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Cultural transformations of lifestyles and dietary practices have been key drivers of human evolution. However, while most of the evidence of genomic adaptations is related to the hunter-gatherer transition to agricultural societies, little is known on the influence of other major cultural manifestations. Shamanism is considered the oldest religion that predominated throughout most of human prehistory and still prevails in many indigenous populations. Several lines of evidence from ethno-archeological studies have demonstrated the continuity and importance of psychoactive plants in South American cultures. However, despite the well-known importance of secondary metabolites in human health, little is known about its role in the evolution of ethnic differences. Herein, we identified candidate genes of adaptation to hallucinogenic cactus in Native Andean populations with a long history of shamanic practices. We used genome-wide expression data from the cactophilic fly Drosophila buzzatii exposed to a hallucinogenic columnar cactus, also consumed by humans, to identify ortholog genes exhibiting adaptive footprints of alkaloid tolerance. Genomic analyses in human populations revealed a suite of ortholog genes evolving under recent positive selection in indigenous populations of the Central Andes. Our results provide evidence of selection in genetic variants related to alkaloids toxicity, xenobiotic metabolism, and neuronal plasticity in Aymara and Quechua populations, suggesting a possible process of gene-culture coevolution driven by religious practices.

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The Drosophila repleta group comprises more than one hundred species that inhabit several environments in the Neotropics and use different hosts as rearing and feeding resources. Rather homogeneous in their external morphology, they are generally distinguished by the male genitalia, seemingly their fastest evolving morphological trait, constituting an excellent model to study patterns of genital evolution in the context of a continental adaptive radiation. Although much is known about the evolution of animal genitalia at population level, surveys on macroevolutionary scale of this phenomenon are scarce. This study used a suite of phylogenetic comparative methods to elucidate the macroevolutionary patterns of genital evolution through deep time and large continental scales. Our results indicate that male genital size and some aspects of shape have been evolving by speciational evolution, probably due to the microevolutionary processes involved in species mate recognition. In contrast, several features of the aedeagus shape seemed to have evolved in a gradual fashion, with heterogeneous evolutionary phenotypic rates among clades. In general, the tempo of the evolution of aedeagus morphology was constant from the origin of the group until the Pliocene, when it accelerated in some clades that diversified mainly in this period. The incidence of novel ecological conditions in the tempo of aedeagus evolution and the relationship between species mate recognition and speciation in the Drosophila repleta group are discussed.

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Closely related species often differ in the signals involved in sexual communication and mate recognition. Determining the factors influencing signal quality (i.e. signal's content and conspicuousness) provides an important insight into the potential pathways by which these interspecific differences evolve. Host specificity could bias the direction of the evolution of sexual communication and the mate recognition system, favouring sensory channels that work best in the different host conditions. In this study, we focus on the cactophilic sibling species Drosophila buzzatii and D. koepferae that have diverged not only in the sensory channel used for sexual communication and mate recognition but also in the cactus species that use as primary hosts. We evaluate the role of the developmental environment in generating courtship song variation using an isofemale line design. Our results show that host environment during development induces changes in the courtship song of D. koepferae males, but not in D. buzzatii males. Moreover, we report for the first time that host rearing environment affects the conspicuousness of courtship song (i.e. song volume). Our results are mainly discussed in the context of the sensory drive hypothesis.

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Drosophila buzzatii and D. koepferae are sibling cactophilic species. The former breeds primarily on prickly pears (genus Opuntia) whereas the latter breeds on columnar cacti of the genera Cereus and Trichocereus, although with certain degree of niche overlapping. We examined the interspecific differences in diurnal temporal patterns of adult emergence from puparia and evaluated whether this behavior is affected by rearing in the different cactus hosts available in nature. We detected important host-dependent genetic variation for this trait differentially affecting the emergence schedule of these species. Diurnal pattern of emergence time was directly correlated with developmental time and negatively correlated with adult wing size, suggesting that early emergences are at least indirectly correlated with increased fitness. We discussed our results in terms of their putative effects on fitness and the genetic-metabolic pathways that would be presumably affected by host's nutritional-chemical differences.

