Juan J. Fanara

Evolution of male genitalia: environmental and genetic factors affect genital morphology in two Drosophila sibling species and their hybrids.

BackgroundThe rapid evolution of genital morphology is a fascinating feature that accompanies many speciation events. However, the underlying patterns and explanatory processes remain to be settled. In this work we investigate the patterns of intraspecific variation and interspecific divergence in male genitalic morphology (size and shape) in the cactophilic sibling species Drosophila buzzatii and D. koepferae. Genital morphology in interspecific hybrids was examined and compared to the corresponding parental lines.ResultsDespite of being siblings, D. buzzatii and D. koepferae showed contrasting patterns of genital morphological variation. Though genitalic size and shape variation have a significant genetic component in both species, shape varied across host cacti only in D. buzzatii. Such plastic expression of genital shape is the first evidence of the effect of rearing substrate on genitalic morphology in Drosophila. Hybrid genital morphology was not intermediate between parental species and the morphological resemblance to parental strains was cross-dependent.ConclusionOur results suggest the evolution of different developmental networks after interspecific divergence and the existence of a complex genetic architecture, involving genetic factors with major effects affecting genital morphology.

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.

Oviposition preference and life history traits in cactophilic Drosophila koepferae and D. buzzatii in association with their natural hosts

Drosophila koepferae and D. buzzatii are two closely related cactophilic species inhabiting the arid lands of southern South America. Previous studies have shown that D. buzzatii breeds primarily on the necrotic cladodes of several Opuntia cacti and D. koepferae on the rotting stems of columnar cacti of the genera Trichocereus and Cereus. In this paper, we analyze the patterns of host plant utilization in a locality where both Drosophila species are sympatric. Field studies showed an absence of differential attraction of adult flies to the rots of two major host cacti: O. sulphurea and T. terschekii. However, the proportion of D. buzzatii flies emerged from the rotting cladodes of O. sulphurea was significantly higher than in T. terschekii. In laboratory experiments, egg to adult viability in single species cultures varied when both Drosophila species were reared in media prepared with O. sulphurea or T. terschekii. In addition, between-species comparisons of flies emerged from single species cultures showed that D. buzzatii adults were smaller and developed faster than D. koepferae. Furthermore, analysis of flies emerged in mixed species cultures showed differences in oviposition preference and oviposition behavior. We discuss the observed between-species differences and suggest that these traits are the result of adaptation to specific patterns of spatial and temporal predictability of their respective preferred host plants: columnar are less dense and less ephemeral resources, whereas the opuntias are more abundant, and fast rotting cacti.

Oviposition acceptance and fecundity schedule in the cactophilic sibling species Drosophila buzzatii and D. koepferae on their natural hosts.

Abstract We tested for the occurrence of oviposition acceptance for different media prepared with cactus tissues of three alternative cactus hosts: Opuntia sulphurea, O. quimilo and Trichocereus terschekii for 4 consecutive days in lines of two Drosophila buzzatii populations and one population of D. koepferae. Our results showed that the former laid significantly more eggs on both Opuntia cacti than on T. terschekii, whereas D. koepferae preferred T. terschekii. In addition, fecundity schedules differed between species: D. buzzatii laid similar numbers of eggs along the fourday sampling period, whereas D. koepferae showed an oviposition peak on the second day of egg collection on T. terschekii. We suggest that the between‐species disparities observed in oviposition acceptance and fecundity schedule may be related to the temporal and spatial predictability of Opuntia versus T. terschekii (cardón) as part of the different adaptive strategies that have evolved after the split of D. koepferae and D. buzzatii from their recent common ancestor. Therefore, the willingness to accept hosts would be an important factor in the habitat selection and in the maintenance of species diversity.

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.

Identifying candidate genes affecting developmental time in Drosophila melanogaster: pervasive pleiotropy and gene-by-environment interaction

