skip to main content


Title: Paleoclimatic evolution as the main driver of current genomic diversity in the widespread and polymorphic Neotropical songbird Arremon taciturnus
Abstract

Several factors have been proposed as drivers of species diversification in the Neotropics, including environmental heterogeneity, the development of drainage systems and historical changes in forest distribution due to climatic oscillations. Here, we investigate which drivers contributed to the evolutionary history and current patterns of diversity of a polymorphic songbird (Arremon taciturnus) that is widely distributed in Amazonian and Atlantic forests as well as in Cerrado gallery and seasonally‐dry forests. We use genomic, phenotypic and habitat heterogeneity data coupled with climatic niche modelling. Results suggest the evolutionary history of the species is mainly related to paleoclimatic changes, although changes in the strength of the Amazon river as a barrier to dispersal, current habitat heterogeneity and geographic distance were also relevant. We propose an ancestral distribution in the Guyana Shield, and recent colonization of areas south of the Amazon river at ~380 to 166 kya, and expansion of the distribution to southern Amazonia, Cerrado and the Atlantic Forest. Since then, populations south of the Amazon River have been subjected to cycles of isolation and possibly secondary contact due to climatic changes that affected habitat heterogeneity and population connectivity. Most Amazonian rivers are not associated with long lasting isolation of populations, but some might act as secondary barriers, susceptible to crossing under specific climatic conditions. Morphological variation, while stable in some parts of the distribution, is not a reliable indicator of genetic structure or phylogenetic relationships.

 
more » « less
NSF-PAR ID:
10456500
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
29
Issue:
15
ISSN:
0962-1083
Page Range / eLocation ID:
p. 2922-2939
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    We assessed population structure and the spatio‐temporal pattern of diversification in the Glossy AntshrikeSakesphorus luctuosus(Aves, Thamnophilidae) to understand the processes shaping the evolutionary history of Amazonian floodplains and address unresolved taxonomic controversies surrounding its species limits. By targeting ultraconserved elements (UCEs) from 32 specimens ofS.luctuosus, we identified independent lineages and estimated their differentiation, divergence times, and migration rates. We also estimated current and past demographic histories for each recovered lineage. We found evidence confirming thatS.luctuosusconsists of a single species, comprising at least four populations, with some highly admixed individuals and overall similar levels of migration between populations. We confirmed the differentiation of the Araguaia River basin population (S. l.araguayae) and gathered circumstantial evidence indicating that the taxonS.hagmannimay represent a highly introgressed population between three distinct phylogroups ofS.luctuosus. Divergences between populations occurred during the last 1.2 mya. Signs of population expansions were detected for populations attributed to subspeciesS. l.luctuosus, but not for theS. l.araguayaepopulation. Our results support thatS.luctuosushas had a complex population history, resulting from a high dependence on southeastern “clear water” seasonally flooded habitats and their availability through time. Spatial and demographic expansions toward the western “white water” flooded forests might be related to recent changes in connectivity and availability of these habitats. Our study reinforces the view that isolation due to absence of suitable habitat has been an important driver of population differentiation within Amazonian flooded forests, but also that differences betweenvárzeas(“white water” floodplains, mostly in southwestern Amazonia) andigapós(“clear water” floodplains, especially located in the east) should be further explored as drivers of micro‐evolution for terrestrial species.

     
    more » « less
  2. Abstract Aim

    The drivers of genetic diversity in Amazonia, the most species‐rich set of ecosystems on Earth, are still incompletely understood. Species from distinct Amazonian ecosystems have unique biogeographic histories that will reflect regional landscape and climatic drivers of genetic diversity. We studied bird species from patchy Amazonian white‐sand ecosystems (WSE) to evaluate the occurrence of shared biogeographic patterns to better understand the complex environmental and landscape history of Amazonia and its biodiversity.

    Location

    Northern South America; Amazonia.

    Taxon

    Passeriformes.

    Methods

    We sequenced Ultra‐conserved Elements (UCEs) from 177 samples of seven bird species associated with WSE that have overlapping ranges. We used the SNP matrices and sequence data to estimate genetic structure and migration surfaces using ‘conStruct’ andeems, performed model‐selection to obtain the most probable demographic histories on ‘PipeMasterand implemented analyses of shared demography withecoevolity.

    Results

    Shallow genetic structure patterns varied among species. The Amazon river was the only barrier shared among them. Population structure dates to no more than 450,000 years ago. Nine geographically structured populations showed signals of population size changes and eight of these occur in Northern Amazonia. Population expansion was inferred at two distinct times: ~100,000 and ~ 50,000 years ago. The timing of co‐expanding populations is consistent with differences in habitat preference, as species that prefer dense scrubby to forested vegetation expanded more recently compared to species that prefer open vegetation.

