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Dehydration is a stress factor for organisms inhabiting natural habitats where water is scarce. Thus, it may be expected that species facing arid environments will develop mechanisms that maximize resistance to desiccation. Insects are excellent models for studying the effects of dehydration as well as the mechanisms and processes that prevent water loss since the effect of desiccation is greater due to the higher area/volume ratio than larger animals. Even though physiological and behavioral mechanisms to cope with desiccation are being understood, the genetic basis underlying the mechanisms related to variation in desiccation resistance and the context-dependent effect remain unsolved. Here we analyze the genetic bases of desiccation resistance in Drosophila melanogaster and identify candidate genes that underlie trait variation. Our quantitative genetic analysis of desiccation resistance revealed sexual dimorphism and extensive genetic variation. The phenotype-genotype association analyses (GWAS) identified 71 candidate genes responsible for total phenotypic variation in desiccation resistance. Half of these candidate genes were sex-specific suggesting that the genetic architecture underlying this adaptive trait differs between males and females. Moreover, the public availability of desiccation data analyzed on the same lines but in a different lab allows us to investigate the reliability and repeatability of results obtained in independent screens. Our survey indicates a pervasive micro-environment lab-dependent effect since we did not detect overlap in the sets of genes affecting desiccation resistance identified between labs.

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Survival and reproduction are the core elements of Darwinian fitness. In the context of a fixed energy budget, organisms tend to allocate resources in order to maximize one at the expense of the other, in what has been called the lifespan-reproduction trade-off. Reproductive arrest and extended lifespan are common responses to low temperatures in many insects including fruit flies. In this study, we aim to understand the overwintering strategy of two closely-related Drosophila species with contrasting distribution ranges. We compared survival, lifespan, ovarian maturation, and reproductive output (fecundity and fertility) of virgin and mated adults of both Drosophila buzzatii and Drosophila koepferae after long-term cold exposure at dormancy-inducing conditions (10 °C, 10:14 L:D) and controls (25 °C, 12:12 L:D). Virgin flies of D. buzzatii showed the longest lifespan (averaging 102 days) under dormancy-inducing conditions. Cold-induced reproductive arrest preserves reproductive capacity mainly in virgin females that mated after reproductive dormancy, indicating that males were much more susceptible to fertility loss than females, in both species. Notably, females of D. buzzatii were capable of protecting stored sperm from cold damage and produced viable progeny. Even if, in D. buzzatii, fertility of flies mated after the cold-exposure was extremely low, cold temperature likely sterilized D. koepferae males, indicating that cold carry-over effects are stronger for the species with the shorter lifespan. Such species-specific effects of low temperature over fitness likely contributed to the divergence of these closely-related species and to the spread of D. buzzatii into cooler environments.

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In phytophagous insects, oviposition behaviour is an important component of habitat selection and, given the multiplicity of genetic and environmental factors affecting its expression, is defined as a complex character resulting from the sum of interdependent traits. Here, we study two components of egg-laying behaviour: oviposition acceptance (OA) and oviposition preference (OP) in Drosophila melanogaster using three natural fruits as resources (grape, tomato and orange) by means of no-choice and two-choice experiments, respectively. This experimental design allowed us to show that the results obtained in two-choice assays (OP) cannot be accounted for by those resulting from no-choice assays (OA). Since the genomes of all lines used are completely sequenced, we perform a genome-wide association study to identify and characterize the genetic underpinnings of these oviposition behaviour traits. The analyses revealed different candidate genes affecting natural genetic variation of both OA and OP traits. Moreover, our results suggest behavioural and genetic decoupling between OA and OP and that egg-laying behaviour is plastic and context-dependent. Such independence in the genetic architectures of OA and OP variation may influence different aspects of oviposition behaviour, including plasticity, canalization, host shift and maintenance of genetic variability, which contributes to the adoption of adaptive strategies during habitat selection.

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Hypogeococcus pungens is a species complex native to southern South America that is composed of at least five putative species, each one specialized in the use of different host plants. Two of these undescribed species were registered as invasive in Central and North America: Hyp-C is a cactophagous mealybug that became an important pest that threatens endemic cactus species in Puerto Rico, and Hyp-AP feeds on Amaranthaceae and Portulacaceae hosts, but does not produce severe damage to the host plants. We quantified genomic variation and investigated the demographic history of both invasive species by means of coalescent-based simulations using high throughput sequencing data. We also evaluated the incidence of host plant infestation produced by both species and used an ecological niche modeling approach to assess potential distribution under current and future climatic scenarios. Our genetic survey evinced the footprints of strong effective population size reduction and signals of genetic differentiation among populations within each species. Incidence of plant attacks varied between species and among populations within species, with some host plant species preferred over others. Ecological niche modeling suggested that under future climatic scenarios both species would expand their distribution ranges in Puerto Rico. These results provide valuable information for the design of efficient management and control strategies of the Puerto Rican cactus pest and shed light on the evolutionary pathways of biological invasions.

