A forest‐specialist carnivore in the middle of the desert?Comments on Anabalon et al. 2019

We present comments on an article recently published in Ecology and Evolution (“High‐resolution melting of the cytochrome B gene in fecal DNA: A powerful approach for fox species identification of the Lycalopex genus in Chile”) by Anabalon et al. that reported the presence of Darwin's fox (Lycalopex fulvipes), a temperate forest specialist, in the hyperarid Atacama Desert of northern Chile. We argue that this putative record lacks ecological support in light of ongoing research on this endangered species, and contains numerous methodological flaws and omissions related to the molecular identification of the species. Based on these issues, we suggest the scientific community and conservation decision‐makers disregard the alleged presence of the Darwin's fox in the Atacama Desert.     

Disrupted phylogeographical microsatellite and chloroplast DNA patterns indicate a vicariance rather than long‐distance dispersal origin for the disjunct distribution of the Chilean endemic Dioscorea biloba (Dioscoreaceae) around the Atacama Desert

Aim The Chilean endemic Dioscorea biloba (Dioscoreaceae) is a dioecious geophyte that shows a remarkable 600 km north–south disjunction in the peripheral arid area of the Atacama Desert. Its restricted present‐day distribution and probable Neogene origin indicate that its populations have a history linked to that of the Atacama Desert, making this an ideal model species with which to investigate the biogeography of the region. Location Chile, Atacama Desert and peripheral arid area. Methods Two hundred and seventy‐five individuals from nine populations were genotyped for seven nuclear microsatellite loci, and plastid trnL–F and trnT–L sequences were obtained for a representative subset of these. Analyses included the estimation of genetic diversity and population structure through clustering, Bayesian and analysis of molecular variance analyses, and statistical parsimony networks of chloroplast haplotypes. Isolation by distance was tested against alternative dispersal hypotheses. Results Microsatellite markers revealed moderate to high levels of genetic diversity within populations, with those from the southern Limarí Valley showing the highest values and northern populations showing less exclusive alleles. Bayesian analysis of microsatellite data identified three genetic groups that corresponded to geographical ranges. Chloroplast phylogeography revealed no haplotypes shared between northern and southern ranges, and little haplotype sharing between the two neighbouring southern valleys. Dispersal models suggested the presence of extinct hypothetical populations between the southern and northern ranges. Main conclusions Our results are consistent with prolonged isolation of the northern and southern groups, mediated by the life‐history traits of the species. Significant isolation was revealed at both large and moderate distances as gene flow was not evident even between neighbouring valleys. Bayesian analyses of microsatellite and chloroplast haplotype diversity identified the southern area of Limarí as the probable area of origin of the species. Our data do not support recent dispersal of D. biloba from the southern range into Antofagasta, but indicate the fragmentation of an earlier wider range, concomitant with the Pliocene–Pleistocene climatic oscillations, with subsequent extinctions of the Atacama Desert populations and the divergence of the peripheral ones as a consequence of genetic drift.     

Historical and ecological divergence among populations of Monttea chilensis (Plantaginaceae), an endemic endangered shrub bordering the Atacama Desert,Chile

The coastal deserts of northern Chile show an important latitudinal gradient of aridity with more arid areas to the north of the Atacama Desert than to the south. Several plant species have disjunct distributions that correspond with the extremes of this latitudinal gradient. In this study, using genetic (chloroplast and nuclear DNA), morphological (vegetative and floral traits of various kinds) and climatic and topographic information, we explored ecological and historical events that have putatively shaped patterns of variation among Monttea chilensis populations—a species that shows this disjunct distribution. Through phylogeographic and phylogenetic analyses, two divergent lineages were identified located at the latitudinal extremes. The lineage located northern lineage (NG) of the Atacama Desert showed more genetic diversity and better-resolved phylogeographic structure than the southern lineage (SG). Considerable morphological variation across the geographical range corresponds with these genetic groups. We observed contrasting relationships between floral and vegetative traits: populations from the most arid region NG possessed larger flowers, but smaller vegetative values, and vice versa. Niche modelling and multivariate analyses, including environmental data, revealed different environmental requirements for each lineage. NG plants occur in regions with warmer and drier climatic conditions and at higher altitudes, while SG populations inhabit colder and more humid environments and lower altitudes. The evolutionary history of M. chilensis exhibits a phylogeographical footprint consistent with past fragmentation and allopatric differentiation, where the hyper-arid zone formed by the Atacama Desert clearly acted as an important gene flow barrier. This barrier has led to considerable differentiation in morphology and ecology, resulting in two ecotypes or geographical races, suggesting incipient speciation promoted by local adaptation and geographical isolation.     