BackgroundUnderstanding the genetic architecture of ecologically relevant adaptive traits requires the contribution of developmental and evolutionary biology. The time to reach the age of reproduction is a complex life history trait commonly known as developmental time. In particular, in holometabolous insects that occupy ephemeral habitats, like fruit flies, the impact of developmental time on fitness is further exaggerated. The present work is one of the first systematic studies of the genetic basis of developmental time, in which we also evaluate the impact of environmental variation on the expression of the trait.ResultsWe analyzed 179 co-isogenic single P[GT1]-element insertion lines of Drosophila melanogaster to identify novel genes affecting developmental time in flies reared at 25°C. Sixty percent of the lines showed a heterochronic phenotype, suggesting that a large number of genes affect this trait. Mutant lines for the genes Merlin and Karl showed the most extreme phenotypes exhibiting a developmental time reduction and increase, respectively, of over 2 days and 4 days relative to the control (a co-isogenic P-element insertion free line). In addition, a subset of 42 lines selected at random from the initial set of 179 lines was screened at 17°C. Interestingly, the gene-by-environment interaction accounted for 52% of total phenotypic variance. Plastic reaction norms were found for a large number of developmental time candidate genes.ConclusionWe identified components of several integrated time-dependent pathways affecting egg-to-adult developmental time in Drosophila. At the same time, we also show that many heterochronic phenotypes may arise from changes in genes involved in several developmental mechanisms that do not explicitly control the timing of specific events. We also demonstrate that many developmental time genes have pleiotropic effects on several adult traits and that the action of most of them is sensitive to temperature during development. Taken together, our results stress the need to take into account the effect of environmental variation and the dynamics of gene interactions on the genetic architecture of this complex life-history trait.

Courtship success and multivariate analysis of sexual selection on morphometric traits inDrosophila buzzatii (Diptera: Drosophilidae)

Using wild-reared flies, we examined sexual selection on five phenotypic traits (thorax length, wing length, wing width, head width, and face width) inDrosophila buzzatii, by scoring copulatory status in nine mass mating cages. Only male face width was identified as a direct target of sexual selection in an analysis of selection gradient, while indirect selection was present on all other studied traits, as expected from their correlations with face width. In contrast to males, there was no indication of selection in females. Nor was there evidence of assortative mating. The suggested direct selection on face width seems to take place during licking behavior of the courtship and might be related to courtship feeding. This study suggests that courtship success gives rise to indirect selection on body size.

Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation

BackgroundThe Drosophila wing represents a particularly appropriate model to investigate the developmental control of phenotypic variation. Previous studies which aimed to identify candidate genes for wing morphology demonstrated that the genetic basis of wing shape variation in D. melanogaster is composed of numerous genetic factors causing small, additive effects. In this study, we analyzed wing shape in males and females from 191 lines of D. melanogaster, homozygous for a single P-element insertion, using geometric morphometrics techniques. The analysis allowed us to identify known and novel candidate genes that may contribute to the expression of wing shape in each sex separately and to compare them to candidate genes affecting wing size which have been identified previously using the same lines.ResultsOur results indicate that more than 63% of induced mutations affected wing shape in one or both sexes, although only 33% showed significant differences in both males and females. The joint analysis of wing size and shape revealed that only 19% of the P-element insertions caused coincident effects on both components of wing form in one or both sexes. Further morphometrical analyses revealed that the intersection between veins showed the smallest displacements in the proximal region of the wing. Finally, we observed that mutations causing general deformations were more common than expected in both sexes whereas the opposite occurred with those generating local changes. For most of the 94 candidate genes identified, this seems to be the first record relating them with wing shape variation.ConclusionsOur results support the idea that the genetic architecture of wing shape is complex with many different genes contributing to the trait in a sexually dimorphic manner. This polygenic basis, which is relatively independent from that of wing size, is composed of genes generally involved in development and/or metabolic functions, especially related to the regulation of different cellular processes such as motility, adhesion, communication and signal transduction. This study suggests that understanding the genetic basis of wing shape requires merging the regulation of vein patterning by signalling pathways with processes that occur during wing development at the cellular level.

Genotype by environment interactions in viability and developmental time in populations of cactophilic Drosophila

The genetic and ecological basis of viability and developmental time differences between Drosophila buzzatii and D. koepferae were analysed using the isofemale line technique. Several isofemale lines were sampled from pairs of allopatric/sympatric populations of each species. Flies were reared in media prepared with decaying tissues of two of the main natural cactus hosts of each species. This experimental design enabled us to evaluate the relative contribution of phenotypic plasticity, genetic variation and genotype by environment interaction (G × E) to total phenotypic variation for two fitness traits, viability and developmental time. Our results revealed significant G × E in both traits, suggesting that the maintenance of genetic variation can be explained, at least in part, by diversifying selection in different patches of a heterogeneous environment in both species. However, the relative importance of the factors involved in the G × E varied between traits and populations within species. For viability, the G × E can be mainly attributed to changes in the rank order of lines across cacti. However, the pattern was different for developmental time. In D. buzzatii the G × E can be mainly accounted for by changes in among line variance across cacti, whereas changes in the rank order of lines across cacti was the main component in D. koepferae. These dissimilar patterns of variation between traits and species suggest that the evolutionary forces shaping genetic variation for developmental time and viability vary between populations within species and between species.

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.