Genome-Scale Data Reveal Deep Lineage Divergence and a Complex Demographic History in the Texas Horned Lizard ( Phrynosoma cornutum ) throughout the Southwestern and Central United States
Title: Genome-Scale Data Reveal Deep Lineage Divergence and a Complex Demographic History in the Texas Horned Lizard ( Phrynosoma cornutum ) throughout the Southwestern and Central United States
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
Leaché, Adam D.; Portik, Daniel M.; Rivera, Danielle; Rödel, Mark‐Oliver; Penner, Johannes; Gvoždík, Václav; Greenbaum, Eli; Jongsma, Gregory F. M.; Ofori‐Boateng, Caleb; Burger, Marius; et al(
, Journal of Biogeography)
AbstractAim
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.
Allen, Kaitlin E.; Greenbaum, Eli; Hime, Paul M.; Tapondjou N., Walter P.; Sterkhova, Viktoria V.; Kusamba, Chifundera; Rödel, Mark‐Oliver; Penner, Johannes; Peterson, A. Townsend; Brown, Rafe M.(
, Ecology and Evolution)
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.
GIBBS, HL.(
, Biological Journal of the Linnean Society)
Identifying the evolutionary and ecological mechanisms that drive lineage diversification in the species-rich tropics is of broad interest to evolutionary biologists. Here, we use phylogeographic and demographic analyses of genomic scale RADseq data to assess the impact of a large geographic feature, the Amazon River, on lineage formation in a venomous pitviper, Bothrops atrox. We compared genetic differentiation in samples from four sites near Santarem, Brazil that spanned the Amazon and represented major habitat types. A species delimitation analysis identified each population as a distinct evolutionary lineage while a species tree analysis with populations as taxa revealed a phylogenetic tree consistent with dispersal across the Amazon from north to south. Phylogenetic analyses of mtDNA variation confirmed this pattern and suggest that all lineages originated during the mid- to late-Pleistocene. Historical demographic analyses support a population model of lineage formation through isolation between lineages with low ongoing migration between large populations and reject a model of differentiation through isolation by distance alone. Our results provide a rare example of a phylogeographic pattern demonstrating dispersal over evolutionary time scales across a large tropical river and suggest a role for the Amazon River as a driver of in-situ divergence by both impeding (but not preventing) gene flow and through parapatric differentiation along an ecological gradient.
Prada, Carlos; Hellberg, Michael E.(
, Journal of Evolutionary Biology)
Abstract
The distributions of many sister species in the sea overlap geographically but are partitioned along depth gradients. The genetic changes leading to depth segregation may evolve in geographic isolation as a prerequisite to coexistence or may emerge during primary divergence leading to new species. These alternatives can now be distinguished via the power endowed by the thousands of scorable loci provided by second‐generation sequence data. Here, we revisit the case of two depth‐segregated, genetically isolated ecotypes of the nominal Caribbean candelabrum coralEunicea flexuosa. Previous analyses based on a handful of markers could not distinguish between models of genetic exchange after a period of isolation (consistent with secondary contact) and divergence with gene flow (consistent with primary divergence). Analyses of the history of isolation, genetic exchange and population size based on 15,640 new SNP markers derived from RNAseq data best support models where divergence began 800K BP and include epochs of divergence with gene flow, but with an intermediate period of transient isolation. Results also supported the previous conclusion that recent exchange between the ecotypes occurs asymmetrically from the Shallow lineage to the Deep. Parallel analyses of data from two other corals with depth‐segregated populations (Agaricia fragilisandPocillopora damicornis) suggest divergence leading to depth‐segregated populations may begin with a period of symmetric exchange, but that an epoch of population isolation precedes more complete isolation marked by asymmetric introgression. Thus, while divergence‐with‐gene flow may account for much of the differentiation that separates closely related, depth‐segregated species, it remains to be seen whether any critical steps in the speciation process only occur when populations are isolated.
