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Under the recently adopted Kunming-Montreal Global Biodiversity Framework, 196 Parties committed to reporting the status of genetic diversity for all species. To facilitate reporting, three genetic diversity indicators were developed, two of which focus on processes contributing to genetic diversity conservation: maintaining genetically distinct populations and ensuring populations are large enough to maintain genetic diversity. The major advantage of these indicators is that they can be estimated with or without DNA-based data. However, demonstrating their feasibility requires addressing the methodological challenges of using data gathered from diverse sources, across diverse taxonomic groups, and for countries of varying socio-economic status and biodiversity levels. Here, we assess the genetic indicators for 919 taxa, representing 5271 populations across nine countries, including megadiverse countries and developing economies. Eighty-three percent of the taxa assessed had data available to calculate at least one indicator. Our results show that although the majority of species maintain most populations, 58% of species have populations too small to maintain genetic diversity. Moreover, genetic indicator values suggest that IUCN Red List status and other initiatives fail to assess genetic status, highlighting the critical importance of genetic indicators.
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Biodiversidad , Conservación de los Recursos Naturales , Variación Genética , AnimalesRESUMEN
Plant-hummingbird interactions are considered a classic example of coevolution, a process in which mutually dependent species influence each other's evolution. Plants depend on hummingbirds for pollination, whereas hummingbirds rely on nectar for food. As a step towards understanding coevolution, this review focuses on the macroevolutionary consequences of plant-hummingbird interactions, a relatively underexplored area in the current literature. We synthesize prior studies, illustrating the origins and dynamics of hummingbird pollination across different angiosperm clades previously pollinated by insects (mostly bees), bats, and passerine birds. In some cases, the crown age of hummingbirds pre-dates the plants they pollinate. In other cases, plant groups transitioned to hummingbird pollination early in the establishment of this bird group in the Americas, with the build-up of both diversities coinciding temporally, and hence suggesting co-diversification. Determining what triggers shifts to and away from hummingbird pollination remains a major open challenge. The impact of hummingbirds on plant diversification is complex, with many tropical plant lineages experiencing increased diversification after acquiring flowers that attract hummingbirds, and others experiencing no change or even a decrease in diversification rates. This mixed evidence suggests that other extrinsic or intrinsic factors, such as local climate and isolation, are important covariables driving the diversification of plants adapted to hummingbird pollination. To guide future studies, we discuss the mechanisms and contexts under which hummingbirds, as a clade and as individual species (e.g. traits, foraging behaviour, degree of specialization), could influence plant evolution. We conclude by commenting on how macroevolutionary signals of the mutualism could relate to coevolution, highlighting the unbalanced focus on the plant side of the interaction, and advocating for the use of species-level interaction data in macroevolutionary studies.
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Psittacanthus schiedeanus (Cham. & Schltdl.) G.Don., 1834, is a mistletoe species in the Loranthaceae, characteristic of the canopy in cloud forest edges and widely distributed in northern Mesoamerica. Here, we report the complete chloroplast genome sequence of P. schiedeanus, the first for a species in the Psittacantheae tribe. The circularized quadripartite structure of the P. schiedeanus chloroplast genome was 122,586 bp in length and included a large single-copy region of 72,507 bp and two inverted repeats of 21,283 bp separated by a small single-copy region of 7,513 bp. The genome contained 112 genes, of which 96 are unique, including 65 protein-coding genes, 27 transfer RNA, and four ribosomal RNA. The overall GC content in the plastome of P. schiedeanus is 36.9%. Based on 43 published complete chloroplast genome sequences for species in the families Loranthaceae and Santalaceae (Santalales), the maximum-likelihood phylogenetic tree with high-support bootstrap values indicated that P. schiedeanus in the Psittacantheae tribe is sister to the tribe Lorantheae. The chloroplast genome provided in this study represents a valuable resource for genetic, phylogenetic and conservation studies of Psittacanthus species, and an important advance for unraveling the evolutionary history of these hemiparasitic plants.