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High-throughput transcriptome studies are breaking new ground to investigate the responses that organisms deploy in alternative environments. Nevertheless, much remains to be understood about the genetic basis of host plant adaptation. Here, we investigate genome-wide expression in the fly Drosophila buzzatii raised in different conditions. This species uses decaying tissues of cactus of the genus Opuntia as primary rearing substrate and secondarily, the necrotic tissues of the columnar cactus Trichocereus terscheckii. The latter constitutes a harmful host, rich in mescaline and other related phenylethylamine alkaloids. We assessed the transcriptomic responses of larvae reared in Opuntia sulphurea and T. terscheckii, with and without the addition of alkaloids extracted from the latter. Whole-genome expression profiles were massively modulated by the rearing environment, mainly by the presence of T. terscheckii alkaloids. Differentially expressed genes were mainly related to detoxification, oxidation-reduction and stress response; however, we also found genes involved in development and neurobiological processes. In conclusion, our study contributes new data onto the role of transcriptional plasticity in response to alternative rearing environments.

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Neriidae are a small family of acalyptratae flies, mostly distributed in the tropics. Very little is known about their biology, and the evolutionary relationships among species have never been evaluated. We perform the first comprehensive phylogenetic analysis of the family, including 48 species from all biogeographic regions inhabited, as well as five species of Micropezidae and one Cypselosomatidae as outgroups. We build a morphological data matrix of 194 characters, including 72 continuous characters. We first explore ways to deal with the issue of scaling continuous characters, including rescaling ranges to unity and using implied weighting. We find that both strategies result in very different phylogenetic hypotheses, and that implied weighting reduces the problem of scaling, but only partially. Furthermore, using implied weighting after rescaling characters improves the congruence between partitions and results in higher values of group support. With respect to the Neriidae, we confirm the monophyly of the family and of most its genera, although we do not obtain any of the currently accepted suprageneric groups. We propose to restrict the Eoneria and Nerius groups exclusively to the Neotropical fauna, and synonymize Glyphidops subgenus Oncopsia Enderlein with Glyphidops subgenus Glyphidops Enderlein, eliminating the subgeneric divisions. This revised phylogeny presents a striking biogeographic consistency, and shows that previous main divisions of the family were based on events of convergence.

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The evolution of cactophily in the genus Drosophila was a major ecological transition involving over a hundred species in the Americas that acquired the capacity to cope with a variety of toxic metabolites evolved as feeding deterrents in Cactaceae. D. buzzatii and D. koepferae are sibling cactophilic species in the D. repleta group. The former is mainly associated with the relatively toxic-free habitat offered by prickly pears (Opuntia sulphurea) and the latter has evolved the ability to use columnar cacti of the genera Trichocereus and Cereus that contain an array of alkaloid secondary compounds. We assessed the effects of cactus alkaloids on fitness-related traits and evaluated the ability of D. buzzatii and D. koepferae to exploit an artificial novel toxic host. Larvae of both species were raised in laboratory culture media to which we added increasing doses of an alkaloid fraction extracted from the columnar cactus T. terschekii. In addition, we evaluated performance on an artificial novel host by rearing larvae in a seminatural medium that combined the nutritional quality of O. sulphurea plus amounts of alkaloids found in fresh T. terschekii. Performance scores in each rearing treatment were calculated using an index that took into account viability, developmental time, and adult body size. Only D. buzzatii suffered the effects of increasing doses of alkaloids and the artificial host impaired viability in D. koepferae, but did not affect performance in D. buzzatii. These results provide the first direct evidence that alkaloids are key determinants of host plant use in these species. However, the results regarding the artificial novel host suggest that the effects of alkaloids on performance are not straightforward as D. koepferae was heavily affected. We discuss these results in the light of patterns of host plan evolution in the Drosophila repleta group.

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BACKGROUND: The 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. RESULTS: Our 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. CONCLUSIONS: Our 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.

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The choice of egg laying site and progeny's performance in a rearing site are important components of habitat selection. Despite the huge amount of genetic, morphological, behavioral and physiological data regarding Drosophila melanogaster Meigen and D. simulans Sturtevant, oviposition site preferences remain poorly known. We investigated resource preference (acceptance and choice) and performance (measured as larval viability, developmental time and wing size) in Vitis vinifera Linneo (grape) and Cydonia oblonga Miller (quince), two fruit plants that D. melanogaster and D. simulans use as breeding substrates in Western Argentina. Females of both species preferred V. vinifera over C. oblonga when offered to lay eggs on grape and/or quince, with D. melanogaster showing a more biased preference for V. vinifera than its sibling. Concerning performance, flies reared in C. oblonga developed faster than in V. vinifera, regardless of the species and D. simulans had a shorter developmental time than D. melanogaster. We also observed inter and intraspecific (between flies reared in different resources) differences in wing size and shape. Our study provides novel data concerning ecological aspects scarcely addressed in these species, and suggest that the use of different resource may be a relevant factor in their recent evolutionary history.

