Shallow genetic divergence and distinct phenotypic differences between two Andean hummingbirds: Speciation with gene flow?

The Auk ◽  
2019 ◽  
Vol 136 (4) ◽  
Author(s):  
Catalina Palacios ◽  
Silvana García-R ◽  
Juan Luis Parra ◽  
Andrés M Cuervo ◽  
F Gary Stiles ◽  
...  
Keyword(s):  
Gene Flow ◽  
Genetic Differentiation ◽  
Incomplete Lineage Sorting ◽  
Lineage Sorting ◽  
Phenotypic Differences ◽  
Adaptive Mechanisms ◽  
The Face ◽  
Gloger’S Rule ◽  
Divergence With Gene Flow ◽  
Neutral Markers

Abstract Ecological speciation can proceed despite genetic interchange when selection counteracts the homogenizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, 2 parapatric Andean hummingbirds with marked plumage divergence. We sequenced putatively neutral markers (mitochondrial DNA [mtDNA] and nuclear ultraconserved elements [UCEs]) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Gloger’s rule that darker forms occur in more humid environments, and examined morphological variation to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was low in both ND2 and UCEs. Coalescent estimates of migration were consistent with divergence with gene flow, but we cannot reject incomplete lineage sorting reflecting recent speciation as an explanation for patterns of genetic variation. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in morphology. Although we reject adaptation to variation in macroclimatic conditions as a cause of divergence, speciation may have occurred in the face of gene flow driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.

scholarly journals Shallow evolutionary divergence between two Andean hummingbirds: Speciation with gene flow?

2018 ◽  
Author(s):  
Catalina Palacios ◽  
Silvana García-R ◽  
Juan Luis Parra ◽  
Andrés M. Cuervo ◽  
F. Gary Stiles ◽  
...  
Keyword(s):  
Gene Flow ◽  
Genetic Differentiation ◽  
Genetic Basis ◽  
Flow Model ◽  
Evolutionary Divergence ◽  
Phenotypic Differences ◽  
Adaptive Mechanisms ◽  
The Face ◽  
Divergence With Gene Flow ◽  
Neutral Markers

AbstractEcological speciation can proceed despite genetic interchange when selection counteracts homogeneizing effects of migration. We tested predictions of this divergence-with-gene-flow model in Coeligena helianthea and C. bonapartei, two parapatric Andean hummigbirds with marked plumage divergence. We sequenced neutral markers (mtDNA and nuclear ultra conserved elements) to examine genetic structure and gene flow, and a candidate gene (MC1R) to assess its role underlying divergence in coloration. We also tested the prediction of Glogers’ rule that darker forms occur in more humid environments, and compared ecomorphological variables to assess adaptive mechanisms potentially promoting divergence. Genetic differentiation between species was very low and coalescent estimates of migration were consistent with divergence with gene flow. MC1R variation was unrelated to phenotypic differences. Species did not differ in macroclimatic niches but were distinct in ecomorphology. Although we reject adaptation to variation in humidity as the cause of divergence, we hypothesize that speciation likely occurred in the face of gene flow, driven by other ecological pressures or by sexual selection. Marked phenotypic divergence with no neutral genetic differentiation is remarkable for Neotropical birds, and makes C. helianthea and C. bonapartei an appropriate system in which to search for the genetic basis of species differences employing genomics.

scholarly journals Highly replicated evolution of parapatric ecotypes

2020 ◽  
Author(s):  
Maddie E. James ◽  
Henry Arenas-Castro ◽  
Jeffery S. Groh ◽  
Jan Engelstädter ◽  
Daniel Ortiz-Barrientos
Keyword(s):  
Gene Flow ◽  
Genetic Structure ◽  
Incomplete Lineage Sorting ◽  
Parallel Evolution ◽  
Geographic Location ◽  
Lineage Sorting ◽  
Colonization History ◽  
Multiple Origins ◽  
History Of ◽  
Neutral Markers

AbstractParallel evolution of ecotypes occurs when selection independently drives the evolution of similar traits across similar environments. The multiple origin of ecotypes is often inferred on the basis of a phylogeny which clusters populations according to geographic location and not by the environment they occupy. However, the use of phylogenies to infer parallel evolution in closely related populations is problematic due to the potential for gene flow and incomplete lineage sorting to uncouple the genetic structure at neutral markers from the colonization history of populations. Here, we demonstrate multiple origins within ecotypes of an Australian wildflower, Senecio lautus. We observed strong genetic structure as well as phylogenetic clustering by geography, and show this is unlikely due to gene flow between parapatric ecotypes, which is surprisingly low. We further confirm this analytically by demonstrating that phylogenetic distortion due to gene flow often requires higher levels of migration than those observed in S. lautus. Our results imply that selection can repeatedly create similar phenotypes despite the perceived homogenizing effects of gene flow.

