Ortholog genes from cactophilic Drosophila provide insight into human adaptation to hallucinogenic cacti.

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.

Limited sexual segregation in a dimorphic avian scavenger, the Andean condor.

Sexual segregation is widely reported among sexually dimorphic species and generally attributed to intraspecific competition. Prey diversity and human activities can reinforce niche segregation by increasing resource heterogeneity. Here, we explored trophic and spatial sexual segregation in the only avian scavenger that exhibits pronounced sexual size dimorphism (up to 50% difference in body mass) and a highly despotic social system, the Andean condor (Vultur gryphus). We predicted that larger and dominant males would exclude smaller and subordinate females from high-quality resources, leading to sexual segregation particularly in human-dominated landscapes showing increased prey diversity. We compared resource use between females and males across six sites in Argentina featuring a range of prey diversity via stable isotopes analysis of molted feathers (n = 141 individuals). We then focused on two sites featuring contrasting levels of prey diversity and quantified assimilated diet via stable isotopes and space use via GPS monitoring (n = 23 and 12 tagged individuals). We found no clear differences in isotopic niche space, individual variation in isotopic signature, or assimilated diet between females and males. However, there were differences in foraging locations between sexes, with females apparently using areas of fewer food resources more frequently than males. Local conditions defined the dynamics of fine-scale sexual differences in foraging sites; yet, unpredictable and ephemeral carrion resources likely prevent segregation by sexes at the landscape scale. Our study highlights complex dynamics of sexual segregation in vultures and the relevancy of analyses under multiple spatial-temporal scales to explore segregation in social species.

Andean and California condors possess dissimilar genetic composition but exhibit similar demographic histories.

While genetic diversity of threatened species is a major concern of conservation biologists, historic patterns of genetic variation are often unknown. A powerful approach to assess patterns and processes of genetic erosion is via ancient DNA techniques. Herein, we analyzed mtDNA from historical samples (1800s to present) of Andean Condors (Vultur gryphus) to investigate whether contemporary low genetic variability is the result of recent human expansion and persecution, and compared this genetic history to that of California condors (Gymnogyps californianus).We then explored historic demographies for both species via coalescent simulations. We found that Andean condors have lost at least 17% of their genetic variation in the early 20th century. Unlike California condors, however, low mtDNA diversity in the Andean condor was mostly ancient, before European arrival. However, we found that both condor species shared similar demographies in that population bottlenecks were recent and co-occurred with the introduction of livestock to the Americas and the global collapse of marine mammals. Given the combined information on genetic and demographic processes, we suggest that the protection of key habitats should be targeted for conserving extant genetic diversity and facilitate the natural recolonization of lost territories, while nuclear genomic data should be used to inform translocation plans.

Pupal emergence pattern in cactophilic Drosophila and the effect of host plants.

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.

Transcriptome modulation during host shift is driven by secondary metabolites in desert Drosophila.

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.

Differences in tolerance to host cactus alkaloids in Drosophila koepferae and D. buzzatii.

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.