Taxonomic dissection based on molecular evidence of the Eriosycecurvispina complex (Cactaceae): identifying nine endemic species from Central Chile.

Chile's distinctive flora, geographical isolation, and complex topography collectively contribute to a notable endemic species diversity, particularly within central regions identified as critical areas for biodiversity conservation. The cactus genus Eriosyce, as currently circumscribed, encompasses seven sections, with Eriosycesect.Horridocatus presenting a notably complex species group. This study investigates the E.curvispina complex, a member of the Notocacteae tribe common in central Chile, by incorporating new populations and examining phylogenetic relationships using four plastid and one nuclear molecular marker. The phylogenetic analysis of sampled individuals identified nine independent lineages, each warranting recognition at the species rank. Despite minimal morphological differences among taxa, morphological characters were utilized to support and stabilize the DNA-based phylogenetic hypothesis. The results highlight the high taxonomic diversity in these cactus lineages and have implications for the classification of the E.curvispina complex, including new combinations and proposals of conservation status.

ResumenLa flora distintiva de Chile, su aislamiento geográfico y topografía compleja contribuyen colectivamente a una notable diversidad de especies endémicas, particularmente dentro de las regiones centrales identificadas como áreas críticas para la conservación de la biodiversidad. El género de cactus Eriosyce, tal como está circunscrito actualmente, abarca siete secciones, presentando Eriosycesect.Horridocatus un grupo de especies notablemente complejo. Este estudio investiga el complejo E.curvispina, un miembro de la tribu Notocacteae común en Chile central, incorporando nuevas poblaciones y examinando las relaciones filogenéticas utilizando cuatro marcadores moleculares del cloroplasto y uno nuclear. El análisis filogenético de las poblaciones muestreadas identificó nueve linajes independientes, cada uno mereciendo reconocimiento a nivel de especie. A pesar de las mínimas diferencias morfológicas entre los taxones, se utilizaron caracteres morfológicos para apoyar y estabilizar la filogenia basada en ADN. Los resultados resaltan la alta diversidad taxonómica en estos linajes de cactus y tienen implicaciones para la clasificación del complejo E.curvispina, incluyendo nuevas combinaciones y propuestas de estado de conservación.

Ecological and metabolic implications of the nurse effect of Maihueniopsis camachoi in the Atacama Desert.

Plant-plant positive interactions are key drivers of community structure. Yet, the underlying molecular mechanisms of facilitation processes remain unexplored. We investigated the 'nursing' effect of Maihueniopsis camachoi, a cactus that thrives in the Atacama Desert between c. 2800 and 3800 m above sea level. We hypothesised that an important protective factor is thermal amelioration of less cold-tolerant species with a corresponding impact on molecular phenotypes. To test this hypothesis, we compared plant cover and temperatures within the cactus foliage with open areas and modelled the effect of temperatures on plant distribution. We combined eco-metabolomics and machine learning to test the molecular consequences of this association. Multiple species benefited from the interaction with M. camachoi. A conspicuous example was the extended distribution of Atriplex imbricata to colder elevations in association with M. camachoi (400 m higher as compared to plants in open areas). Metabolomics identified 93 biochemical markers predicting the interaction status of A. imbricata with 79% accuracy, independently of year. These findings place M. camachoi as a key species in Atacama plant communities, driving local biodiversity with an impact on molecular phenotypes of nursed species. Our results support the stress-gradient hypothesis and provide pioneer insights into the metabolic consequences of facilitation.

Climatic Niche Dynamics of the Astereae Lineage and Haplopappus Species Distribution following Amphitropical Long-Distance Dispersal.

The tribe Astereae (Asteraceae) displays an American Amphitropical Disjunction. To understand the eco-evolutionary dynamics associated with a long-distance dispersal event and subsequent colonization of extratropical South America, we compared the climatic and geographic distributions of South American species with their closest North American relatives, focusing on the diverse South American Astereae genus, Haplopappus. Phylogenetic analysis revealed that two South American genera are closely related to seven North American genera. The climatic niche overlap (D = 0.5) between South and North America exhibits high stability (0.89), low expansion (0.12), and very low unfilling (0.04). The distribution of the North American species predicted the climatic and geographic space occupied by the South American species. In central Chile, Haplopappus showed a non-random latitudinal gradient in species richness, with Mediterranean climate variables mainly explaining the variation. Altitudinal patterns indicated peak richness at 600 m, declining at lower and higher elevations. These findings support climatic niche conservatism in shaping Haplopappus species distribution and diversity. Two major endemism zones were identified in central Chile and the southern region, with a transitional zone between Mediterranean and Temperate macro-bioclimates. Our results indicate strong niche conservatism following long-distance dispersal and slight niche expansion due to unique climatic variables in each hemisphere.