High‐resolution melting of the cytochrome B gene in fecal DNA: A powerful approach for fox species identification of the Lycalopex genus in Chile

Easy, economic, precise species authentication is currently necessary in many areas of research and diagnosis in molecular biology applied to conservation studies of endangered species. Here, we present a new method for the identification of three fox species of the Lycalopex genus in Chile. We developed an assay based on high‐resolution melt analysis of the mitochondrial cytochrome B gene, allowing a simple, low cost, fast, and accurate species determination. To validate the assay applicability for noninvasive samples, we collected fecal samples in the Atacama Desert, finding unexpectedly one species outside of its known distribution range. We conclude that the assay has a potential to become a valuable tool for a standardized genetic monitoring of the Lycalopex species in Chile.     

Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile

Little is known about the nature of the association between mycobionts and photobionts in isolated lichen communities. Here we studied the photobiont diversity of different Caloplaca species in a fog-induced community in the Atacama Desert. We compared nrDNA ITS sequences of both symbionts, photobionts and mycobionts, along with morphological characters of the different lichen thalli, to investigate the diversity and to assess the degree of selectivity and specificity of photobiont species in a community of Caloplaca species. Specimens of six fungal species (C. orthoclada, C. fernandeziana, and four undescribed species) were sampled along an altitudinal gradient on a coastal bluff with a strong fog presence, 60 km south of Iquique, Chile. The photobiont species in this community belong to three species of the genus Trebouxia in the strict sense: T. arboricola, T. decolorans, and T. gigantea. Most of the fungal species were lichenized with photobionts belonging to different haplotypes of T. arboricola and T. decolorans, although the algae of three specimens, associated with two fungal species (C. orthoclada and C. sp1), were related to representatives of T. gigantea. These results indicate that members of the genus Caloplaca in northern Chile have moderate photobiont selectivity and appear to be selective to members of the T. arboricola group. Also, at high altitudes, changes in the photobiontal haplotype composition were observed in comparison to lower altitudes, probably generated by a higher water availability given higher fog condensation and precipitation in the upper areas of the bluff. This may suggest that ecological factors, such as altitude and water availability could result in a local shift of the associated photobiont and specialization as a product of local adaptation.     

Natural product diversity of actinobacteria in the Atacama Desert

The Atacama Desert of northern Chile is considered one of the most arid and extreme environment on Earth. Its core region was described as featuring “Mars-like” soils that were at one point deemed too extreme for life to exist. However, recent investigations confirmed the presence of diverse culturable actinobacteria. In the current review, we discuss a total of 46 natural products isolated to date representing diverse chemical classes characterized from different actinobacteria isolated from various locations in the Atacama Desert. Their reported biological activities are also discussed.     

From ancient to contemporary molecular eco-epidemiology of Chagas disease in the Americas

One of the best-studied populations with regard to Chagas disease is from the coastal area of northern Chile at the foot of the western Andean slopes. The extremely arid climate here generates rapid, spontaneous desiccation of buried bodies, arresting the decay process. The absence of rainfall then preserves these dried bodies (mummies) for millennia. The aim of the present study was to perform the first molecular paleoepidemiological study on a set of 43 mummified human remains from the Atacama Desert in Northern Chile in order to elucidate the transmission dynamics and determinants of ancient genotypes, to try to unravel the natural history of the Trypanosoma cruzi taxon and Chagas disease. Interestingly, TcBat, a recently described Discrete Taxonomic Unit, emerges as the plausible ancestor of T. cruzi. The findings herein presented allow us to present a plausible model of T. cruzi transmission in pre-Columbian civilisations.     

Climatic niche evolution in the Andean genus <Emphasis Type="Italic">Menonvillea</Emphasis> (Cremolobeae: Brassicaceae)

The study of how climatic niches change over evolutionary time has recently attracted the interest of many researchers. Different methodologies have been employed principally to analyze the temporal dynamics of the niche and specially to test for the presence of phylogenetic niche conservatism. Menonvillea, a genus of Brassicaceae including 24 species, is distributed primarily along the Andes of Argentina and Chile, with some taxa growing in southern Patagonia and others in the Atacama Desert and the Chilean Matorral. The genus is highly diversified morphologically but also presents a remarkably wide ecological range, growing from the high Andean elevations, to the dry coastal deserts in Chile, or the Patagonia Steppe in Argentina. In this study, we used molecular phylogenies together with climatic data to study climatic niche evolution in the genus. The results show that the main climatic niche shifts in Menonvillea occurred between the sections Cuneata-Scapigera and sect. Menonvillea throughout the Mid-Late Miocene, and associated with the two main geographical distribution centers of the genus: the highlands of the central-southern Andes and the Atacama Desert-Chilean Matorral, respectively. Climatic niches in these lineages were mainly differentiated by the aridity and potential evapotranspiration, the minimum temperatures of the coldest month, and the temperature annual range and seasonality. Niche evolution in Menonvillea deviated from a Brownian motion process, with most of the climatic dimension best-fitting to an Ornstein-Uhlenbeck model of multiple adaptive peaks. Our results also indicated that higher aridity levels and lower annual temperature ranges were associated with the evolution of the annual habit, as exemplified by the distribution of sect. Menonvillea. Finally, the results suggested that climatic niche evolution in Menonvillea exhibited some degree of phylogenetic niche conservatism, fundamentally within the two main lineages (sect. Menonvillea and sects. Cuneata-Scapigera).     