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Research Highlight: Maglianesi, M. A., Maruyama, P. K., Temeles, E. J., Schleuning, M., Zanata, T. B., Sazima, M., Gutiérrez-Zamora, A., Marín-Gómez, O. H., Rosero-Lasprilla, L., Ramírez-Burbano, M. B., Ruffini, A. E., Salamanca-Reyes, J. R., Sazima, I., Nuñez-Rosas, L. E., Arizmendi, M. C., Rahbek, C., & Dalsgaard, B. (2022). Behavioural and morphological traits influence sex-specific floral resource use by hummingbirds across the Americas. Journal of Animal Ecology, 00: 00-00. https://doi.org/10.1111/1365-2656.13746. In their paper on intersexual differences in niche breadth and niche overlap in floral resource use in hummingbird communities, Maglianesi et al. compiled data of plant-hummingbird interactions based on pollen loads, and territoriality and morphological traits for 31 hummingbird species, and investigated whether patterns of resource use by females and males were related to sexual dimorphism and foraging behaviour. While accounting for evolutionary relatedness among species, the authors found a high level of resource partitioning between sexes (broader and more dissimilar floral niche breadth in females) and the sex-specific resource use by hummingbird species was related to territoriality and morphological traits; niche overlap between sexes was greater for territorial than non-territorial species, and lower for species with greater sexual dimorphism in bill curvature. This paper addresses two very timely issues, on the one hand on resource partitioning by sex to reduce intersexual competition in hummingbirds, and on the other hand highlight the much needed information on foraging ecology of female hummingbirds for better understanding of intersexual variation in shaping coexistence and species diversity in hummingbird communities and the interactions between plants and their hummingbird pollinators.
Investigación Destacada: Maglianesi, M. A., Maruyama, P. K., Temeles, E. J., Schleuning, M., Zanata, T. B., Sazima, M., Gutiérrez-Zamora, A., Marín-Gómez, O. H., Rosero-Lasprilla, L., Ramírez-Burbano, M. B., Ruffini, A. E., Salamanca-Reyes, J. R., Sazima, I., Nuñez-Rosas, L. E., Arizmendi, M. C., Rahbek, C., & Dalsgaard, B. (2022). Behavioural and morphological traits influence sex-specific floral resource use by hummingbirds across the Americas. Journal of Animal Ecology, 00: 00-00. https://doi.org/10.1111/1365-2656.13746. En su artículo sobre las diferencias intersexuales en la amplitud de nicho y la superposición de nicho en el uso de recursos florales en las comunidades de colibríes, Maglianesi et al. recopilaron datos de interacciones planta-colibrí basados en cargas de polen, y de territorialidad y rasgos morfológicos para 31 especies de colibríes, e investigaron si los patrones de uso de recursos por parte de hembras y machos estaban relacionados con el dimorfismo sexual y la conducta de forrajeo. Al tener en cuenta la relación evolutiva entre las especies, los autores encontraron un alto nivel de partición de recursos entre sexos (amplitud de nicho floral más amplio y diferente en las hembras) y el uso de recursos específico del sexo por parte de las especies de colibríes estaba relacionado con la territorialidad y los rasgos morfológicos; la superposición de nicho entre sexos fue mayor para las especies territoriales que para las no territoriales, y menor para las especies con mayor dimorfismo sexual en la curvatura del pico. Este artículo aborda dos temas muy oportunos, por un lado, la partición de recursos por sexo para reducir la competencia intersexual en los colibríes y, por otro lado, destaca la necesidad de información sobre la ecología de alimentación de las hembras de los colibríes para una mejor comprensión de la variación intersexual en la conformación de la coexistencia y diversidad de especies en las comunidades de colibríes y las interacciones entre las plantas y sus colibríes polinizadores.
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Aves , Flores , Animales , Flores/anatomía & histología , Ecología , Polen , Evolución Biológica , PolinizaciónRESUMEN
The mistletoe Psittacanthus schiedeanus, a keystone species in interaction networks between plants, pollinators, and seed dispersers, infects a wide range of native and non-native tree species of commercial interest. Here, using RNA-seq methodology we assembled the whole circularized quadripartite structure of P. schiedeanus chloroplast genome and described changes in the gene expression of the nuclear genomes across time of experimentally inoculated seeds. Of the 140,467 assembled and annotated uniGenes, 2,000 were identified as differentially expressed (DEGs) and were classified in six distinct clusters according to their expression profiles. DEGs were also classified in enriched functional categories related to synthesis, signaling, homoeostasis, and response to auxin and jasmonic acid. Since many orthologs are involved in lateral or adventitious root formation in other plant species, we propose that in P. schiedeanus (and perhaps in other rootless mistletoe species), these genes participate in haustorium formation by complex regulatory networks here described. Lastly, and according to the structural similarities of P. schiedeanus enzymes with those that are involved in host cell wall degradation in fungi, we suggest that a similar enzymatic arsenal is secreted extracellularly and used by mistletoes species to easily parasitize and break through tissues of the host.
