skip to main content


Title: Exploring rain forest diversification using demographic model testing in the African foam‐nest treefrog Chiromantis rufescens
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
NSF-PAR ID:
10120511
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Biogeography
Volume:
46
Issue:
12
ISSN:
0305-0270
Page Range / eLocation ID:
p. 2706-2721
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Aim

    To investigate how putative barriers, forest refugia, and ecological gradients across the lower Guineo‐Congolian rain forest shape genetic and phenotypic divergence in the leaf‐folding frogAfrixalus paradorsalis, and examine the role of adjacent land bridge and sky‐islands in diversification.

    Location

    The Lower Guineo‐Congolian Forest, the Cameroonian Volcanic Line (CVL), and Bioko Island, Central Africa.

    Taxon

    Afrixalus paradorsalis(Family: Hyperoliidae), an African leaf‐folding frog.

    Methods

    We used molecular and phenotypic data to investigate diversity and divergence among theA. paradorsalisspecies complex distributed across lowland rain forests, a land bridge island, and mountains in Central Africa. We examined the coincidence of population boundaries, landscape features, divergence times, and spatial patterns of connectivity and diversity, and subsequently performed demographic modelling using genome‐wide SNP variation to distinguish among divergence mechanisms in mainland (riverine barriers, forest refugia, ecological gradients) and land bridge island populations (vicariance, overwater dispersal).

    Results

    We detected four genetically distinct allopatric populations corresponding to Bioko Island, the CVL, and two lowland rain forest populations split by the Sanaga River. Although lowland populations are phenotypically indistinguishable, pronounced body size evolution occurs at high elevation, and the timing of the formation of the high elevation population coincides with mountain uplift in the CVL. Spatial analyses and demographic modelling revealed population divergence across mainland Lower Guinea is best explained by forest refugia rather than riverine barriers or ecological gradients, and that the Bioko Island population divergence is best explained by vicariance (marine incursion) rather than overseas dispersal.

    Main conclusions

    We provide growing support for the important role of forest refugia in driving intraspecific divergences in the Guineo‐Congolian rain forest. InA. paradorsalis, sky‐islands in the CVL have resulted in greater genetic and phenotypic divergences than marine incursions of the land bridge Bioko Island, highlighting important differences in patterns of island‐driven diversification in Lower Guinea.

     
    more » « less
  2. Baldauf, Sandra (Ed.)
    Abstract The southwestern and central United States serve as an ideal region to test alternative hypotheses regarding biotic diversification. Genomic data can now be combined with sophisticated computational models to quantify the impacts of paleoclimate change, geographic features, and habitat heterogeneity on spatial patterns of genetic diversity. In this study, we combine thousands of genotyping-by-sequencing (GBS) loci with mtDNA sequences (ND1) from the Texas horned lizard (Phrynosoma cornutum) to quantify relative support for different catalysts of diversification. Phylogenetic and clustering analyses of the GBS data indicate support for at least three primary populations. The spatial distribution of populations appears concordant with habitat type, with desert populations in AZ and NM showing the largest genetic divergence from the remaining populations. The mtDNA data also support a divergent desert population, but other relationships differ and suggest mtDNA introgression. Genotype–environment association with bioclimatic variables supports divergence along precipitation gradients more than along temperature gradients. Demographic analyses support a complex history, with introgression and gene flow playing an important role during diversification. Bayesian multispecies coalescent analyses with introgression (MSci) analyses also suggest that gene flow occurred between populations. Paleo-species distribution models support two southern refugia that geographically correspond to contemporary lineages. We find that divergence times are underestimated and population sizes are overestimated when introgression occurred and is ignored in coalescent analyses, and furthermore, inference of ancient introgression events and demographic history is sensitive to inclusion of a single recently admixed sample. Our analyses cannot refute the riverine barrier or glacial refugia hypotheses. Results also suggest that populations are continuing to diverge along habitat gradients. Finally, the strong evidence of admixture, gene flow, and mtDNA introgression among populations suggests that P. cornutum should be considered a single widespread species under the General Lineage Species Concept. 
    more » « less
  3. Abstract