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The choice of criteria to delimit a group or class is a subjective matter, even though the reasoning, the objectives and the criteria themselves should always be clearly stated. This paper is part of a discussion about the criteria used to identify seminal fluid proteins (SFPs) in Drosophila species. SFPs are proteins that are transferred to females during copulation together with sperm. The only way to ascertain that a protein is an SFP is to prove that it is produced in a male reproductive organ and is found in the female reproductive tract after insemination. Nevertheless, the required methodology is labour-intensive and expensive, and therefore this kind of data is unlikely to be available for many species, precluding comparative and evolutionary studies on the subject. To conduct evolutionary analyses, in a previous study, we capitalized on the accumulated knowledge we have in the model species D. melanogaster to recommend a set of criteria for identifying candidate SFPs in other Drosophila species. Those criteria, based on transcriptomic evidence and in silico predictions from sequences, would allow a good balance between sensitivity (the inclusion of true SFPs) and specificity (the exclusion of false positives). In view of the criticism raised by another group, here we defend our criteria on one hand while accepting there is room for improvement on the other. The results are updated sets of criteria and SFPs that we believe can be useful in future evolutionary studies.

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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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Cities usually offer a suitable environment for the dengue vector Aedes aegypti, providing oviposition sites, accessibility to human hosts and nectar meals. However, large urban centres are highly heterogeneous environments, forming a patched landscape that could affect Ae. aegypti population dynamics and dispersal. Here, we performed a genome-wide analysis using Rad-seq data from 99 Ae. aegypti specimens collected in three areas within Buenos Aires city with varying levels of urbanization/land use: highly urbanized Area 1, intermediate Area 2 and poorly urbanized Area 3. We found an inverse association between urbanization levels and spatial genetic structure. Populations from highly urbanized Area 1 did not present genetic structure whereas two and three clusters were detected in Areas 2 and 3, respectively. In the case of Area 3, initial analyses showed separation in clusters was mostly due to elevated consanguinity within sites although three clusters were still detected after closely related individuals were discarded. Mosquitoes around each site displayed a high degree of isolation, evidencing a close dependence between the vector and human dwellings. Interestingly, specimens from distant boroughs (within the limits of the city) and the city's outskirts formed a single cluster with inner city sites (Area 1), highlighting the role of passive transport in shaping population structure. Genetic distances were poorly correlated with geographic distances in Buenos Aires, suggesting a stronger influence of passive than active dispersal on population structure. Only Area 2 displayed a significant isolation-by-distance pattern (p = 0.046), with males dispersing more than females (p = 0.004 and p = 0.016, respectively). Kinship analyses allowed us to detect full-siblings located 1.5 km apart in Area 1, which could be due to an extreme event of active female dispersal. Effective population size was higher in Area 2 confirming that cemeteries represent highly favourable environments for Ae. aegypti and need to be specifically targeted. Our results suggest that control programs should take into account urban landscape heterogeneity in order to improve vector control.

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While the striking effects of seminal fluid proteins (SFPs) on females are fairly conserved among Diptera, most SFPs lack detectable homologues among the SFP repertoires of phylogenetically distant species. How such a rapidly changing proteome conserves functions across taxa is a fascinating question. However, this and other pivotal aspects of SFPs' evolution remain elusive because discoveries on these proteins have been mainly restricted to the model Drosophila melanogaster. Here, we provide an overview of the current knowledge on the inter-specific divergence of the SFP repertoire in Drosophila and compile the increasing amount of relevant genomic information from multiple species. Capitalizing on the accumulated knowledge in D. melanogaster, we present novel sets of high-confidence SFP candidates and transcription factors presumptively involved in regulating the expression of SFPs. We also address open questions by performing comparative genomic analyses that failed to support the existence of many conserved SFPs shared by most dipterans and indicated that gene co-option is the most frequent mechanism accounting for the origin of Drosophila SFP-coding genes. We hope our update establishes a starting point to integrate further data and thus widen the understanding of the intricate evolution of these proteins.