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BACKGROUND: Plant-pollinator mutualistic networks show non-random structural properties that promote species coexistence. However, these networks show high variability in the interacting species and their connections. Mismatch between plant and pollinator attributes can prevent interactions, while trait matching can enable exclusive access, promoting pollinators' niche partitioning and, ultimately, modularity. Thus, plants belonging to specialized modules should integrate their floral traits to optimize the pollination function. Herein, we aimed to analyze the biological processes involved in the structuring of plant-hummingbird networks by linking network morphological constraints, specialization, modularity and phenotypic floral integration. METHODS: We investigated the understory plant-hummingbird network of two adjacent habitats in the Lacandona rainforest of Mexico, one characterized by lowland rainforest and the other by savanna-like vegetation. We performed monthly censuses to record plant-hummingbird interactions for 2 years (2018-2020). We also took hummingbird bill measurements and floral and nectar measurements. We summarized the interactions in a bipartite matrix and estimated three network descriptors: connectance, complementary specialization (H2'), and nestedness. We also analyzed the modularity and average phenotypic floral integration index of each module. RESULTS: Both habitats showed strong differences in the plant assemblage and network dynamics but were interconnected by the same four hummingbird species, two Hermits and two Emeralds, forming a single network of interaction. The whole network showed low levels of connectance (0.35) and high specialization (H2' = 0.87). Flower morphologies ranged from generalized to specialized, but trait matching was an important network structurer. Modularity was associated with morphological specialization. The Hermits Phaethornis longirostris and P. striigularis each formed a module by themselves, and a third module was formed by the less-specialized Emeralds: Chlorestes candida and Amazilia tzacatl. The floral integration values were higher in specialized modules but not significantly higher than that formed by generalist species. CONCLUSIONS: Our findings suggest that biological processes derived from both trait matching and "forbidden" links, or nonmatched morphological attributes, might be important network drivers in tropical plant-hummingbird systems while morphological specialization plays a minor role in the phenotypic floral integration. The broad variety of corolla and bill shapes promoted niche partitioning, resulting in the modular organization of the assemblage according to morphological specialization. However, more research adding larger datasets of both the number of modules and pollination networks for a wider region is needed to conclude whether phenotypic floral integration increases with morphological specialization in plant-hummingbird systems.
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PREMISE: Mistletoes parasitize many hardwood and softwood tree species; however, they play key roles in forest ecosystems. Adult individuals of Psittacanthus schiedeanus take up water and xylem nutrients from both deciduous and evergreen host trees, suggesting the ability to modify its physiology according to the availability of host resources. Yet, there is little information regarding the effects of mistletoes on their host trees from the eophyll stage to reproductive phases of the parasite. METHODS: Taking advantage of the fact that P. schiedeanus can reach sexual maturity in 1 year, we investigated its physiological performance during development on deciduous (Liquidambar styraciflua) and evergreen (Quercus germana) host trees in a cloud forest in eastern Mexico. Variables related to chlorophyll fluorescence, carbon assimilation, photosynthetic pigments, and nitrogen, phosphorus, and carbon contents of the parasite and non-infected and infected hosts were analyzed in a nursery experiment. RESULTS: Mistletoe had lower water-use efficiency and higher transpiration rates than the host species did. Despite the fact that P. schiedeanus obtained resources from species with differing phenology and resource availability, the parasite steadily improved its CO2 assimilation, electron transport rate, and nutrient content from seedling establishment to adult life stages. Mistletoe decreased the photosynthetic reactions of carbon metabolism in the deciduous host, photosynthetic light reactions in the evergreen host, and nutritional status of both host species, mostly in the evergreen host. CONCLUSIONS: The hypothesis that mistletoes adjust their physiology according to the availability of host resources could extend to the early growth of the parasite.