scholarly journals Complete mitochondrial genomes do not distinguish phenotypically distinct lineages of Andean Coeligena hummingbirds

2020 ◽  
Author(s):  
Catalina Palacios ◽  
Leonardo Campagna ◽  
Juan Luis Parra ◽  
Carlos Daniel Cadena
Keyword(s):  
Genetic Differentiation ◽  
Incomplete Lineage Sorting ◽  
Haplotype Network ◽  
Mitochondrial Genomes ◽  
Lineage Sorting ◽  
Evolutionary Mechanisms ◽  
Phenotypic Differences ◽  
Network Analyses ◽  
Alternative Hypotheses ◽  
Complete Mitochondrial Genomes

AbstractLack of divergence in mitochondrial DNA between species with clear phenotypic differences may be the result of low resolution of markers, incomplete lineage sorting, introgression, or the interplay of various evolutionary mechanisms acting on different traits and genomic regions through time. Previous work revealed that the Andean hummingbirds Coeligena bonapartei and C. helianthea lack genetic divergence in the mitochondrial ND2 gene, which shows variation discordant with coloration phenotype but consistent with geography. We sequenced and analyzed complete mitochondrial genomes for C. b. bonapartei, C. b. consita, C. h. helianthea and C. h. tamai to assess whether patterns revealed by ND2 analyses hold when considering the entire mitogenome, and to shed light into the evolutionary history of these hummingbirds. We found very low genetic differentiation in mitogenomes among the four lineages of Coeligena, confirming patterns based on ND2 data. Estimates of genetic differentiation, phylogenies and haplotype network analyses of complete mitogenomes did not separate phenotypically distinct taxa, but were consistent with a previously described pattern of northern vs. southern divergence along the Cordillera Oriental of Colombia. Mitogenomes of C. b. bonapartei and C. h. helianthea are indistinguishable, suggesting incomplete lineage sorting or strong introgression. Mitogenomes of C. b. consita and C. h. tamai are slightly differentiated, but they are more similar to each other than either is to that of its respective nominate subspecies, a result also suggestive of mtDNA introgression despite distinct phenotypic differences. Our results indicate that various evolutionary mechanisms playing out over a complex biogeographic scenario in the Colombian Andes drove divergence in phenotypes and mitochondrial genomes of Coeligena hummingbirds, and lead to alternative hypotheses to be tested with whole-genome analyses.

scholarly journals The Perfect Storm: Gene Tree Estimation Error, Incomplete Lineage Sorting, and Ancient Gene Flow Explain the Most Recalcitrant Ancient Angiosperm Clade, Malpighiales

2020 ◽  
Author(s):  
Liming Cai ◽  
Zhenxiang Xi ◽  
Emily Moriarty Lemmon ◽  
Alan R Lemmon ◽  
Austin Mast ◽  
...  
Keyword(s):  
Gene Flow ◽  
Incomplete Lineage Sorting ◽  
Estimation Error ◽  
Gene Tree ◽  
Species Tree ◽  
Flowering Plant ◽  
Estimation Methods ◽  
Lineage Sorting ◽  
Tree Estimation ◽  
Perfect Storm

Abstract The genomic revolution offers renewed hope of resolving rapid radiations in the Tree of Life. The development of the multispecies coalescent (MSC) model and improved gene tree estimation methods can better accommodate gene tree heterogeneity caused by incomplete lineage sorting (ILS) and gene tree estimation error stemming from the short internal branches. However, the relative influence of these factors in species tree inference is not well understood. Using anchored hybrid enrichment, we generated a data set including 423 single-copy loci from 64 taxa representing 39 families to infer the species tree of the flowering plant order Malpighiales. This order includes nine of the top ten most unstable nodes in angiosperms, which have been hypothesized to arise from the rapid radiation during the Cretaceous. Here, we show that coalescent-based methods do not resolve the backbone of Malpighiales and concatenation methods yield inconsistent estimations, providing evidence that gene tree heterogeneity is high in this clade. Despite high levels of ILS and gene tree estimation error, our simulations demonstrate that these two factors alone are insufficient to explain the lack of resolution in this order. To explore this further, we examined triplet frequencies among empirical gene trees and discovered some of them deviated significantly from those attributed to ILS and estimation error, suggesting gene flow as an additional and previously unappreciated phenomenon promoting gene tree variation in Malpighiales. Finally, we applied a novel method to quantify the relative contribution of these three primary sources of gene tree heterogeneity and demonstrated that ILS, gene tree estimation error, and gene flow contributed to 10.0%, 34.8%, and 21.4% of the variation, respectively. Together, our results suggest that a perfect storm of factors likely influence this lack of resolution, and further indicate that recalcitrant phylogenetic relationships like the backbone of Malpighiales may be better represented as phylogenetic networks. Thus, reducing such groups solely to existing models that adhere strictly to bifurcating trees greatly oversimplifies reality, and obscures our ability to more clearly discern the process of evolution.