    Main conclusions

    WSE species responded in concert to environmental and landscape changes that occurred in the relatively recent past. Population expansions were likely driven by the genesis of new WSE patches and a return to wetter conditions after glacial periods. Pleistocene climatic cycles affected the distribution and dynamics of open vegetation habitats in Amazonia, especially in the Northern region, driving genetic diversity and demographic patterns of its associated biota.

     
    more » « less
  3. 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
  4. Abstract Aim

    Species with wide distributions spanning the African Guinean and Congolian rain forests are often composed of genetically distinct populations or cryptic species with geographic distributions that mirror the locations of the remaining forest habitats. We used phylogeographic inference and demographic model testing to evaluate diversification models in a widespread rain forest species, the African foam‐nest treefrogChiromantis rufescens.

    Location

    Guinean and Congolian rain forests, West and Central Africa.

    Taxon

    Chiromantis rufescens.

    Methods

    We collected mitochondrial DNA (mtDNA) and single‐nucleotide polymorphism (SNP) data for 130 samples ofC. rufescens. After estimating population structure and inferring species trees using coalescent methods, we tested demographic models to evaluate alternative population divergence histories that varied with respect to gene flow, population size change and periods of isolation and secondary contact. Species distribution models were used to identify the regions of climatic stability that could have served as forest refugia since the last interglacial.

    Results

    Population structure withinC. rufescensresembles the major biogeographic regions of the Guinean and Congolian forests. Coalescent‐based phylogenetic analyses provide strong support for an early divergence between the western Upper Guinean forest and the remaining populations. Demographic inferences support diversification models with gene flow and population size changes even in cases where contemporary populations are currently allopatric, which provides support for forest refugia and barrier models. Species distribution models suggest that forest refugia were available for each of the populations throughout the Pleistocene.

    Main conclusions

    Considering historical demography is essential for understanding population diversification, especially in complex landscapes such as those found in the Guineo–Congolian forest. Population demographic inferences help connect the patterns of genetic variation to diversification model predictions. The diversification history ofC. rufescenswas shaped by a variety of processes, including vicariance from river barriers, forest fragmentation and adaptive evolution along environmental gradients.

     
    more » « less
  5. Abstract Aim

    To investigate the cryptic diversity and diversification timing in the putatively low‐dispersal Amazonian leaf‐litter lizardLoxopholis osvaldoi, and to ask how geography (rivers, isolation by distance, IBD), ecological drivers (isolation by environment, IBE) and historical factors (climatic refugia) explain intraspecific genetic variation.

    Location

    Central Amazonia, Brazil.

    Taxon

    Squamata; Gymnophthalmidae;Loxopholis osvaldoi.

    Methods

    We sequenced two mitochondrial and two nuclear markers in 157 individuals. Phylogeographic structure and the occurrence of independent evolving lineages where explored through phylogenetic and coalescent analyses. A species tree and divergence dates of lineages were inferred with *BEAST, employing multiple DNA substitution rates. The potential genetic impacts of geographical distance among localities, the environment and the position of localities in relation to main rivers were tested by redundancy analysis (RDA).

    Results

    We detected 11 independently evolving and largely divergent intraspecific lineages. Lineage distribution patterns are complex and do not match any conspicuous barrier to gene flow, except for the Amazon River. Most lineages appear to have originated in the lower Miocene and Pliocene, in disagreement with the Pleistocene refuge hypothesis. IBD, IBE and rivers appear to have acted in concert establishing and maintaining genetic structure. However, when controlling for other explanatory variables, IBD explains significantly more variation than rivers, IBE or historical factors.

    Main Conclusions

    Our results strongly suggest thatL.osvaldoiis a species complex. Future taxonomic work should use an integrative approach to explore whether morphological variation is present and congruent with the genetic data. While the use of a sensitive dating analysis allowed us to better describe the diversification history ofL.osvaldoi, the lack of a spatial model of Neogene river dynamics prevents the test of specific, more informative river barrier hypotheses. The data suggest that nonlinear correlation analyses (e.g. RDA) should be preferred to detect factors that affect phylogeographic patterns in the Amazon, instead of linear multiple regressions (e.g. Mantel tests). Given the high level of cryptic diversity detected within this and other Amazonian species, we caution against hypothesis tests based solely on the distribution of nominal taxa, which can provide a rather incomplete view of the processes behind Amazonian diversity.

     
    more » « less