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Muérdago , Árboles , Ecosistema , Humanos , México , Hojas de la PlantaRESUMEN
Differential visitation of pollinators due to divergent floral traits can lead to reproductive isolation via assortative pollen flow, which may ultimately be a driving force in plant speciation, particularly in areas of overlap. We evaluate the effects of pollinator behavioral responses to variation of intraspecific floral color and nectar rewards, on reproductive isolation between two hybrid flower color morphs (fuchsia and blue) and their parental species Penstemon roseus and P. gentianoides with a mixed-pollination system. We show that pollinators (bumblebees and hummingbirds) exhibit different behavioral responses to fuchsia and blue morphs, which could result from differential attraction or deterrence. In addition to differences in color (spectral reflectance), we found that plants with fuchsia flowers produced more and larger flowers, produced more nectar and were more visited by pollinators than those with blue flowers. These differences influenced the foraging behavior and effectiveness as pollinators of both bumblebees and hummingbirds, which contributed to reproductive isolation between the two hybrid flower color morphs and parental species. This study demonstrates how differentiation of pollination traits promotes the formation of hybrid zones leading to pollinator shifts and reproductive isolation. While phenotypic traits of fuchsia and red flowers might encourage more efficient hummingbird pollination in a mixed-pollination system, the costs of bumblebee pollination on plant reproduction could be the drivers for the repeated shifts from bumblebee- to hummingbird-mediated pollination.
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Abejas/fisiología , Flores/fisiología , Penstemon/clasificación , Penstemon/fisiología , Polinización , Aislamiento Reproductivo , Simpatría/fisiología , Animales , Abejas/anatomía & histología , Evolución Biológica , Color , Penstemon/anatomía & histología , Fenotipo , PolenRESUMEN
The biogeographical history of Mesoamerican cloud forests is complex, encompassing a diverse and heterogeneous mixture of species with temperate and tropical origins. The dynamic geological landscape and climate change from the Miocene to the Pleistocene affected the distributions and composition of cloud forests in the region, and contributed to divergence events at different time scales. We assessed genetic variation of 29 populations of P. matudae, and closely related P. guatemalensis and P. oleifolius (Podocarpaceae) by sequencing 255 samples of the psbA-trnH and trnL-F intergenic spacer regions across the species ranges. We conducted phylogenetic, population and spatial genetic analyses as well as divergence time estimation and ecological niche modelling (ENM) to test the generality of demographic and genetic scenarios for cloud forest-adapted species. The results revealed genetic differentiation among species, with some individuals of P. oleifolius and P. guatemalensis placed in the P. matudae group and some P. oleifolius in the P. guatemalensis group. Predictions of ENMs under past climatic conditions and a strong signal of spatial expansion suggest that the highland P. matudae and P. oleifolius populations experienced expansions into lower elevation during the Last Glacial Maximum (LGM). Contrary to predictions by the two precipitation models and elevational ups and downs for cloud forest taxa during the LGM, genetic differentiation and predicted distribution of suitable habitat support the hypotheses that P. matudae and P. oleifolius remained in situ during the LGM primarily within the current fragmented distribution of the cloud forest and spread into the lowlands during the LGM, whereas the distribution of suitable habitat for P. guatemalensis had no major changes upwards from the Last Inter Glacial (LIG) to current conditions.
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Variación Genética , Tracheophyta/genética , Américas , Ecosistema , Genética de Población , Haplotipos/genética , Filogenia , Filogeografía , Análisis de Componente Principal , Factores de TiempoRESUMEN
Mutualistic interactions are powerful drivers of biodiversity on Earth that can be represented as complex interaction networks that vary in connection pattern and intensity. One of the most fascinating mutualisms is the interaction between hummingbirds and the plants they visit. We conducted an exhaustive search for articles, theses, reports, and personal communications with researchers (unpublished data) documenting hummingbird visits to flowers of nectar-rewarding plants. Based on information gathered from 4532 interactions between 292 hummingbird species and 1287 plant species, we built an interaction network between nine hummingbird clades and 100 plant families used by hummingbirds as nectar resources at a continental scale. We explored the network architecture, including phylogenetic, morphological, biogeographical, and distributional information. As expected, the network between hummingbirds and their nectar plants was heterogeneous and nested, but not modular. When we incorporated ecological and historical information in the network nodes, we found a generalization gradient in hummingbird morphology and interaction patterns. The hummingbird clades that most recently diversified in North America acted as generalist nodes and visited flowers with ornithophilous, intermediate and non-ornithophilous morphologies, connecting a high diversity of plant families. This pattern was favored by intermediate morphologies (bill, wing, and body size) and by the low niche conservatism in these clades compared to the oldest clades that diversified in South America. Our work is the first effort exploring the hummingbird-plant mutualistic network at a continental scale using hummingbird clades and plant families as nodes, offering an alternative approach to exploring the ecological and evolutionary factors that explain plant-animal interactions at a large scale.