Musher, Lukas J.; Galante, Peter J.; Thom, Gregory; Huntley, Jerry W.; Blair, Mary E.(
, Journal of Biogeography)
AbstractAim
We aim to test the biogeographic drivers of diversification and gene‐flow at the Isthmus of Panama using a species complex of suboscine birds as a case study. We specifically evaluate whether diversification in these birds is better explained by continuous parapatry or a Refuge Model of periodic isolation and gene‐flow due glacial cycling.
We develop an approach to distinguish among the two biogeographic hypotheses—parapatric ecological speciation versus climatically mediated speciation—by making explicit predictions for demographic history, niche evolution and change in geographic connectivity over time. We sequenced genome‐wide markers (ultraconserved elements) to estimate the evolutionary and demographic history of this group. We applied both phylogenomic network analyses and demographic modelling using a supervised machine learning approach. These genetic analyses were combined with a novel distribution modelling method that estimates the probability of interspecies contact as a function of climatic conditions through time.
Results
We found that both spatial and genetic analyses revealed concordant results. All speciation events occurred during the Pleistocene and were characterized by non‐continuous gene‐flow, supporting a scenario of climate‐mediated diversification. Spatial connectivity was highest at present, consistent with our best demographic model of secondary contact.
Main conclusions
This study exemplifies a mechanism by which speciation, dispersal and introgression unfold in an important region for Neotropical diversification—the Isthmus of Panama—where periods ofbothisolation and introgression probably drive diversification. Overall, our results are consistent with the Refuge Model of biotic diversification, but suggest that introgression may be a crucial yet underappreciated component of this classic paradigm.
Finger, Nicholas, Farleigh, Keaka, Bracken, Jason T, Leaché, Adam D, François, Olivier, Yang, Ziheng, Flouri, Tomas, Charran, Tristan, Jezkova, Tereza, Williams, Dean A, and Blair, Christopher. Genome-Scale Data Reveal Deep Lineage Divergence and a Complex Demographic History in the Texas Horned Lizard ( Phrynosoma cornutum ) throughout the Southwestern and Central United States. Retrieved from https://par.nsf.gov/biblio/10330080. Genome Biology and Evolution 14.1 Web. doi:10.1093/gbe/evab260.
Finger, Nicholas, Farleigh, Keaka, Bracken, Jason T, Leaché, Adam D, François, Olivier, Yang, Ziheng, Flouri, Tomas, Charran, Tristan, Jezkova, Tereza, Williams, Dean A, & Blair, Christopher. Genome-Scale Data Reveal Deep Lineage Divergence and a Complex Demographic History in the Texas Horned Lizard ( Phrynosoma cornutum ) throughout the Southwestern and Central United States. Genome Biology and Evolution, 14 (1). Retrieved from https://par.nsf.gov/biblio/10330080. https://doi.org/10.1093/gbe/evab260
Finger, Nicholas, Farleigh, Keaka, Bracken, Jason T, Leaché, Adam D, François, Olivier, Yang, Ziheng, Flouri, Tomas, Charran, Tristan, Jezkova, Tereza, Williams, Dean A, and Blair, Christopher.
"Genome-Scale Data Reveal Deep Lineage Divergence and a Complex Demographic History in the Texas Horned Lizard ( Phrynosoma cornutum ) throughout the Southwestern and Central United States". Genome Biology and Evolution 14 (1). Country unknown/Code not available. https://doi.org/10.1093/gbe/evab260.https://par.nsf.gov/biblio/10330080.
@article{osti_10330080,
place = {Country unknown/Code not available},
title = {Genome-Scale Data Reveal Deep Lineage Divergence and a Complex Demographic History in the Texas Horned Lizard ( Phrynosoma cornutum ) throughout the Southwestern and Central United States},
url = {https://par.nsf.gov/biblio/10330080},
DOI = {10.1093/gbe/evab260},
abstractNote = {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.},
journal = {Genome Biology and Evolution},
volume = {14},
number = {1},
author = {Finger, Nicholas and Farleigh, Keaka and Bracken, Jason T and Leaché, Adam D and François, Olivier and Yang, Ziheng and Flouri, Tomas and Charran, Tristan and Jezkova, Tereza and Williams, Dean A and Blair, Christopher},
editor = {Baldauf, Sandra}
}
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