and fourth chromosomes of the cactophilic Drosophila buzzatti in the native distribution range of the species are described. Over 5,000 flies from 26 localities were scored revealing interesting geographic structuring of arrangement frequencies. Multiple regression and partial correlation approaches showed that the frequencies of second and fourth chromosome arrangements vary clinically along latitudinal and altitudinal gradients and to a lesser extent with longitude. Although many non selective explanations can account for this pattern, its resemblance to the clinal pattern described in recently established Australian populations of Drosophila buzzatii, strongly suggests a selective explanation. Additionally, the correlated variation observed between the frequencies of arrangements 2St on the second chromosome and 4St on the fourth suggests a pattern of interchromosomal association, which, when considering the vast area surveyed, might be explained as the result of epistatic interactions. The analysis of population structure revealed a significant regional pattern, concordant with previously described phytogeographic regions. F‐statistics showed that the patterns of variation were different not only between the second and fourth chromosomes, but also between second chromosome arrangements, suggesting that selective differentiation might have contributed to population structure.

The evolutionary history of Drosophila buzzatii . XXIV. Second chromosome inversions have different average effects on thorax length

We demonstrate a genetic correlation between rearrangements of the second chromosome of D. buzzatii and thorax length, as a measure of body size. The results indicate that 2j and 2jz3 arrangements are correlated with large size, whereas 2st arrangement is correlated with small size. Some inversions (2st and 2jz3) show dominant effects and others (2j/jz3) exhibit overdominance. These results show that at least 25 per cent of body size variation may be accounted for by the studied karyotypes. The possible integration of the genotypic, phenotypic and fitness levels, and also the possible implications to life-history evolution theories, are discussed. These results suggest that, under moderate to high heritability values, some kinds of chromosomal endocyclic and/or balancing selection may be valuable mechanisms for maintenance of body size variation.

INVERSION POLYMORPHISM, LONGEVITY, AND BODY SIZE IN A NATURAL POPULATION OF DROSOPHILA BUZZATII

In this study we present the results of an analysis of differential longevity associated with Drosophila buzzatii second chromosome inversion karyotypes based on the assessment of more than 1000 individuals collected in a natural population. Comparisons of inversion frequencies between emerged and bait‐collected flies showed not only that inversion arrangements were associated with differential longevity, but also that selection was sex specific. Because each individual fly was scored for thorax length and karyotype, we were able to show that longevity selection favoring larger flies coupled with the average effect of inversions on thorax length can account for the change of inversion frequencies due to longevity in females. The observed genotypic‐by‐sex interaction could be an important mechanism involved in the maintenance of the polymorphism. Arrangement 2Jz3, which was shown to impaired fecundity in two independent previous studies, exhibited a positive effect on longevity. This pattern of negative pleiotropy may be another plausible mechanism accounting for the maintenance of the polymorphism.

An adaptive chromosomal polymorphism affecting size-related traits, and longevity selection in a natural population of Drosophila buzzatii

Size-related phenotypic variation among second-chromosome karyotypes inDrosophila buzzatii was examined in an Argentinian natural population. For all measured traits (thorax and wing length; wing, head and face width), this inversion polymorphism exhibited a significant and (additive) linear contribution to the phenotypic variance in newly emerged wild flies. The results suggest that only overall body size, and not body shape, is affected. as no karyotypic variation was found for any trait when the effects of differences in within-karyotype size were removed with Burnabys method. Likewise, in an experiment of longevity selection in the wild, variation in chromosomal frequencies was verified in the direction predicted on the basis of: (i) previous studies on longevity selection for body size in the wild and (ii) the pattern of chromosomal effects we observed on size. The direction of such selection is consistent with a pattern of antagonistic selection detected in previous studies on the inversion polymorphism.

The evolutionary history of Drosophila buzzatii. XVI. Fitness component analysis in an original natural population from Argentina

The adaptive significance of the chromosomal polymorphism of Drosophila buzzati has been studied by means of fitness component analysis in an original population from Argentina. The results show evidence of selection acting through pupal viability, longevity (adult viability) and fecundity on the second chromosome polymorphism, and through pupal viability and virility on the fourth chromosome polymorphism.

The evolutionary history of Drosophila buzzatii XXVII

The correlation between body size and longevity was tested in an Argentinian natural population of Drosophila buzzatii. Mean thorax length of flies newly emerging from rotting cladodes of Opuntia vulgaris was significantly smaller than that of two samples of flies caught at baits. The present results which might be interpreted as directional selection for longevity favoring larger flies are in agreement with previous results achieved in a Spanish natural population of D. buzzatii. Flies emerging from different substrates showed significant differences in thorax length, suggesting that an important fraction of phenotypic variance can be attributed to environmental variability. However, laboratory and field work in different populations of D. buzzatii showed a significant genetic component for thorax length variation.