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Surveys of patterns of genetic variation in natural sympatric and allopatric populations of recently diverged species are necessary to understand the processes driving intra- and interspecific diversification. The South American moths Cactoblastis cactorum, Cactoblastis doddi and Cactoblastis bucyrus are specialized in the use of cacti as host plants. These species have partially different geographic ranges and differ in patterns of host plant use. However, there are areas that overlap, particularly, in northwestern Argentina, where they are sympatric. Using a combination of genome-wide SNPs and mitochondrial data we assessed intra and interspecific genetic variation and investigated the relative roles of geography and host plants on genetic divergence. We also searched for genetic footprints of hybridization between species. We identified three well delimited species and detected signs of hybridization in the area of sympatry. Our results supported a hypothetical scenario of allopatric speciation in the generalist C. cactorum and genetic interchange during secondary geographic contact with the pair of specialists C. bucyrus and C. doddi that probably speciated sympatrically. In both cases, adaptation to new host plants probably played an important role in speciation. The results also suggested the interplay of geography and host plant use as drivers of divergence and limiting gene flow at intra and interspecific levels.

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Despite considerable progress in recent decades in dissecting the genetic causes of natural morphological variation, there is limited understanding of how variation within species ultimately contributes to species differences. We have studied patterning of the non-sensory hairs, commonly known as "trichomes," on the dorsal cuticle of first-instar larvae of Drosophila. Most Drosophila species produce a dense lawn of dorsal trichomes, but a subset of these trichomes were lost in D. sechellia and D. ezoana due entirely to regulatory evolution of the shavenbaby (svb) gene. Here, we describe intraspecific variation in dorsal trichome patterns of first-instar larvae of D. virilis that is similar to the trichome pattern variation identified previously between species. We found that a single large effect QTL, which includes svb, explains most of the trichome number difference between two D. virilis strains and that svb expression correlates with the trichome difference between strains. This QTL does not explain the entire difference between strains, implying that additional loci contribute to variation in trichome numbers. Thus, the genetic architecture of intraspecific variation exhibits similarities and differences with interspecific variation that may reflect differences in long-term and short-term evolutionary processes.

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Aedes aegypti is the primary vector of arboviruses of great impact on human health. Our goal was to assess the spatial genetic structure of Ae. aegypti at the regional and local levels in Northwestern Argentina, an area with high prevalence of dengue fever. We analyzed 59 Ae. aegypti individuals collected from six locations in Northwestern Argentina using nuclear genome-wide Single Nucleotide Polymorphisms (SNPs) generated with double digest Restriction-site Associated DNA Sequencing. We also performed an entomological survey in 70 households in the cities of Orán and Tartagal. An analysis at the regional level indicated that the populations of Ae. aegypti in Northwestern Argentina are spatially structured and present a significant IBD pattern. Our results suggest that passive transport of eggs/immature stages, in both northward and southward directions, plays an important role in structuring Ae. aegypti populations at a regional scale and also as a source for the introduction of novel genetic variants through migration events into established populations. At a local level, we found neither spatial genetic structure nor significant isolation by distance (IBD) in Tartagal, indicating high gene flow within the city and active dispersal. In contrast, samples from Orán formed two clusters with a significant IBD pattern, although weaker than that at a regional level. Both populations showed signs of recent bottleneck events, probably coincident with past eradication campaigns. The entomological survey revealed a high prevalence of Ae. aegypti in both cities, although significantly higher in Tartagal.

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The Drosophila repleta group is an array of more than 100 species endemic to the "New World", many of which are cactophilic. The ability to utilize decaying cactus tissues as breeding and feeding sites is a key aspect that allowed the successful diversification of the repleta group in American deserts and arid lands. Within this group, the Drosophila buzzatii cluster is a South American clade of seven closely related species in different stages of divergence, making them a valuable model system for evolutionary research. Substantial effort has been devoted to elucidating the phylogenetic relationships among members of the D. buzzatii cluster, including molecular phylogenetic studies that have generated ambiguous results where different tree topologies have resulted dependent on the kinds of molecular marker used. Even though mitochondrial DNA regions have become useful markers in evolutionary biology and population genetics, none of the more than twenty Drosophila mitogenomes assembled so far includes this cluster. Here, we report the assembly of six complete mitogenomes of five species: D. antonietae, D. borborema, D. buzzatii, two strains of D. koepferae and D. seriema, with the aim of revisiting phylogenetic relationships and divergence times by means of mitogenomic analyses. Our recovered topology using complete mitogenomes supports the hypothesis of monophyly of the D. buzzatii cluster and shows two main clades, one including D. buzzatii and D. koepferae (both strains), and the other containing the remaining species. These results are in agreement with previous reports based on a few mitochondrial and/or nuclear genes, but conflict with the results of a recent large-scale nuclear phylogeny, indicating that nuclear and mitochondrial genomes depict different evolutionary histories.