Seasonal diet by a generalist raptor: the case of the variable hawk (Geranoaetus polyosoma) at Atacama Desert,northern Chile

We determined the seasonal diet of the variable hawk, Geranoaetus polyosoma, in a hyperarid and threatened habitat in the Atacama Desert, northern Chile, by analysing the contents of the bird's pellets. We estimated the biomass and number of individuals of each prey species consumed. We compared our results with those of other studies on G. polyosoma in South America. In general, the diet was characterised by extremely low number of prey, low diversity of species consumed and high dietary breadth. In contrast with other biomes of Chile, in our study reptiles formed the dominant food item and accounted for the highest percentage of biomass consumed from autumn to spring, with rodents being a seasonally significant major food item. Arthropods were also consumed, but the biomass ingested was negligible. Statistically significant differences were noted across seasons in the prey items consumed, reflecting a flexible and opportunistic response to the scarcity of prey available. Our findings add to the data present on the basic natural history of G. polyosoma and can aid in its conservation in the Atacama Desert.     

New records of an invasive bumble bee in northern Chile: expansion of its range or new introduction events?

The Eurasian bumble bee Bombus terrestris Linnaeus has been used commercially for pollination of a large number of crop species worldwide. This species has become invasive in several countries where it has escaped into natural environments. This species has become naturalized in many zones of Chile and southern Argentina, and may potentially invade other regions and countries in South America. These naturalized populations of B. terrestris have been associated with rapid population declines of the native bee B. dahlbomii Guérin-Méneville. We report new records of the exotic bee B. terrestris in the Region de Arica y Parinacota in the far north of Chile, which includes portions of the Atacama Desert. We used species distribution models (SDMs) and multivariate analyses to evaluate whether these occurrences represent new escapes from managed colonies or natural dispersal of the species from its southern invaded range. These reports of B. terrestris indicate a northward expansion of this bee. In our analyses, these new areas of occurrences have environmental conditions similar to those observed in the species’ southern invaded range, and our SDMs predict that B. terrestris dispersal through the Atacama is possible, although not likely given the occasional flower blooming in that region of Chile. These new occurrences in northern Chile reflect a potential for future invasion into other regions of South America by B. terrestris. Future surveys in the area should be intensified to evaluate if viable populations of this invasive species may become established.     

Phylogenetic position of a remarkable new fideliine bee from northern Chile (Hymenoptera: Megachilidae)

Fideliine bees are an archaic group with a disjunct distribution mostly restricted to deserts of South America and South Africa. This group was previously thought to be more diverse in Africa than in South America, where only one genus (Neofidelia) comprising five species is known. Here we describe a species belonging to a second South American genus: Xenofidelia colorada Packer gen. et sp.n. , from northern Chile. The species is illustrated and its phylogenetic position within Megachilidae is assessed using morphological, molecular and combined data. The 214 character morphological matrix includes 55 new characters with an additional 16 hitherto unexplored for megachilid phylogeny. The molecular dataset is based upon seven nuclear gene sequences, totalling 6439 bp, many of which are published for the first time for particular megachilid taxa. In all analyses, Xenofidelia was found as sister to Neofidelia (endemic to Chile and Peru). It differs from that genus most notably in its short mouthparts, absence of a glossal rod, unmodified female metabasitarsus and an elongate and horizontal dorsal surface of the metapostnotum. Morphological and combined data support a monophyletic Fideliinae (excluding Pararhophites), while molecular data alone failed to recover fideliine monophyly. Dating analyses suggest that Xenofidelia and Neofidelia diverged 34.3–40.6 Ma, indicating that New World fideliines were probably present in arid habitats of South America during the Eocene. This divergence time predates both the main orogenic events that resulted in the formation of the Andean mountains and the origin of hyperarid conditions in the Atacama Desert; it also corresponds to a period prior to the origin of the summer rainfall area in the far north of Chile where the new genus is found. These results support the view that arid habitats have been present continuously in South America since the Eocene. This published work has been registered in ZooBank, http://zoobank.org/urn:lsid:zoobank.org:pub:EA69BB4A‐6F59‐4A15‐AB44‐2A8949E3CF8F .     