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Aves/fisiología , Conducta Alimentaria/fisiología , Néctar de las Plantas/fisiología , Fenómenos Fisiológicos de las Plantas , Animales , Biodiversidad , Tamaño Corporal , Flores/fisiología , Polinización/fisiología , Estaciones del Año , América del Sur , Especialización , Simbiosis/genéticaRESUMEN
The host dependence of mistletoes suggests that they track the distributions of their hosts. However, the factors that determine the geographic distribution of mistletoes are not well understood. In this study, the phylogeography of Psittacanthus sonorae was reconstructed by sequencing one nuclear (ITS) and two plastid (trnL-F and atpB-rbcL) regions of 148 plants from populations separated by the Sea of Cortez. Divergence time and gene flow were estimated to gain insight into the historical demography and geographic structuring of genetic variation. We also described and mapped the spatial distribution of suitable habitat occupied by P. sonorae and its most common host Bursera microphylla in the Sonoran Desert, along with their responses to Quaternary climate fluctuations using environmental data and ecological niche modeling (ENM). We detected environmental and genetic differentiation between the peninsular and continental P. sonorae populations. Population divergence occurred during the Pleistocene, around the time of the Last Glacial Maximum. No signals of population growth were detected, with net gene flow moving from the continent to the peninsula. ENM models indicate decoupled responses by the mistletoe and its main host to past climate changes. For the Last Interglacial to the present, most models produce only partial areas of overlap on both the peninsula and the continent. Our results support a scenario of Late-Pleistocene isolation and divergence with asymmetrical gene flow between peninsular and continental P. sonorae populations. Continental populations migrated to the peninsula and the spatial isolation probably produced genetic differentiation under different environmental conditions.
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Loranthaceae/clasificación , Loranthaceae/genética , Filogenia , Filogeografía , Evolución Biológica , Clima Desértico , Ambiente , Variación Genética , Genética de Población , Geografía , Haplotipos , Modelos TeóricosRESUMEN
The pollination syndrome concept implies that flowers evolved with particular sets of characteristics, such as colors, shapes, orientations, and rewards, as a means of attracting pollinators. However, these traits may have also evolved to deter unwanted visitors. The North American genus Penstemon exhibits a great floral diversity that is mainly associated with bumblebee and hummingbird pollination. Evolutionary shifts from insect pollination to hummingbird pollination have occurred in Penstemon repeatedly, but some species maintain mixed-pollination systems and intermediate floral traits between bee- and hummingbird-pollination modes. The apparently intermediate floral traits of species with mixed-pollination systems might be potentially acting to deter bumblebee foragers. Then, bird-flower traits might be selected with increased hummingbird visitation over evolutionary time might, resulting in specialization to and the evolution of floral traits present in hummingbird-pollinated species. Here, we modified bee-pollination floral traits in Penstemon gentianoides with a mixed pollination system, to resemble hummingbird-pollination traits, and measured the effects of trait modification on bumblebee foraging behavior and plant female reproductive fitness. Our results showed that reduction in the width of the corolla tube and the absence of the corolla lip negatively affects bumblebee visitation and their efficiency as pollinators, and that the synergistic interaction of both traits enhanced the "anti-bee" effect. We conclude that acquisition of floral traits that resemble those of hummingbird-pollination enables Penstemon plant species to deter bumblebee visits.