Independent Evolutionary Lineages in a Globular Cactus Species Complex Reveals Hidden Diversity in a Central Chile Biodiversity Hotspot.

Unraveling the processes involved in the origin of a substantial fraction of biodiversity can be a particularly difficult task in groups of similar, and often convergent, morphologies. The genus Eriosyce (Cactaceae) might present a greater specific diversity since much of its species richness might be hidden in morphological species complexes. The aim of this study was to investigate species delimitation using the molecular data of the globose cacti "E. curvispina", which harbor several populations of unclear evolutionary relationships. We ran phylogenetic inferences on 87 taxa of Eriosyce, including nine E. curvispina populations, and by analyzing three plastid noncoding introns, one plastid and one nuclear gene. Additionally, we developed 12 new pairs of nuclear microsatellites to evaluate the population-level genetic structure. We identified four groups that originated in independent cladogenetic events occurring at different temporal depths; these groups presented high genetic diversity, and their populations were genetically structured. These results suggest a complex evolutionary history in the origin of globular cacti, with independent speciation events occurring at different time spans. This cryptic richness is underestimated in the Mediterranean flora of central Chile, and thus unique evolutionary diversity could be overlooked in conservation and management actions.

Flowering Phenology Adjustment and Flower Longevity in a South American Alpine Species.

Delayed flowering due to later snowmelt and colder temperatures at higher elevations in the alpine are expected to lead to flowering phenological adjustment to prevent decoupling of peak flowering from the warmest time of the year, thereby favoring pollination. However, even if flowering is brought forward in the season at higher elevations, an elevational temperature gap is likely to remain between the high- and low-elevation populations of a species at the time these reach peak flowering on account of the atmospheric reduction in temperature with increasing elevation. The negative effect of this temperature gap on pollination could be compensated by plastically-prolonged flower life spans at higher elevations, increasing the probability of pollination. In a tightly temperature-controlled study, the flowering phenology adjustment and flower longevity compensation hypotheses were investigated in an alpine species in the Andes of central Chile. The snow free period varied from 7 to 8.2 months over 810 m elevation. Temperatures were suitable for growth on 82-98% of the snow free days. Flowering onset was temporally displaced at the rate of 4.6 d per 100 m increase in elevation and flowering was more synchronous at higher elevations. Flowering phenology was adjusted over elevation. The latter was manifest in thermal sums tending to decrease with elevation for population flowering onset, 50% flowering, and peak flowering when the lower thermal limit for growth (TBASE) was held constant over elevation. For TBASE graded over elevation so as to reflect the growing season temperature decline, thermal sums did not vary with elevation, opening the door to a possible elevational decline in the thermal temperature threshold for growth. Potential flower longevity was reduced by passive warming and was more prolonged in natural populations when temperatures were lower, indicating a plastic trait. Pollination rates, as evaluated with the Relative Pollination Rate index (RPR), when weighted for differences in floral abundance over the flowering season, declined with elevation as did fruit set. Contrary to expectation, the life-spans of flowers at higher elevations were not more prolonged and failed to compensate for the elevational decrease in pollination rates. Although strong evidence for phenological adjustment was forthcoming, flower longevity compensation did not occur over Oxalis squamata´s elevational range. Thus, flower longevity compensation is not applicable in all alpine species. Comparison with work conducted several decades ago on the same species in the same area provides valuable clues regarding the effects of climate change on flowering phenology and fitness in the central Chilean alpine where temperatures have been increasing and winter snow accumulation has been declining.

Niches and climate-change refugia in hundreds of species from one of the most arid places on Earth.