scholarly journals A Bayesian Implementation of the Multispecies Coalescent Model with Introgression for Phylogenomic Analysis

2019 ◽  
Vol 37 (4) ◽  
pp. 1211-1223 ◽  
Author(s):  
Tomáš Flouri ◽  
Xiyun Jiao ◽  
Bruce Rannala ◽  
Ziheng Yang
Keyword(s):  
Gene Flow ◽  
Genomic Sequence ◽  
Sequence Data ◽  
Incomplete Lineage Sorting ◽  
Mosquito Species ◽  
Phylogenomic Analysis ◽  
Data Sets ◽  
Lineage Sorting ◽  
Coalescent Model ◽  
Multispecies Coalescent

Abstract Recent analyses suggest that cross-species gene flow or introgression is common in nature, especially during species divergences. Genomic sequence data can be used to infer introgression events and to estimate the timing and intensity of introgression, providing an important means to advance our understanding of the role of gene flow in speciation. Here, we implement the multispecies-coalescent-with-introgression model, an extension of the multispecies-coalescent model to incorporate introgression, in our Bayesian Markov chain Monte Carlo program Bpp. The multispecies-coalescent-with-introgression model accommodates deep coalescence (or incomplete lineage sorting) and introgression and provides a natural framework for inference using genomic sequence data. Computer simulation confirms the good statistical properties of the method, although hundreds or thousands of loci are typically needed to estimate introgression probabilities reliably. Reanalysis of data sets from the purple cone spruce confirms the hypothesis of homoploid hybrid speciation. We estimated the introgression probability using the genomic sequence data from six mosquito species in the Anopheles gambiae species complex, which varies considerably across the genome, likely driven by differential selection against introgressed alleles.

scholarly journals A Bayesian implementation of the multispecies coalescent model with introgression for comparative genomic analysis

2019 ◽  
Author(s):  
Thomas Flouris ◽  
Xiyun Jiao ◽  
Bruce Rannala ◽  
Ziheng Yang
Keyword(s):  
Gene Flow ◽  
Genomic Sequence ◽  
Sequence Data ◽  
Incomplete Lineage Sorting ◽  
Mosquito Species ◽  
Genomic Analysis ◽  
Comparative Genomic ◽  
Lineage Sorting ◽  
Multispecies Coalescent ◽  
Important Means

AbstractRecent analyses suggest that cross-species gene flow or introgression is common in nature, especially during species divergences. Genomic sequence data can be used to infer introgression events and to estimate the timing and intensity of introgression, providing an important means to advance our understanding of the role of gene flow in speciation. Here we implement the multispecies-coalescent-with-introgression (MSci) model, an extension of the multispecies-coalescent (MSC) model to incorporate introgression, in our Bayesian Markov chain Monte Carlo (MCMC) program BPP. The MSci model accommodates deep coalescence (or incomplete lineage sorting) and introgression and provides a natural framework for inference using genomic sequence data. Computer simulation confirms the good statistical properties of the method, although hundreds or thousands of loci are typically needed to estimate introgression probabilities reliably. Re-analysis of datasets from the purple cone spruce confirms the hypothesis of homoploid hybrid speciation. We estimated the introgression probability using the genomic sequence data from six mosquito species in the Anopheles gambiae species complex, which varies considerably across the genome, likely driven by differential selection against introgressed alleles.

scholarly journals Co-estimating Reticulate Phylogenies and Gene Trees from Multi-locus Sequence Data

2016 ◽  
Author(s):  
Dingqiao Wen ◽  
Luay Nakhleh
Keyword(s):  
Gene Flow ◽  
Incomplete Lineage Sorting ◽  
Phylogenetic Network ◽  
Simulated Data ◽  
Biological Data ◽  
Generative Model ◽  
Divergence Times ◽  
Gene Trees ◽  
Lineage Sorting ◽  
Coalescence Times