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Abejas/fisiología , Aves/fisiología , Flores/fisiología , Penstemon/fisiología , Polinización/fisiología , Animales , Biodiversidad , Evolución Biológica , Flores/anatomía & histología , Penstemon/anatomía & histologíaRESUMEN
Recent studies on ecological networks have quantified the contribution of ecological, historical, and evolutionary factors on the structure of local communities of interacting species. However, the influence of species' biogeographical traits, such as migratory habits or phylogeographical history, on ecological networks is poorly understood. Meta-networks, i.e., networks that cover large spatial extensions and include species not co-occurring locally, enable us to investigate mechanisms that operate at larger spatial scales such as migratory patterns or phylogeographical distributions, as well as indirect relationships among species through shared partners. Using a meta-network of hummingbird-plant interaction across Mexico, we illustrate the usefulness of this approach by investigating (1) how biogeographical and morphological factors associate with observed interactions and (2) how species-specific biogeographical characteristics associate with species' network roles. Our results show that all studied hummingbird and plant species in the meta-network were interrelated, either directly or through shared partners. The meta-network was structured into modules, resulting from hummingbirds and plants interacting preferentially with subsets of species, which differed in biogeographical, and, to a lesser extent, morphological traits. Furthermore, migrants and hummingbirds from Nearctic, Transition, and widespread regions had a higher topological importance in the meta-network. Our study illustrates how meta-networks may contribute to our current knowledge on species' biogeographical traits and biotic interactions, providing a perspective complementary to local-scale networks.
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Aves/fisiología , Ecosistema , Animales , Aves/clasificación , México , PlantasRESUMEN
Host specialization after host shifting is traditionally viewed as the pathway to speciation in parasitic plants. However, geographical and environmental changes can also influence parasite speciation, through hybridization processes. Here we investigated the impact of past climatic fluctuations, environment, and host shifts on the genetic structure and patterns of hybridization and gene flow between Psittacanthus calyculatus and P. schiedeanus, a Mesoamerican species complex. Using microsatellites (408 individuals), we document moderate genetic diversity but high genetic differentiation between widespread parental clusters, calyculatus in dry pine-oak forests and schiedeanus in cloud forests. Bayesian analyses identified a third cluster, with admixture between parental clusters in areas of xeric and tropical dry forests and high levels of migration rates following secondary contact. Coincidently host associations in these areas differ from those in areas of parental species, suggesting that past hybridization played a role in environmental and host shifts. Overall, the observed genetic and geographic patterns suggest that these Psittacanthus populations could have entered a distinct evolutionary pathway. The results provide evidence for highlights on the importance of the Pleistocene climate changes, habitat differences, and potential host shifts in the evolutionary history of Neotropical mistletoes.
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Ambiente , Hibridación Genética , Muérdago/genética , Teorema de Bayes , Flujo GénicoRESUMEN
The predominantly Asian tribe Miliuseae (Annonaceae) includes over 37 Neotropical species that are mainly distributed across Mesoamerica, from southern Mexico to northern Colombia. The tremendous ecological and morphological diversity of this clade, including ramiflory, cauliflory, flagelliflory, and clonality, suggests adaptive radiation. Despite the spectacular phenotypic divergence of this clade, little is known about its phylogenetic and evolutionary history. In this study we used a nuclear DNA marker and seven chloroplast markers, and maximum parsimony, maximum likelihood and Bayesian inference methods to reconstruct a comprehensive time-calibrated phylogeny of tribe Miliuseae, especially focusing on the Desmopsis-Stenanona clade. We also perform ancestral area reconstructions to infer the biogeographic history of this group. Finally, we use ecological niche modeling, lineage distribution models, and niche overlap tests to assess whether geographic isolation and ecological specialization influenced the diversification of lineages within this clade. We reconstructed a monophyletic Miliuseae that is divided into two strongly supported clades: (i) a Sapranthus-Tridimeris clade and (ii) a Desmopsis-Stenanona clade. The colonization of the Neotropics and subsequent diversification of Neotropical Miliuseae seems to have been associated with the expansion of the boreotropical forests during the late Eocene and their subsequent fragmentation and southern displacement. Further speciation within Neotropical Miliuseae out of the Maya block seems to have occurred during the last 15 million years. Lastly, the geographic structuring of major lineages of the Desmopsis-Stenanona clade seems to have followed a climatic gradient, supporting the hypothesis that morphological differentiation between closely related species resulted from both long-term isolation between geographic ranges and adaptation to environmental conditions.