BACKGROUND AND AIMS: Global climate change is a major threat to biodiversity worldwide. Several arid areas might expand in the future, but it is not clear if this change would be positive or negative for arid-adapted lineages. Here, we explore whether climatic niche properties are involved in the configuration of climate refugia and thus in future species trends. METHODS: To estimate putative climate refugia and potential expansion areas, we used maximum entropy models and four climate-change models to generate current and future potential distributions of 142 plant species endemic to the Atacama and mediterranean Chilean ecosystems. We assessed the relationship between the similarity and breadth of thermal and precipitation niches with the size of climate refugia and areas of potential expansions. KEY RESULTS: We found a positive relationship between breadth and similarity for thermal niche with the size of climate refugia, but only niche similarity of the thermal niche was positively related with the size of expansion areas. Although all lineages would reduce their distributions in the future, few species are predicted to be at risk of extinction in their current distribution, and all of them presented potential expansion areas. CONCLUSION: Species with a broad niche and niche dissimilarity will have larger refugia, and species with niche dissimilarity will have larger expansion areas. In addition, our prediction for arid lineages shows that these species will be moderately affected by climate change.

Bees may drive the reproduction of four sympatric cacti in a vanishing coastal mediterranean-type ecosystem.

BACKGROUND: Sympatric congeneric plants might share pollinators, or each species might avoid competition by evolving specialized traits that generate partitions in pollinator assemblages. In both cases, pollen limitation (a decrease in the quality and quantity of compatible reproductive pollen) can occur, driving the plant mating system to autogamy as a mechanism of reproductive assurance. We assessed the relationships between pollinator assemblages and mating systems in a group of sympatric congeneric plants. We attempted to answer the following questions: (i) How similar are pollinator assemblages among sympatric cactus species? (ii) Which mating systems do sympatric cactus species use? METHODS: We studied sympatric Eriosyce taxa that inhabit a threatened coastal strip in a mediterranean-type ecosystem in central Chile. We performed field observations on four taxa and characterized pollinators during the years 2016 and 2017. We estimated differences in the pollinator assemblages using the Bray-Curtis index. To elucidate the mating systems, we conducted hand-pollination experiments using three treatments: manual cross-pollination, automatic self-pollination, and control (unmanipulated individuals). We tested differences in seed production for statistical significance using Kruskal-Wallis analysis. RESULTS: Eriosyce subgibbosa showed a distinctive pollinator assemblage among the sympatric species that we studied (similarity ranged from 0% to 8%); it was visited by small bees and was the only species that was visited by the giant hummingbird Patagona gigas. Pollinator assemblages were similar between E. chilensis (year 2016 = 4 species; 2017 = 8) and E. chilensis var. albidiflora (2016 = 7; 2017 = 4); however, those of E. curvispina var. mutabilis (2016 = 7; 2017 = 6) were less similar to those of the aforementioned species. E. curvispina var. mutabilis showed the highest interannual variation in its pollinator assemblage (18% similarity). Reproduction in E. subgibbosa largely depends on pollinators, although it showed some degree of autogamy. Autonomous pollination was unfeasible in E. chilensis, which depended on flower visitors for its reproductive success. Both E. chilensis var. albidiflora and E. curvispina var. mutabilis showed some degree of autogamy. DISCUSSION: We observed differences in pollinator assemblages between E. subgibbosa and the remaining Eriosyce taxa, which depend on hymenopterans for pollen transfer. Pollinator assemblages showed considerable interannual variation, especially those of E. subgibbosa (ornithophilous syndrome) and E. curvispina var. mutabilis (melitophilous syndrome). Autogamous reproduction in these taxa may act as a reproductive assurance mechanism when pollinator availability is unpredictable. Our study contributes to improving our understanding of the reproductive systems of ecological interactions between threatened species in a Chilean mediterranean-type ecosystem.

Phylogenetic Relationships and Evolutionary Trends in the Cactus Family.

