skip to main content


Title: Historical biogeography of Vochysiaceae reveals an unexpected perspective of plant evolution in the Neotropics
Premise

Despite the fast pace of exploration of the patterns and processes influencing Neotropical plant hyperdiversity, the taxa explored are mostly from large groups that are widely distributed, morphologically diverse, or economically important. Vochysiaceae is an example of an undersampled taxon, providing an excellent system for investigating Neotropical biogeography. We present a phylogenomics‐based hypothesis of species relationships in Vochysiaceae to investigate its evolutionary history through space and time.

Methods

We inferred a phylogeny for 122 species from Vochysiaceae and seven other families of Myrtales. Fossils from four myrtalean families were used to estimate the divergence times within Vochysiaceae. Historical biogeography was estimated using ancestral range probabilities and stochastic mapping.

Results

Monophyly of all genera was supported except forQualea, which was split byRuizteraniainto two clades. Vochysiaceae originated ~100 mya, splitting into an Afrotropical and a Neotropical lineage ~50 mya, and its ancestral range is in the area currently occupied by the Cerrado.

Conclusions

The most recent common ancestor of Vochysiaceae + Myrtaceae had a West Gondwanan distribution, supporting a South American + African ancestral range of Vochysiaceae. On a global scale, geographic range reduction was the principal biogeographic event. At a finer scale, initial range reduction was also important and the Cerrado region was the most ancestral area with multiple colonization events to the Amazon, Central America, and the Atlantic Forest. Colonization events occurred from open areas to forest vegetation, an unusual finding regarding the evolution of plants in the Neotropics.

 
more » « less
NSF-PAR ID:
10456144
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
American Journal of Botany
Volume:
107
Issue:
7
ISSN:
0002-9122
Page Range / eLocation ID:
p. 1004-1020
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Aim

    We investigate the biogeographical history and diversification in a treefrog lineage distributed in contrasting (open and forested) ecoregions of South America, including three biodiversity hotspots. We evaluate the role of dispersal and whether other factors such as diversity‐dependence or paleotemperatures could explain the diversification pattern for this group. Especially focusing on the savanna endemics, we illuminate the processes governing the species assembly and evolution of the Cerrado savanna.

    Location

    South American ecoregions south of the Amazon (i.e. Atlantic Forest, Cerrado, Araucaria Forest, Pampas, Central and Southern Andes).

    Taxon

    Boana pulchellagroup.

    Methods

    We built the most complete time‐calibrated phylogeny for the group to date. We then reconstructed ancestral ranges using the dispersal‐extinction‐cladogenesis (DEC) model comparing different dispersal scenarios considering distance, adjacency and ecological similarity among regions. Centre‐of‐origin hypotheses in forest and open ecoregions were also tested. Using biogeographical stochastic mapping, we additionally estimated the contribution of range shifts across different biomes. Lastly, we evaluated several diversification models, including the effect of time, diversity‐dependence and temperature‐dependence on speciation and extinction rates.

    Results

    TheBoana pulchellagroup originated during the Early Miocene (~17.5 MYA) and underwent high speciation rates during the Middle Miocene Climatic Optimum, with a decreasing trend following the Miocene Climatic Transition. We found no support for a single ecoregion acting as a centre of origin and diversification; instead, we inferred recurrent range shifts with dispersal among dissimilar adjacent ecoregions. Speciation linearly dependent on paleotemperatures, with either no or very low constant extinction rates, best explained the slowdown diversification pattern.

    Main conclusions

    Our results support a species assembly of Cerrado savanna in South America during the Miocene with intermittent interchange with rain forest habitats. Past climate changes impacted the rate new species originated with apparently no impact on extinction. Finally, the repeated habitat shifts among open/dry and forested/humid ecoregions, rather than long‐term in‐situ diversification in single areas, highlights the very dynamic historical interchange between contrasting habitats in South America, possibly contributing to its high species diversity.

     
    more » « less
  2. Abstract Questions

    Models predicting the distribution of savannas worldwide have identified rainfall and fire as their primary determinants. However, most of them have relied upon adult traits, while juvenile traits, at the bottleneck of the plant's life cycle, have been largely overlooked. We developed a novel mechanistic model based on the effects of temperature and fire on germination traits to predict the distribution of Cerrado, i.e., the largest neotropical savanna.

    Location

    Cerrado and neighboring biomes.

    Methods

    We compiled data on the germination of seeds subjected to temperature and heat shock treatments and used generalized additive mixed models to predict germination potential as a function of temperature, species, physiognomy (forest/savanna), habits (herbs/shrubs/trees), and fire frequency.

    Results

    The best model showed that seasonal temperatures set the germination limits for seeds of both savanna and forest physiognomies. Forest seeds presented a higher germinability in the optimum temperature range, but savanna seeds had higher survival rates after heat shocks. The model revealed that the southern limit of Cerrado is determined by low winter temperatures, while the western and eastern boundaries are set by high summer temperatures. The model also predicted an area of high germination potential that coincides with high biodiversity and climate stability in the Cerrado.

