ABSTRACT
MAIN CONCLUSION: Natural selection influenced adaptive divergence between Cereus fernambucensis and Cereus insularis, revealing key genes governing abiotic stress responses and supporting neoteny in C. insularis. Uncovering the molecular mechanisms driving adaptive divergence in traits related to habitat adaptation remains a central challenge. In this study, we focused on the cactus clade, which includes Cereus sericifer F.Ritter, Cereus fernambucensis Lem., and Cereus insularis Hemsley. These allopatric species inhabit distinct relatively drier regions within the Brazilian Atlantic Forest, each facing unique abiotic conditions. We leveraged whole transcriptome data and abiotic variables datasets to explore lineage-specific and environment-specific adaptations in these species. Employing comparative phylogenetic methods, we identified genes under positive selection (PSG) and examined their association with non-synonymous genetic variants and abiotic attributes through a PhyloGWAS approach. Our analysis unveiled signatures of selection in all studied lineages, with C. fernambucensis northern populations and C. insularis showing the most PSGs. These PSGs predominantly govern abiotic stress regulation, encompassing heat tolerance, UV stress response, and soil salinity adaptation. Our exclusive observation of gene expression tied to early developmental stages in C. insularis supports the hypothesis of neoteny in this species. We also identified genes associated with abiotic variables in independent lineages, suggesting their role as environmental filters on genetic diversity. Overall, our findings suggest that natural selection played a pivotal role in the geographic range of these species in response to environmental and biogeographic transitions.
Subject(s)
Adaptation, Physiological , Cactaceae , Forests , Gene Expression Profiling , Phylogeny , Brazil , Cactaceae/genetics , Cactaceae/physiology , Adaptation, Physiological/genetics , Selection, Genetic , Transcriptome , Stress, Physiological/genetics , Gene Expression Regulation, PlantABSTRACT
Here we use population genomic data (ddRAD-Seq) and ecological niche modeling to test biogeographic hypotheses for the divergence of the island-endemic cactus species Cereus insularis Hemsl. (Cereeae; Cactaceae) from its sister species C. fernambucensis Lem. The Cereus insularis grows in the Fernando de Noronha Islands (FNI), a Neotropical archipelago located 350 km off the Brazilian Atlantic Forest (BAF) coast. Phylogeographic reconstructions support a northward expansion by the common ancestor of C. insularis and C. fernambucensis along the mainland BAF coast, with C. insularis diverging from the widespread mainland taxon C. fernambucensis after colonizing FNI in the late Pleistocene. The morphologically distinct C. insularis is monophyletic and nested within C. fernambucensis, as expected from a progenitor-derivative speciation model. We tested alternative biogeographic and demographic hypotheses for the colonization of the FNI using Approximate Bayesian Computation. We found the greatest support for a stepping-stone path that emerged during periods of decreased sea level (the "bridge" hypothesis), in congruence with historical ecological niche modeling that shows highly suitable habitats on stepping-stone islands during glacial periods. The outlier analyses reveal signatures of selection in C. insularis, suggesting a putative role of adaptation driving rapid anagenic differentiation of this species in FNI.
Subject(s)
Bayes Theorem , Cactaceae , Islands , Phylogeny , Phylogeography , Cactaceae/genetics , Brazil , Ecosystem , Genetics, PopulationABSTRACT
Inselbergs are azonal formations found scattered in different biomes globally. The first floristic list focusing on an inselberg in the Brazilian Amazon is presented here. We aimed to investigate floristic and phylogenetic connections among Neotropical inselbergs and analyze whether environmental variables act as a filter of plant lineages. We used a database compiled from 50 sites spanning three main Neotropical biomes (Amazon, 11 sites, Atlantic Forest, 14 sites, and Caatinga, 25 sites) comprising 2270 Angiosperm species. Our data highlight the vastly different inselberg flora found in each biome. The inselberg floras of the Atlantic Forest and Caatinga show closer phylogenetic ties than those seen in the other biome pairs. The phylogenetic lineages found in all three biomes are also strongly divergent, even within plant families. The dissimilarity between biomes suggests that distinct biogeographical histories might have unfolded even under comparable environmental filtering. Our data suggest that the inselberg flora is more related to the biome where it is located than to other factors, even when the microclimatic conditions in the outcrops differ strongly from those of the surrounding matrix. Relative to the other biomes, the flora of the Caatinga inselbergs has the highest level of species turnover. There is a possibility that plants colonized these rather distant inselbergs even when they were found under very different climatic conditions than those in the Amazonian and Atlantic Forest biomes. It is worth noting that none of the studied inselbergs found in the Caatinga biome is protected. In view of the uniqueness and drought-resilient lineages present in each group of inselbergs, along with their vulnerability to destruction or disturbance and their strong connection with water availability, we stress the need to protect this ecosystem not only to conserve plants potentially useful for ecological restoration but also to preserve the balance of this ecosystem and its connections.