Members of the cactus family are keystone species of arid and semiarid biomes in the Americas, as they provide shelter and resources to support other members of ecosystems. Extraordinary examples are the several species of flies of the genus Drosophila that lay eggs and feed in their rotting stems, which provide a model system for studying evolutionary processes. Although there is significant progress in understanding the evolution of Drosophila species, there are gaps in our knowledge about the cactus lineages hosting them. Here, we review the current knowledge about the evolution of Cactaceae, focusing on phylogenetic relationships and trends revealed by the study of DNA sequence data. During the last several decades, the availability of molecular phylogenies has considerably increased our understanding of the relationships, biogeography, and evolution of traits in the family. Remarkably, although succulent cacti have very low growth rates and long generation times, they underwent some of the fastest diversifications observed in the plant kingdom, possibly fostered by strong ecological interactions. We have a better understanding of the reproductive biology, population structure and speciation mechanisms in different clades. The recent publication of complete genomes for some species has revealed the importance of phenomena such as incomplete lineage sorting. Hybridization and polyploidization are common in the family, and have been studied using a variety of phylogenetic methods. We discuss potential future avenues for research in Cactaceae, emphasizing the need of a concerted effort among scientists in the Americas, together with the analyses of data from novel sequencing techniques.

Evaluating methods for phylogenomic analyses, and a new phylogeny for a major frog clade (Hyloidea) based on 2214 loci.

Phylogenomic approaches offer a wealth of data, but a bewildering diversity of methodological choices. These choices can strongly affect the resulting topologies. Here, we explore two controversial approaches (binning genes into "supergenes" and inclusion of only rapidly evolving sites), using new data from hyloid frogs. Hyloid frogs encompass ∼53% of frog species, including true toads (Bufonidae), glassfrogs (Centrolenidae), poison frogs (Dendrobatidae), and treefrogs (Hylidae). Many hyloid families are well-established, but relationships among these families have remained difficult to resolve. We generated a dataset of ultraconserved elements (UCEs) for 50 ingroup species, including 18 of 19 hyloid families and up to 2214 loci spanning >800,000 aligned base pairs. We evaluated these two general approaches (binning, rapid sites only) based primarily on their ability to recover and strongly support well-established clades. Data were analyzed using concatenated likelihood and coalescent species-tree methods (NJst, ASTRAL). Binning strongly affected inferred relationships, whereas use of only rapidly evolving sites did not (indicating ∼87% of the data contributed little information). The optimal approaches for maximizing recovery and support of well-established clades were concatenated likelihood analysis and the use of a limited number of naive bins (statistical binning gave more problematic results). These two optimal approaches converged on similar relationships among hyloid families, and resolved them with generally strong support. The relationships found were very different from most previous estimates of hyloid phylogeny, and a new classification is proposed. The new phylogeny also suggests an intriguing biogeographical scenario, in which hyloids originated in southern South America before radiating throughout the world.

An integrative approach to understanding the evolution and diversity of Copiapoa (Cactaceae), a threatened endemic Chilean genus from the Atacama Desert.

PREMISE OF THE STUDY: Species of the endemic Chilean cactus genus Copiapoa have cylindrical or (sub)globose stems that are solitary or form (large) clusters and typically yellow flowers. Many species are threatened with extinction. Despite being icons of the Atacama Desert and well loved by cactus enthusiasts, the evolution and diversity of Copiapoa has not yet been studied using a molecular approach. METHODS: Sequence data of three plastid DNA markers (rpl32-trnL, trnH-psbA, ycf1) of 39 Copiapoa taxa were analyzed using maximum likelihood and Bayesian inference approaches. Species distributions were modeled based on geo-referenced localities and climatic data. Evolution of character states of four characters (root morphology, stem branching, stem shape, and stem diameter) as well as ancestral areas were reconstructed using a Bayesian and maximum likelihood framework, respectively. KEY RESULTS: Clades of species are revealed. Though 32 morphologically defined species can be recognized, genetic diversity between some species and infraspecific taxa is too low to delimit their boundaries using plastid DNA markers. Recovered relationships are often supported by morphological and biogeographical patterns. The origin of Copiapoa likely lies between southern Peru and the extreme north of Chile. The Copiapó Valley limited colonization between two biogeographical areas. CONCLUSIONS: Copiapoa is here defined to include 32 species and five heterotypic subspecies. Thirty species are classified into four sections and two subsections, while two species remain unplaced. A better understanding of evolution and diversity of Copiapoa will allow allocating conservation resources to the most threatened lineages and focusing conservation action on real biodiversity.