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Hypogeococcus pungens, a mealybug native of southern South America, is devastating native cacti in Puerto Rico and threatening cactus diversity in the Caribbean, and potentially in Central and North America. The taxonomic status of H. pungens is controversial since it has been reported feeding not only on Cactaceae but also on other plant families throughout its distribution range. However, in Australia, where the species had been exported from Argentina to control weedy American cacti, it was never found on host plants other than Cactaceae. These conflicting pieces of evidence not only cast doubt on the species identity that invaded Puerto Rico, but also have a negative impact on the search for natural enemies to be used in biological control programs against this pest. Here we present reproductive incompatibility and phylogenetic evidences that give support to the hypothesis that H. pungens is a species complex in which divergence appears to be driven by the host plants. The nuclear EF1α and 18S and the mitochondrial COI genes were used as markers to evaluate the phylogenetic relationships among H. pungens populations collected in Argentina, Australia and Puerto Rico feeding on Cactaceae and/or Amaranthaceae. Additionally, we conducted reciprocal crosses between mealybugs from both hosts. Species delimitation analysis revealed two well-supported putative species within H. pungens, one including mealybugs feeding on Amaranthaceae (H. pungens sensu stricto), and a new undescribed species using Cactaceae as hosts. Additionally, we found asymmetric reproductive incompatibility between these putative species suggesting recent reproductive isolation. The Bayesian species delimitation also suggested that the Australian mealybug population may derive from another undescribed species. Overall, the patterns of genetic differentiation may be interpreted as the result of recent speciation events prompted by host plant shifts. Finally, the finding of a single haplotype in the Puerto Rico population suggests only one invasive event. We still need to identify the geographical origin of the pest in order to enable the use of biological control to reduce the threat to cacti diversity in the Caribbean.

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Host plant shifts in herbivorous insects often involve facing new environments that may speed up the evolution of oviposition behavior, performance-related traits, morphology, and, incidentally, reproductive isolation. In the genus Drosophila, cactophilic species of the repleta group include emblematic species in the study of the evolution of host plant utilization. The South American D. buzzatii and its sibling D. koepferae are a model system for the study of differential host plant use. Although these species exhibit a certain degree of niche overlap, the former breeds primarily on decaying cladodes of Opuntia cacti while D. koepferae main hosts are columnar cacti of the genus Trichocereus. Opuntia sulphurea and Trichocereus terscheckii are among the main hosts in nature. These cacti differ in ecological (spatial and temporal predictability) and chemical characteristics. Particularly relevant is the presence of toxic alkaloids in T. terscheckii. Studies of the effects of these cacti and alkaloids revealed the remarkable impact on oviposition behavior, viability, developmental time, wing morphology, mating success, and developmental stability in both species. Recent whole-genome expression studies showed that expression profiles are massively affected by the rearing cactus, and that the presence of alkaloids is the main factor modulating gene expression in D. buzzatii. Functional enrichment analysis indicated that differentially expressed genes are related to detoxification processes and stress response-though genes involved in development are an important part of the transcriptomic response. The implications of our studies in the evolution of host plant use in the 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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Courtship songs have undergone a spectacular diversification in the Drosophila buzzatii cluster. Accordingly, it has been suggested that sexual selection has played a significant role in promoting rapid diversification, reproductive isolation and speciation. However, there is no direct evidence (i.e., song playback experiments with wingless males) supporting this tenet. Moreover, several studies have showed that the courtship song in the genus Drosophila is not always used in female mate choice decisions, nor plays the same role when it is taken into account. In this vein, we use an approach that combines manipulative and playback experiments to explore the importance and the role of courtship song in female mate choice in four species of the D. buzzatii cluster and one species of the closely related D. martensis cluster for outgroup comparison. We also investigate the importance of courtship song in sexual isolation in sympatry between the only semi-cosmopolitan species, D. buzzatii, and the other species of the D. buzzatii cluster. Our study revealed that the courtship song is used by females of the D. buzzatii cluster as a criterion for male acceptance or influences the speed with which males are chosen. In contrast, we showed that this characteristic is not shared by D. venezolana, the representative species of the D. martensis cluster. We also found that the studied species of the D. buzzatii cluster differ in the role that conspecific and heterospecific songs have in female mate choice and in sexual isolation. Our findings support the hypothesis that divergence in female preferences for courtship songs has played a significant role in promoting rapid diversification and reproductive isolation in the D. buzzatii cluster. However, evidence from D. venezolana suggests that the use of the courtship song in female mate choice is not a conserved feature in the D. buzzatii complex.