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Annonaceae/clasificación , Filogenia , Annonaceae/genética , Teorema de Bayes , Evolución Biológica , Núcleo Celular/genética , América Central , Clima , ADN de Plantas/química , ADN de Plantas/aislamiento & purificación , ADN de Plantas/metabolismo , Bosques , Análisis de Secuencia de ADNRESUMEN
BACKGROUND: In many plant species, pollination syndromes predict the most effective pollinator. However, other floral visitors may also offer effective pollination services and promote mixed pollination systems. Several species of the species-rich Penstemon (Plantaginaceae) exhibit a suite of floral traits that suggest adaptation for pollination by both hymenopterans and hummingbirds. Transitions from the ancestral hymenopteran pollination syndrome to more derived hummingbird pollination syndrome may be promoted if the quantity or quality of visits by hummingbirds is increased and if the ancestral pollinator group performs less efficiently. The quantification of such shifts in pollination systems in the group is still limited. We aimed to investigate floral traits linked to this pollination syndrome in Penstemon gentianoides with flowers visited by bumblebees and hummingbirds. METHODS: We investigated the floral biology, pollinator assemblages, breeding system and nectar production patterns of P. gentianoides inhabiting a temperate montane forest in central Mexico. Pollination experiments were also conducted to assess the pollinator effectiveness of bumblebees and hummingbirds. RESULTS: P. gentianoides flowers are protandrous, with 8-d male phase (staminate) flowers, followed by the â¼1-7 d female phase (pistillate phase). Flowers display traits associated with hymenopteran pollination, including purple flowers abruptly ampliate-ventricose to a broad throat with anthers and stigmas included, and long lifespans. However, the nectar available in the morning hours was abundant and dilute, traits linked to flowers with a hummingbird pollination syndrome. Two hummingbird species made most of the visits to flowers, Selasphorus platycercus (30.3% of all visits), followed by Archilochus colubris (11.3%). Bumblebees (Bombus ephippiatus, B. huntii and B. weisi) accounted for 51.8% of all recorded visits, but their foraging activity was restricted to the warmer hours. Hummingbirds made more foraging bouts and visited more flowers than hymenopteran species. Flowers experimentally pollinated by B. ephippiatus produced significantly more fruits than those pollinated by S. platycercus. However, there was no statistical difference in the number of seeds produced per fruit when a bumblebee or a hummingbird was the pollinator. CONCLUSIONS: We have shown that bumblebees and hummingbirds visit and pollinate P. gentianoides flowers. Despite floral traits resembling the hymenoptera pollination syndrome, flowers of P. gentianoides offer characteristic nectar rewards to flowers with a hummingbird pollination syndrome. Although pollination efficiency is higher among flowers visited by hymenoptera, the noteworthy percentage of fruit production and number of seeds per fruit derived from hummingbird pollination highlights the importance of hummingbirds as a functional group of pollinators that might have potential evolutionary consequences to the plants.
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BACKGROUND: Geographical and temporal patterns of diversification in bee hummingbirds (Mellisugini) were assessed with respect to the evolution of migration, critical for colonization of North America. We generated a dated multilocus phylogeny of the Mellisugini based on a dense sampling using Bayesian inference, maximum-likelihood and maximum parsimony methods, and reconstructed the ancestral states of distributional areas in a Bayesian framework and migratory behavior using maximum parsimony, maximum-likelihood and re-rooting methods. RESULTS: All phylogenetic analyses confirmed monophyly of the Mellisugini and the inclusion of Atthis, Calothorax, Doricha, Eulidia, Mellisuga, Microstilbon, Myrmia, Tilmatura, and Thaumastura. Mellisugini consists of two clades: (1) South American species (including Tilmatura dupontii), and (2) species distributed in North and Central America and the Caribbean islands. The second clade consists of four subclades: Mexican (Calothorax, Doricha) and Caribbean (Archilochus, Calliphlox, Mellisuga) sheartails, Calypte, and Selasphorus (incl. Atthis). Coalescent-based dating places the origin of the Mellisugini in the mid-to-late Miocene, with crown ages of most subclades in the early Pliocene, and subsequent species splits in the Pleistocene. Bee hummingbirds reached western North America by the end of the Miocene and the ancestral mellisuginid (bee hummingbirds) was reconstructed as sedentary, with four independent gains of migratory behavior during the evolution of the Mellisugini. CONCLUSIONS: Early colonization of North America and subsequent evolution of migration best explained biogeographic and diversification patterns within the Mellisugini. The repeated evolution of long-distance migration by different lineages was critical for the colonization of North America, contributing to the radiation of bee hummingbirds. Comparative phylogeography is needed to test whether the repeated evolution of migration resulted from northward expansion of southern sedentary populations.