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The inversion polymorphisms of the cactophilic Drosophila buzzatti Patterson and Wheeler (Diptera: Drosophilidae) were studied in new areas of its distribution in Argentina. A total of thirty-eight natural populations, including 29 from previous studies, were analyzed using multiple regression analyses. The results showed that about 23% of total variation was accounted for by a multiple regression model in which only altitude contributed significantly to population variation, despite the fact that latitude and longitude were also included in the model. Also, inversion frequencies exhibited significant associations with mean annual temperature, precipitation, and atmospheric pressure. In addition, expected heterozygosity exhibited a negative association with temperature and precipitation and a positive association with atmospheric pressure. The close similarity of the patterns detected in this larger dataset to previous reports is an indication of the stability of the clines. Also, the concurrence of the clines detected in Argentina with those reported for colonizing populations of Australia suggests the involvement of natural selection as the main mechanism shaping inversion frequencies in D. buzzatii.

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Drosophila serido Vilela & Sene is a polytypic and cactophilic species with broad geographic distribution in Brazil. The morphology of the aedeagi of eight natural populations of D. serido was analyzed. Based on features of their aedeagi, populations of D. serido were discriminated with an efficiency of nearly 75%. The analysis using the Mantel test suggests that the morphological divergence of D. serido is correlated with the geographic distance among populations. There is no single cause to explain the observed pattern; therefore, the results were discussed considering the three main hypotheses to explain the aedeagus evolution: lock and key, pleiotropy and sexual selection. Alternatively, the aedeagus variability of D. serido might be related to environmental causes, such as temperature and/or host cacti.

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Drosophila serido Vilela & Sene é uma espécie cactofílica e politípica, com ampla distribuição geográfica no Brasil. A morfologia do edeago de indivíduos provenientes de oito populações naturais de D. serido foi avaliada. De acordo com as características dos seus edeagos, as populações de D. serido foram discriminadas com eficiência de aproximadamente 75 por cento. O resultado do teste de Mantel sugere que a divergência morfológica de D. serido é correlacionada com a distância geográfica das populações. A explicação para o padrão observado não é única. Por esta razão, os resultados foram discutidos considerando-se as três principais hipóteses para explicar a evolução do edeago: chave-fechadura, pleiotropia e seleção sexual. Alternativamente, a variabilidade encontrada nos edeagos de D. serido poderia estar relacionada a fatores ambientais, tais como temperatura e/ou cacto hospedeiro.

Drosophila serido Vilela & Sene is a polytypic and cactophilic species with broad geographic distribution in Brazil. The morphology of the aedeagi of eight natural populations of D. serido was analyzed. Based on features of their aedeagi, populations of D. serido were discriminated with an efficiency of nearly 75 percent. The analysis using the Mantel test suggests that the morphological divergence of D. serido is correlated with the geographic distance among populations. There is no single cause to explain the observed pattern; therefore, the results were discussed considering the three main hypotheses to explain the aedeagus evolution: lock and key, pleiotropy and sexual selection. Alternatively, the aedeagus variability of D. serido might be related to environmental causes, such as temperature and/or host cacti.

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In this work we investigate the effect of interspecific hybridization on wing morphology using geometric morphometrics in the cactophilic sibling species D. buzzatii and D. koepferae. Wing morphology in F1 hybrids exhibited an important degree of phenotypic plasticity and differs significantly from both parental species. However, the pattern of morphological variation between hybrids and the parental strains varied between wing size and wing shape, across rearing media, sexes, and crosses, suggesting a complex genetic architecture underlying divergence in wing morphology. Even though there was significant fluctuating asymmetry for both, wing size and shape in F1 hybrids and both parental species, there was no evidence of an increased degree of fluctuating asymmetry in hybrids as compared to parental species. These results are interpreted in terms of developmental stability as a function of a balance between levels of heterozygosity and the disruption of coadaptation as an indirect consequence of genomic divergence.

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BACKGROUND: The 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. RESULTS: Despite 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. CONCLUSION: Our 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.

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