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Long-term exposure to low temperatures during adult maturation might decrease fertility after cold recovery as a consequence of carry-over effects on reproductive tissues. This pattern should be more pronounced in tropical than in temperate species as protective mechanisms against chilling injuries are expected to be more effective in the latter. We initially determined the lower thermal thresholds to induce ovarian maturation in four closely related Drosophila species, two inhabiting temperate regions and the other two tropical areas of South America. As expected, only temperate species regularly experience cold-inducing conditions for reproductive arrest during winter in their natural environment. Subsequently, we exposed reproductively arrested and mature females to cold-inducing conditions for reproductive arrest over a long period. Following cold exposure, tropical species exhibited a dramatic fertility decline, irrespective of reproductive status. In contrast, not only were temperate females fecund and fertile but also fertility was superior in females that underwent cold-induced reproductive arrest, suggesting that it might act as a protecting mechanism ensuring fertility after cold recovery. Based on these findings, we decided to evaluate the extent to which reproductive status affects cold tolerance and energy metabolism at low temperature. We found a lower metabolic rate and a higher cold tolerance in reproductively arrested females, although only temperate species attained high levels of chill tolerance. These findings highlight the role of cold-induced reproductive arrest as part of an integrated mechanism of cold adaptation that could potentially contribute to the spread of temperate species into higher latitudes or altitudes.

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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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Body size is a complex character associated to several fitness related traits that vary within and between species as a consequence of environmental and genetic factors. Latitudinal and altitudinal clines for different morphological traits have been described in several species of Drosophila and previous work identified genomic regions associated with such variation in D. melanogaster. However, the genetic factors that orchestrate morphological variation have been barely studied. Here, our main objective was to investigate genetic variation for different morphological traits associated to the second chromosome in natural populations of D. melanogaster along latitudinal and altitudinal gradients in Argentina. Our results revealed weak clinal signals and a strong population effect on morphological variation. Moreover, most pairwise comparisons between populations were significant. Our study also showed important within-population genetic variation, which must be associated to the second chromosome, as the lines are otherwise genetically identical. Next, we examined the contribution of different candidate genes to natural variation for these traits. We performed quantitative complementation tests using a battery of lines bearing mutated alleles at candidate genes located in the second chromosome and six second chromosome substitution lines derived from natural populations which exhibited divergent phenotypes. Results of complementation tests revealed that natural variation at all candidate genes studied, invected, Fasciclin 3, toucan, Reticulon-like1, jing and CG14478, affects the studied characters, suggesting that they are Quantitative Trait Genes for morphological traits. Finally, the phenotypic patterns observed suggest that different alleles of each gene might contribute to natural variation for morphological traits. However, non-additive effects cannot be ruled out, as wild-derived strains differ at myriads of second chromosome loci that may interact epistatically with mutant alleles.

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Under the preference-performance hypothesis, natural selection will favor females that choose oviposition sites that optimize the fitness of their offspring. Such a preference-performance relationship may entail important consequences mainly on fitness-related traits. We used the well-characterized cactus-Drosophila system to investigate the reproductive capacity in the pair of sibling species D. buzzatii and D. koepferae reared in two alternative host plants. According to our hypothesis, ovariole number (as a proxy of reproductive capacity) depends on host plant selection. Our results indicate that the capacity of D. buzzatii showed to be mild, only increasing the number of ovarioles by as much as 10% when reared in its preferred host. In contrast, D. koepferae exhibited a similar reproductive capacity across host cacti, even though it showed a preference for its primary host cactus. Our study also revealed that D. buzzatii has a larger genetic variation for phenotypic plasticity than its sibling, although ovariole number did not show clear-cut differences between species. We will discuss the weak preference-performance pattern observed in these cactophilic species in the light of nutritional and toxicological differences found between the natural host plants.