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Aves/genética , Aves/fisiología , Migración Animal , Animales , Teorema de Bayes , Evolución Biológica , Aves/clasificación , Femenino , Especiación Genética , Masculino , América del Norte , Filogenia , Filogeografía , Análisis de Secuencia de ADNRESUMEN
The prevalent view on genetic structuring in parasitic plants is that host-race formation is caused by varying degrees of host specificity. However, the relative importance of ecological niche divergence and host specificity to population differentiation remains poorly understood. We evaluated the factors associated with population differentiation in mistletoes of the Psittacanthus schiedeanus complex (Loranthaceae) in Mexico. We used genetic data from chloroplast sequences and nuclear microsatellites to study population genetic structure and tested its association with host preferences and climatic niche variables. Pairwise genetic differentiation was associated with environmental and host preferences, independent of geography. However, environmental predictors appeared to be more important than host preferences to explain genetic structure, supporting the hypothesis that the occurrence of the parasite is largely determined by its own climatic niche and, to a lesser degree, by host specificity. Genetic structure is significant within this mistletoe species complex, but the processes associated with this structure appear to be more complex than previously thought. Although host specificity was not supported as the major determinant of population differentiation, we consider this to be part of a more comprehensive ecological model of mistletoe host-race formation that incorporates the effects of climatic niche evolution.
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Genética de Población , Muérdago/genética , Clima , Ecosistema , Interacciones Huésped-Parásitos , Loranthaceae/fisiología , México , Repeticiones de MicrosatéliteRESUMEN
BACKGROUND: Cloud forests, characterized by a persistent, frequent or seasonal low-level cloud cover and fragmented distribution, are one of the most threatened habitats, especially in the Neotropics. Tree ferns are among the most conspicuous elements in these forests, and ferns are restricted to regions in which minimum temperatures rarely drop below freezing and rainfall is high and evenly distributed around the year. Current phylogeographic data suggest that some of the cloud forest-adapted species remained in situ or expanded to the lowlands during glacial cycles and contracted allopatrically during the interglacials. Although the observed genetic signals of population size changes of cloud forest-adapted species including tree ferns correspond to predicted changes by Pleistocene climate change dynamics, the observed patterns of intraspecific lineage divergence showed temporal incongruence. METHODS: Here we combined phylogenetic analyses, ancestral area reconstruction, and divergence time estimates with climatic and altitudinal data (environmental space) for phenotypic traits of tree fern species to make inferences about evolutionary processes in deep time. We used phylogenetic Bayesian inference and geographic and altitudinal distribution of tree ferns to investigate ancestral area and elevation and environmental preferences of Mesoamerican tree ferns. The phylogeny was then used to estimate divergence times and ask whether the ancestral area and elevation and environmental shifts were linked to climatic events and historical climatic preferences. RESULTS: Bayesian trees retrieved Cyathea, Alsophyla, Gymnosphaera and Sphaeropteris in monophyletic clades. Splits for species in these genera found in Mesoamerican cloud forests are recent, from the Neogene to the Quaternary, Australia was identified as the ancestral area for the clades of these genera, except for Gymnosphaera that was Mesoamerica. Climate tolerance was not divergent from hypothesized ancestors for the most significant variables or elevation. For elevational shifts, we found repeated change from low to high elevations. CONCLUSIONS: Our data suggest that representatives of Cyatheaceae main lineages migrated from Australia to Mesoamerican cloud forests in different times and have persisted in these environmentally unstable areas but extant species diverged recentrly from their ancestors.