Contrasting population genetic structures using allozymes and the inversion polymorphism in Drosophila buzzatii

Second chromosome inversion and genotypic frequencies at seven allozyme loci, differentially associated with inversions, were determined in seven natural populations of Drosophila buzzatii. The patterns of variation of allozymes and the inversion polymorphisms were significantly different, indicating the role of adaptive differentiation for the latter. Moreover, the patterns of population structure varied among allozyme loci, suggesting the operation of diversifying selection for certain loci. Differentiation was negligible for Leucyl‐amino peptidase (Lap) and Peptidase‐2 (Pep‐2), low to moderate for Aldehyde oxidase (Aldox), Peptidase‐1 (Pep‐1) and Esterase‐1 (Est‐1) and high for Esterase‐2 (Est‐2) and Xanthine dehydrogenase (Xdh). Significant linkage disequilibria were detected between inversions and Aldox, Est‐1, Est‐2 and Xdh. Multiple regression analyses of inversion and allele frequencies on environmental variables revealed the existence of clines for inversions, Est‐1, Est‐2, Xdh and Aldox along altitudinal, latitudinal and/or climatic gradients. Tests using conditional allele frequencies showed that Est‐1 and Aldox clines could be accounted for by hitchhiking with inversions, whereas natural selection should be invoked to explain the clines observed for Est‐2 and Xdh.

The evolutionary history of Drosophila buzzatii . XXXIII. Are Opuntia hosts a selective factor for the inversion polymorphism

Previous work has shown fitness differences among chromosomal arrangements by means of selection component analysis in two Drosophila buzzatii natural populations, one of which is native to Argentina and the other a colonized population from Carboneras, Spain. Founder effects or niche shifts were proposed to explain the differences observed in the pattern of pleiotropic effects of inversions on fitness components. In this paper, we address the possible role of niche shifts by determining whether differential attraction to, oviposition on, or utilization of the rotting cladodes of two different Opuntia species (O. quimilo and O. ficus-indica) occurred among individuals carrying different second chromosome karyotypes in a natural Argentinian population. Through the analysis of more than 2500 individuals comprising five different life cycle stages associated with the necroses of these two cactus species, we found that the distributions of inversion frequencies in samples of adult flies, third instar larvae and emerging adults collected on both Opuntia species were not significantly different. Likewise, no evidence of differential oviposition was observed. These findings suggest that niche shifts cannot, solely, account for the changes observed in the Carboneras population. In addition, the selection component analysis did not reveal any significant relationship between chromosomal arrangements and the fitness components tested. These results suggest either that fitness differences might be too small to be detected or that the assumptions of the model concerning the mode of selection may not be tenable in the studied population.

Inversion and allozyme polymorphism show contrasting patterns of microgeographical population structure in a natural population of Drosophila buzzatii from Argentina

Second chromosome inversions and genotypic frequencies at seven allozyme loci were determined in a natural population of the cactophilic species Drosophila buzzatii that uses as breeding sites the necrotic cladodes of the prickly pear Opuntia quimilo and the rotting stems of cardón, Trichocereus terschekii. Different processes govern the evolutionary fate of inversion and allozyme polymorphisms. A pattern of heterotic balance for inversions seems to be acting uniformly in each breeding site and could depend on different regimes of density‐dependent selection within cactus hosts. Patterns of variation of allozymes revealed significant heterogeneity in allele frequencies for Esterase‐1 (Est‐1) among O. quimilo rots and Aldehyde oxidase (Aldox) and Xanthine dehydrogenase (Xdh) among T. terschekii substrates and showed gene‐cactus effects only for Esterase‐2 (Est‐2). Consistent and significant excesses of homozygotes were detected at both the within‐rot and in the total population levels that could be accounted for by diversifying selection among individual breeding sites.

Genetic structure is determined by stochastic factors in a natural population of Drosophila buzzatii in Argentina

D. buzzatii is a cactophilic species associated with several cactaceae in Argentina. This particular ecological niche implies that this species is faced with a non-uniform environment constituted by discrete and ephemeral breeding sites, which are colonized by a finite number of inseminated females. The genetic consequences of this population structure upon the second chromosome polymorphism were investigated by means of F-statistics in a natural endemic population of Argentina. The present study suggests that differentiation of inversion frequencies in third instar larvae among breeding sites has taken place mainly at random and selection is not operating to determine the structure of this population. The average number of parents breeding on a single pad seems to be similar to the number colonizing Opuntia ficus indica rotting cladodes in Carboneras, a derived population from Spain. There is no significant excess of heterokaryotypes within pads or in the population as a whole. The results obtained in the present study suggest that the potential role of selective versus stochastic factors relative to the among pad heterogeneity in the population here studied is different from that of the Spanish population previously reported. Potential mechanisms responsible for these differences are discussed.