ABSTRACT
Climate change has impacted biodiversity, affecting species and altering their geographical distribution. Besides understanding the impact in the species, it has been advocated that answering if different traits will be differently impacted could allow refined predictions of how climate change will jeopardize biodiversity. Our aim was to evaluate if climate change will potentially impact plant species differently, considering their traits. We evaluated 608 plant species that occur in the naturally open areas of ferruginous outcrops (namely, cangas) in the National Forest of Carajás (Eastern Amazon). Firstly, we estimated the effects of climate change on each species using species distribution modeling, and analyzed this impact in the set containing all species. Secondly, we classified plant species considering the following traits: (i) pollination syndromes (melittophily, phalaenophily, psychophily, cantharophily, entomophily, ornithophily, chiropterophily, anemophily); (ii) habit (tree, shrub, herb, liana, parasite); and (iii) the main habitat of occurrence (open areas and forests). Thirdly, we investigated if the effects of climate change could be significantly more intense considering all the different traits quoted. Our results showed that most plant species will potentially face reduction of suitable habitats under future climate and the scenarios showed that 42% of them may not find suitable areas in the cangas of Carajás. We found no significant difference within each analyzed trait, considering the potential impact of climate change. The most climatically suitable areas (i.e., areas with high probability of species occurrence in the future) are those in the southwest of the study area. These areas can be considered as priority areas for species protection against climate change.
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Abstract: Honey pollen samples of Melipona seminigra pernigraMoure & Kerr 1950 sampled between 2017 and 2019 from experimental apiaries installed in campo rupestre on canga (CRC) vegetation of the Serra dos Carajás aimed to evaluated seasonal floral availability of undisturbed and mining-influenced areas. Around one hundred pollen types were identified mainly belonging to Fabaceae, Myrtaceae and Euphorbiaceae (31, 6 and 5 species, respectively). Mining area presented the highest pollen richness, almost twice those identified in the undisturbed areas. 80% of the pollen types are rare with concentrations ≤ 2,000 pollen grains/10 g, while the remaining were the most abundant, frequent and the primary bee sources. These latter correspond mostly to native plants species such as Tapirira guianensis Aubl., Protium spp., Aparisthmium cordatum (A.Juss.) Baill., Mimosa acutistipula var. ferrea Barneby, Periandra mediterranea (Vell.) Taub., Miconia spp., Pleroma carajasense K.Rocha, Myrcia splendens (Sw.) DC., Serjania spp. and Solanum crinitum Lam. All pollen types were identified during both seasons, but higher concentration values are related to the dry period (June-September). The statistical analysis of the pollen data indicated that there was no significant difference between undisturbed and mining-influenced areas, since primary bee sources of this study are widespread used in revegetation of mined areas.
Resumo: O conteúdo polínico de amostras de mel coletadas nos anos de 2017 e 2019 de apiários experimentais de Melipona seminigra pernigraMoure & Kerr 1950, instalado dentro de uma vegetação de campo rupestre em um afloramento de canga na Serra dos Carajás, sudeste da Amazônia, foi analisado para entender a variabilidade local dos recursos florais em áreas naturais e perturbadas. Aproximadamente 100% dos tipos polínicos foram identificados e pertencem principalmente às famílias Fabaceae, Myrtaceae e Euphorbiaceae (31, 6 e 5 espécies, respectivamente). Áreas de mineração apresentaram a maior riqueza de pólen, quase o dobro daquelas identificadas em áreas perturbadas. 80% dos tipos de pólen são raros com concentrações ≤ 2.000 grãos de pólen/10g, enquanto que os restantes foram os mais abundantes, frequentes e fontes primárias para as abelhas. Este últimos correspondem principalmente a plantas nativas como Tapirira guianensis Aubl., Protium spp., Aparisthmium cordatum (A.Juss.) Baill., Mimosa acutistipula var. ferrea Barneby, Periandra mediterrânea (Vell.) Taub., Miconia spp., Pleroma carajasense K.Rocha, Myrcia splendens (Sw.) DC., Serjania spp. e Solanum crinitum Lam. Todos os tipos polínicos foram identificados durante ambas as estações, mas altas concentrações estão relacionadas ao período seco (junho-setembro). A análise estatística indicou que não houve diferença significativa nos dados de pólen de mel entre áreas naturais e áreas anteriormente degradadas, uma vez que as fontes primárias das abelhas deste estudo são amplamente utilizadas na revegetação de áreas mineradas.