    Conclusions

    Germination traits are highly valuable to predict vegetation responses to climate. Seasonal temperatures are primary determinants of the Cerrado’s extent, while fire favors the recruitment of savanna species over the Cerrado–Amazonia ecotone. Global warming may significantly impact the germination potential of native species.

     
    more » « less
  3. Abstract

    The megadiverse genusCarex(c. 2000 species, Cyperaceae) has a nearly cosmopolitan distribution, displaying an inverted latitudinal richness gradient with higher species diversity in cold‐temperate areas of the Northern Hemisphere. Despite great expansion in our knowledge of the phylogenetic history of the genus and many molecular studies focusing on the biogeography of particular groups during the last few decades, a global analysis ofCarexbiogeography and diversification is still lacking. For this purpose, we built the hitherto most comprehensiveCarex‐dated phylogeny based on three markers (ETS–ITS–matK), using a previous phylogenomic Hyb‐Seq framework, and a sampling of two‐thirds of its species and all recognized sections. Ancestral area reconstruction, biogeographic stochastic mapping, and diversification rate analyses were conducted to elucidate macroevolutionary biogeographic and diversification patterns. Our results reveal thatCarexoriginated in the late Eocene in E Asia, where it probably remained until the synchronous diversification of its main subgeneric lineages during the late Oligocene. E Asia is supported as the cradle ofCarexdiversification, as well as a “museum” of extant species diversity. Subsequent “out‐of‐Asia” colonization patterns feature multiple asymmetric dispersals clustered toward present times among the Northern Hemisphere regions, with major regions acting both as source and sink (especially Asia and North America), as well as several independent colonization events of the Southern Hemisphere. We detected 13 notable diversification rate shifts during the last 10 My, including remarkable radiations in North America and New Zealand, which occurred concurrently with the late Neogene global cooling, which suggests that diversification involved the colonization of new areas and expansion into novel areas of niche space.

     
    more » « less
  4. Abstract

    The water scavenger beetle subfamily Acidocerinae is a cosmopolitan, ecologically diverse lineage with more than 500 described species whose morphology and classification are poorly understood. We present the first phylogenetic analyses of the subfamily inferred from five loci (18S, 28S, H3, CAD, COI). We used secondary calibrations to estimate divergence times and employ this phylogeny to revise the classification and examine the historical biogeography of this lineage. Most genera are resolved as reciprocally monophyletic, with several exceptions:Horelophopsissyn. n.is recovered as a derived lineage of and placed in synonymy withAgraphydrus. The large genusHelochares, as well as its primary constituent subgeneraHelochares(s. str.) andHydrobaticusare found to be polyphyletic.Batocharesstat. n.andSindolusstat. rev.are elevated from subgenera ofHelocharesto generic rank.Crephelocharesstat. rev.is removed from synonymy withChasmogenus. We found that the crown Acidocerinae date to the mid‐Jurassic in South America + Africa (West Gondwana). South America and Africa remain important areas of endemism throughout the evolution of the lineage and are resolved either individually or in combination as the ancestral area for all but one clade that is older than 90 million years ago. Six of the seven lineages occurring in South America diverged more than 100 million years ago and are endemic to the region, suggesting the Neotropical acidocerine fauna became isolated following the breakup of West Gondwana. Conversely, lineages found on other Gondwanan fragments (India, Madagascar, Australia) are comparatively young and derived, with all being Cenozoic in age. The few taxa that occur in North America today are all the result of recent Cenozoic dispersal from South America, although North America may have played an important role as an ancestral area in the Mesozoic.

     
    more » « less
  5. Abstract Aim

    Species adapt differently to contrasting environments, such as open habitats with sparse vegetation and forested habitats with dense forest cover. We investigated colonization patterns in the open and forested environments in the diagonal of open formations and surrounding rain forests (i.e. Amazonia and Atlantic Forest) in Brazil, tested whether the diversification rates were affected by the environmental conditions and identified traits that enabled species to persist in those environments.

    Location

    South America, Brazil.

    Taxon

    Squamata, Lizards.

    Methods

    We used phylogenetic information and the current distribution of species in open and forested habitats to estimate ancestral ranges and identify range shifts relative to the current habitats. To evaluate whether these environments influenced species diversification, we tested 12 models using a Hidden Geographic State Speciation and Extinction analysis. Finally, we combined phylogenetic relatedness and species traits in a machine learning framework to identify the traits permitting adaptation in those contrasting environments.

    Results

    We identified 41 total transitions between open and forested habitats, of which 80% were from the forested habitats to the open habitats. Widely distributed species had higher speciation, turnover, extinction, and extinction fraction rates than species in forested or open habitats, but had also the lower net diversification rate. Mean body temperature, microhabitat, female snout–vent length and diet were identified as putative traits that enabled adaptation to different environments, and phylogenetic relatedness was an important predictor of species occurrence.

    Main conclusions

    Transitions from forested to open habitats are most common, highlighting the importance of habitat shift in current patterns of biodiversity. The combination of phylogenetic reconstruction of ancestral distributions and the machine learning framework enables us to integrate organismal trait data, environmental data and evolutionary history in a manner that could be applied on a global scale.

     
    more » « less