    The relative roles of rivers versus refugia in shaping the high levels of species diversity in tropical rainforests have been widely debated for decades. Only recently has it become possible to take an integrative approach to test predictions derived from these hypotheses using genomic sequencing and paleo‐species distribution modeling. Herein, we tested the predictions of the classic river, refuge, and river‐refuge hypotheses on diversification in the arboreal sub‐Saharan African snake genusToxicodryas. We used dated phylogeographic inferences, population clustering analyses, demographic model selection, and paleo‐distribution modeling to conduct a phylogenomic and historical demographic analysis of this genus. Our results revealed significant population genetic structure within bothToxicodryasspecies, corresponding geographically to river barriers and divergence times from the mid‐Miocene to Pliocene. Our demographic analyses supported the interpretation that rivers are indications of strong barriers to gene flow among populations since their divergence. Additionally, we found no support for a major contraction of suitable habitat during the last glacial maximum, allowing us to reject both the refuge and river‐refuge hypotheses in favor of the river‐barrier hypothesis. Based on conservative interpretations of our species delimitation analyses with the Sanger and ddRAD data sets, two new cryptic species are identified from east‐central Africa. This study highlights the complexity of diversification dynamics in the African tropics and the advantages of integrative approaches to studying speciation in tropical regions.

     
    more » « less
  4. Abstract Aim

    To test the importance of alternative diversification drivers and biogeographical processes for the evolution of Amazonian upland forest birds through a densely sampled analysis of diversification of the endemic Amazonian genusRhegmatorhinaat multiple taxonomic and temporal scales.

    Location

    Amazonia.

    Taxon

    Antbirds (Thamnophilidae).

    Methods

    We sequenced four mtDNAand nuclear gene regions of 120 individuals from 50 localities representing all recognized species and subspecies of the genus. We performed molecular phylogenetic analyses using both gene tree and species tree methods, molecular dating analysis and estimated population demographic history and gene flow.

    Results

    Dense sampling throughout the distribution ofRhegmatorhinarevealed that the main Amazonian rivers delimit the geographic distribution of taxa as inferred from mtDNAlineages. Molecular phylogenetic analyses resulted in a strongly supported phylogenetic hypothesis for the genus, with two main clades currently separated by the Madeira River. Molecular dating analysis indicated diversification during the Quaternary. Reconstruction of recent demographic history of populations revealed a trend for population expansion in eastern Amazonia and stability in the west. Estimates of gene flow corroborate the possibility that migration after divergence had some influence on the current patterns of diversity.

    Main Conclusions

    Based on broad‐scale sampling, a clarification of taxonomic boundaries, and strongly supported phylogenetic relationships, we confirm that, first, mitochondrial lineages within this upland forest Amazonian bird genus agree with spatial patterns known for decades based on phenotypes, and second, that most lineages are geographically delimited by the large Amazonian rivers. The association between past demographic changes related to palaeoclimatic cycles and the historically varying strength and size of rivers as barriers to dispersal may be the path to the answer to the long‐standing question of identifying the main drivers of Amazonian diversification.

     
    more » « less
  5. Abstract Aim

    Present Amazonian diversity patterns can result from many different mechanisms and, consequently, the factors contributing to divergence across regions and/or taxa may differ. Nevertheless, the river‐barrier hypothesis is still widely invoked as a causal process in divergence of Amazonian species. Here we use model‐based phylogeographic analyses to test the extent to which major Amazonian rivers act similarly as barriers across time and space in two broadly distributed Amazonian taxa.

    Local

    Amazon rain forest.

    Taxon

    The lizardGonatodes humeralis(Sphaerodactylidae) and the tree frogDendropsophus leucophyllatus(Hylidae).

    Methods

    We obtained RADseq data for samples distributed across main river barriers, representing main Areas of Endemism previously proposed for the region. We conduct model‐based phylogeographic and genetic differentiation analyses across each population pair.

    Results

    Measures of genetic differentiation (based onFSTcalculated from genomic data) show that all rivers are associated with significant genetic differentiation. Parameters estimated under investigated divergence models showed that divergence times for populations separated by each of the 11 bordering rivers were all fairly recent. The degree of differentiation consistently varied between taxa and among rivers, which is not an artifact of any corresponding difference in the genetic diversities of the respective taxa, or to amounts of migration based on analyses of the site‐frequency spectrum.

    Main conclusions

    Taken together, our results support a dispersal (rather than vicariance) history, without strong evidence of congruence between these species and rivers. However, once a species crossed a river, populations separated by each and every river have remained isolated—in this sense, rivers act similarly as barriers to any further gene flow. This result suggests differing degrees of persistence and gives rise to the seeming contradiction that the divergence process indeed varies across time, space and species, even though major Amazonian rivers have acted as secondary barriers to gene flow in the focal taxa.

     
    more » « less