ABSTRACT
The world's largest mineral iron province, Serra dos Carajás, is home to an open vegetation known as canga, found on top of isolated outcrops rising out of the Amazon rainforest. Over one thousand vascular plants species have been recorded in these canga sites, including 38 edaphic endemics. A new survey adds to our investigation of biogeographic relationships between sixteen canga outcrops and the effect of the distance between site pairs on the number of shared species, regional species turnover and species distribution patterns. Plant collecting expeditions to the westernmost site, the Serra de Campos of São Félix do Xingu (SFX), were carried out followed by the identification of all collected specimens and the creation of a species database, built to perform biogeographical analyses. Floristic relationships among the sites were investigated regarding their similarity, using multivariate analyses. The correlation between canga areas and species richness was tested, as well as the geographical distance between pairs of outcrops and their shared species. Vascular plants at SFX total 254 species including 17 edaphic endemics. All canga sites are grouped with 25% of minimum similarity, and the SFX falls within a large subgroup of outcrops. The total species number shared between site pairs does not change significantly with geographical distance but is positively correlated with the area of each outcrop. Meanwhile, shared endemic species numbers between site pairs decline when geographical distance increases, possibly imposed by the barrier of the rainforest. Our data suggest higher shared similarity between the largest and species-richest sites as opposed to geographically nearby sites, and provide useful insight for drafting conservation and compensation measures for canga locations. The size of the canga outcrops is associated to higher floristic diversity but connectivity among islands also plays a role in their similarity.
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The study of transferability of simple sequence repeats (SSR) among closely related species is a well-known strategy in population genetics, however transferability among distinct genera is less common. We tested cross-genera SSR amplification in the family Cactaceae using a total of 20 heterologous primers previously developed for the genera Ariocarpus, Echinocactus, Polaskia and Pilosocereus, in four taxa of the genus Cereus: C. fernambucensis subsp. fernambucensis, C. fernambucensis subsp. sericifer, C. jamacaru and C. insularis. Nine microsatellite loci were amplified in Cereus resulting in 35.2% of success in transferability, which is higher than the average rate of 10% reported in the literature for cross-genera transferability in eudicots. The genetic variation in the transferred markers was sufficient to perform standard clustering analysis, indicating each population as a cohesive genetic cluster. Overall, the amount of genetic variation found indicates that the transferred SSR markers might be useful in large-scale population studies within the genus Cereus.
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The results of intensive fieldwork in the National Forest of Carajás (FLONA Carajás) led to the discovery of pistillate plants of Daphnopsisfilipedunculata, an endemic species from the Serra dos Carajás, previously known only from staminate individuals. These newly discovered populations add valuable missing information related to pistillate buds, mature flowers and fruits.
ABSTRACT
In order to investigate biogeographic influences on xeric biota in the Brazilian Atlantic Forest (BAF), a biodiversity hotspot, we used a monophyletic group including three cactus taxa as a model to perform a phylogeographic study: Cereus fernambucensis subsp. fernambucensis, C. fernambucensis subsp. sericifer, and C. insularis. These cacti are allopatric and grow in xeric habitats along BAF, including isolated granite and gneiss rock outcrops (Inselbergs), sand dune vegetation (Restinga forest), and the rocky shore of an oceanic archipelago (islands of Fernando de Noronha). The nucleotide information from nuclear gene phytochrome C and plastid intergenic spacer trnS-trnG was used to perform different approaches and statistical analyses, comprising population structure, demographic changes, phylogenetic relationships, and biogeographic reconstruction in both spatial and temporal scales. We recovered four allopatric population groups with highly supported branches in the phylogenetic tree with divergence initiated in the middle Pleistocene: southern distribution of C. fernambucensis subsp. fernambucensis, northern distribution of C. fernambucensis subsp. fernambucensis together with C. insularis, southern distribution of C. fernambucensis subsp. sericifer, and northern distribution of C. fernambucensis subsp. sericifer. Further, the results suggest that genetic diversity of population groups was strongly shaped by an initial colonization event from south to north followed by fragmentation. The phylogenetic pattern found for C. insularis is plausible with peripatric speciation in the archipelago of Fernando de Noronha. To explain the phylogeographic patterns, the putative effects of both climatic and sea level changes as well as neotectonic activity during the Pleistocene are discussed.