High proportion of cactus species threatened with extinction.

A high proportion of plant species is predicted to be threatened with extinction in the near future. However, the threat status of only a small number has been evaluated compared with key animal groups, rendering the magnitude and nature of the risks plants face unclear. Here we report the results of a global species assessment for the largest plant taxon evaluated to date under the International Union for Conservation of Nature (IUCN) Red List Categories and Criteria, the iconic Cactaceae (cacti). We show that cacti are among the most threatened taxonomic groups assessed to date, with 31% of the 1,478 evaluated species threatened, demonstrating the high anthropogenic pressures on biodiversity in arid lands. The distribution of threatened species and the predominant threatening processes and drivers are different to those described for other taxa. The most significant threat processes comprise land conversion to agriculture and aquaculture, collection as biological resources, and residential and commercial development. The dominant drivers of extinction risk are the unscrupulous collection of live plants and seeds for horticultural trade and private ornamental collections, smallholder livestock ranching and smallholder annual agriculture. Our findings demonstrate that global species assessments are readily achievable for major groups of plants with relatively moderate resources, and highlight different conservation priorities and actions to those derived from species assessments of key animal groups.

Climatic niche conservatism and biogeographical non-equilibrium in Eschscholzia californica (Papaveraceae), an invasive plant in the Chilean Mediterranean region.

Species climate requirements are useful for predicting their geographic distribution. It is often assumed that the niche requirements for invasive plants are conserved during invasion, especially when the invaded regions share similar climate conditions. California and central Chile have a remarkable degree of convergence in their vegetation structure, and a similar Mediterranean climate. Such similarities make these geographic areas an interesting natural experiment for testing climatic niche dynamics and the equilibrium of invasive species in a new environment. We tested to see if the climatic niche of Eschscholzia californica is conserved in the invaded range (central Chile), and we assessed whether the invasion process has reached a biogeographical equilibrium, i.e., occupy all the suitable geographic locations that have suitable conditions under native niche requirements. We compared the climatic niche in the native and invaded ranges as well as the projected potential geographic distribution in the invaded range. In order to compare climatic niches, we conducted a Principal Component Analysis (PCA) and Species Distribution Models (SDMs), to estimate E. californica's potential geographic distribution. We also used SDMs to predict altitudinal distribution limits in central Chile. Our results indicated that the climatic niche occupied by E. californica in the invaded range is firmly conserved, occupying a subset of the native climatic niche but leaving a substantial fraction of it unfilled. Comparisons of projected SDMs for central Chile indicate a similarity, yet the projection from native range predicted a larger geographic distribution in central Chile compared to the prediction of the model constructed for central Chile. The projected niche occupancy profile from California predicted a higher mean elevation than that projected from central Chile. We concluded that the invasion process of E. californica in central Chile is consistent with climatic niche conservatism but there is potential for further expansion in Chile.

Evolutionary lag times and recent origin of the biota of an ancient desert (Atacama-Sechura).

The assembly of regional biotas and organismal responses to anthropogenic climate change both depend on the capacity of organisms to adapt to novel ecological conditions. Here we demonstrate the concept of evolutionary lag time, the time between when a climatic regime or habitat develops in a region and when it is colonized by a given clade. We analyzed the time of colonization of four clades (three plant genera and one lizard genus) into the Atacama-Sechura Desert of South America, one of Earth's driest and oldest deserts. We reconstructed time-calibrated phylogenies for each clade and analyzed the timing of shifts in climatic distributions and biogeography and compared these estimates to independent geological estimates of the time of origin of these deserts. Chaetanthera and Malesherbia (plants) and Liolaemus (animal) invaded arid regions of the Atacama-Sechura Desert in the last 10 million years, some 20 million years after the initial onset of aridity in the region. There are also major lag times between when these clades colonized the region and when they invaded arid habitats within the region (typically 4-14 million years). Similarly, hyperarid climates developed ∼8 million years ago, but the most diverse plant clade in these habitats (Nolana) only colonized them ∼2 million years ago. Similar evolutionary lag times may occur in other organisms and habitats, but these results are important in suggesting that many lineages may require very long time scales to adapt to modern desertification and climatic change.