Phylogenetic relationships and ecological speciation in the mistletoe Tristerix (Loranthaceae): the influence of pollinators, dispersers, and hosts

Phylogenies can provide valuable information on biotic and abiotic factors associated with speciation. We examined species relationships in Tristerix (Loranthaceae), a genus of 11 species with an Andean distribution from Colombia to Chile. A previous classification divided Tristerix into subgenera Tristerix (two species) and Metastachys (nine species). We tested this classification by generating a molecular phylogeny of the genus using nuclear ribosomal DNA ITS and chloroplast atpB-rbcL intergenic spacer and trnL-F regions. All partitions generally gave congruent trees, thus a combined analysis was conducted. Tristerix was composed of a northern clade (six species) and a southern clade (four species). Tristerix verticillatus and T. penduliflorus (Metastachys) were strongly supported as members of the (southern) subgenus Tristerix clade. Speciation appears to be correlated with the emergence of matorral and cloud forest biomes and is driven by interactions with pollinators and seed dispersers. Tristerix aphyllus is sister to T. corymbosus of the matorral, not to neighboring temperate forest populations, thus rendering the latter species paraphyletic. This ecological speciation event may have occurred in sympatry. Tristerix provides excellent examples of how, during the orography of the Andes, many dynamic and interacting ecological factors have influenced their speciation.     

Evolutionary trends in the columnar cactus genus Eulychnia (Cactaceae) based on molecular phylogenetics,morphology, distribution,and habitat

Populations of the columnar cactus genus Eulychnia (Cactaceae) are an iconic sight in the Chilean Atacama Desert. The most recent taxonomic treatment of the genus suggested to accept up to seven taxa at species level based on morphological data. To date, species boundaries and infrageneric relationships in Eulychnia have not been investigated using a molecular approach. In this study, sequence data were generated for six chloroplast markers (rpl32-trnL, trnH-psbA, trnL-trnF, trnQ-rps16, trnS-trnG, and ycf1) for the seven species. Where possible, samples were collected from the south and north of the distribution range of widely distributed species, as well as plants from two morphologically distinct populations in the Atacama and Coquimbo Regions. Evolutionary trends of morphological characters were investigated using ancestral state reconstruction, and the habitat of the Chilean taxa was taken into account based on latitudinal and altitudinal distribution, precipitation regime, and vegetation zones. Two major clades were retrieved in the molecular phylogenetic hypotheses, a northern clade and a southern clade, which can easily be distinguished morphologically by differences in rib shape and type of the indumentum of the pericarpel and the hypanthium. The only Eulychnia taxon found outside Chile is most commonly accepted as Eulychnia iquiquensis subsp. ritteri. However, its isolated geographic distribution and the fact that this taxon is not most closely related to E. iquiquensis but was retrieved as sister to the rest of the northern clade in our molecular phylogenetic results support the recognition of E. ritteri at species level. Our results also provide some support for the two recently published species, E. chorosensis (previously placed in E. acida s.l.) and E. taltalensis (previously considered to be part of E. breviflora s.l.). The relationships in the southern clade need further study.     

Patterns of drought response in leaf-succulent shrubs of the coastal Atacama Desert in Northern Chile

Summary Despite the extrame aridity of the coastal Atacama Desert in northern Chile, sparse communities of leaf succulent shrubs and small cacti are regularly present. While most shrub species have small succulent leaves and accumulate high concentrations of salts in their tissues, the variable rooting patterns and mixed dominance of CAM and C₃ species indicates a significant divergence in adaptive strategies. All dominant shrubs are readily surviving extended drought, but some species are much better able than others to maintain active growth and flowering. Regular flowering may not be a prerequisite for shrub population maintenance since large piles of viable seeds are present under the canopies of many species.     

Microbial colonization of the salt deposits in the driest place of the Atacama Desert (Chile)

The Atacama Desert (Chile), one of the most arid places on Earth, shows hostile conditions for the development of epilithic microbial communities. In this study, we report the association of cyanobacteria (Chroococcidiopsis sp.) and bacteria belonging to Actinobacteria and Beta-Gammaproteobacteria and Firmicutes phyla inhabiting the near surface of salt (halite) deposits of the Salar Grande Basin, Atacama Desert (Chile). The halite deposits were investigated by using optical, confocal and field emission scanning electron microscopes, whereas culture-independent molecular techniques, 16S rDNA clone library, alongside RFLP analysis and 16S rRNA gene sequencing were applied to investigate the bacterial diversity. These microbial communities are an example of life that has adapted to extreme environmental conditions caused by dryness, high irradiation, and metal concentrations. Their adaptation is, therefore, important in the investigation of the environmental conditions that might be expected for life outside of Earth.