AbstractThe multispecies network coalescent (MSNC) is a stochastic process that captures how gene trees grow within the branches of a phylogenetic network. Coupling the MSNC with a stochastic mutational process that operates along the branches of the gene trees gives rise to a generative model of how multiple loci from within and across species evolve in the presence of both incomplete lineage sorting (ILS) and reticulation (e.g., hybridization). We report on a Bayesian method for sampling the parameters of this generative model, including the species phylogeny, gene trees, divergence times, and population sizes, from DNA sequences of multiple independent loci. We demonstrate the utility of our method by analyzing simulated data and reanalyzing three biological data sets. Our results demonstrate the significance of not only co-estimating species phylogenies and gene trees, but also accounting for reticulation and ILS simultaneously. In particular, we show that when gene flow occurs, our method accurately estimates the evolutionary histories, coalescence times, and divergence times. Tree inference methods, on the other hand, underestimate divergence times and overestimate coalescence times when the evolutionary history is reticulate. While the MSNC corresponds to an abstract model of “intermixture,” we study the performance of the model and method on simulated data generated under a gene flow model. We show that the method accurately infers the most recent time at which gene flow occurs. Finally, we demonstrate the application of the new method to a 106-locus yeast data set. [Multispecies network coalescent; reticulation; incomplete lineage sorting; phylogenetic network; Bayesian inference; RJMCMC.]

Molecular systematics and phylogeography of a widespread Neotropical avian lineage: evidence for cryptic speciation with protracted gene flow throughout the Late Quaternary

2020 ◽  
Author(s):  
Leonardo S Miranda ◽  
Bernardo O Prestes ◽  
Alexandre Aleixo
Keyword(s):  
Gene Flow ◽  
Incomplete Lineage Sorting ◽  
Late Quaternary ◽  
Integrative Approach ◽  
Lineage Sorting ◽  
Distribution Models ◽  
The North ◽  
History Of ◽  
Andean South America ◽  
Spatio Temporal

Abstract Here we use an integrative approach, including coalescent-based methods, isolation–migration and species distribution models, to infer population structure, divergence times and diversification in the two species of the genus Cymbilaimus (Aves, Thamnophilidae). Our results support a recent and rapid diversification with both incomplete lineage sorting and gene flow shaping the evolutionary history of Cymbilaimus. The spatio-temporal pattern of cladogenesis suggests that Cymbilaimus originated in the north/western portion of cis-Andean South America and then diversified into the Brazilian Shield and Central America after consolidation of the modern Amazonian drainage and the Andean range. This evolutionary scenario is explained by cycles of range expansion and dispersal, followed by isolation, and recurrent gene flow, during the last 1.2 Myr. Our results agree with those recently reported for other closely related suboscine lineages, whereby the window of introgression between closely related taxa remains open for up to a few million years after their original split. In Cymbilaimus, introgression was recurrent between C. lineatus and C. sanctaemariae, even after they acquired vocal and ecological differentiation, supporting the claim that at least in Neotropical suboscines, full reproductive compatibility may take millions of years to evolve and cannot be interpreted as synonymous with a lack of speciation.

scholarly journals Evaluating the taxonomic status of the Great White Heron (Ardea herodias occidentalis) using morphological, behavioral and genetic evidence

The Auk ◽  
2019 ◽  
Vol 136 (1) ◽  
Author(s):  
Heather L McGuire ◽  
Sabrina S Taylor ◽  
Frederick H Sheldon
Keyword(s):  
Gene Flow ◽  
Dna Analysis ◽  
Incomplete Lineage Sorting ◽  
Size Variation ◽  
Florida Bay ◽  
Taxonomic Status ◽  
Morphological Characters ◽  
Lineage Sorting ◽  
Species Status ◽  
Significant Difference

Abstract The Great White Heron (GWH) has an all-white plumage and occurs in the Gulf of Mexico and Caribbean. Described originally as Ardea occidentalis, it is now considered a subspecies of Great Blue Heron (GBH; A. herodias). GWH and GBH meet in Florida Bay at the southern tip of Florida, providing the opportunity to evaluate their interaction and species status. To this end, we examined size variation and mate choice across their contact zone and genetic variation range-wide. Measurements of 7 morphological characters indicate trends, but not a significant difference, in size between GBH and GWH in southern Florida. GBH and GWH nest mainly in different places (mainland vs. islands) and at different peak times. In Florida Bay, mixed pairs occur, but white-white and blue-blue pairs are more common than in a randomly mating population. Assessing mating, however, is complicated because most, if not all, nesting blue birds are of mixed parentage. Microsatellite DNA analysis indicates that white and blue herons in Florida Bay and the outer Keys (outside Florida Bay) form a group distinct from blue forms on Florida Peninsula and elsewhere in North America. However, some gene flow occurs from white herons on the outer Keys to white and blue herons in Florida Bay, and from blue herons in Florida Bay to GBH on the Florida Peninsula. GWH alleles occur in all North American populations, but whether this is from gene flow or incomplete lineage sorting is unknown. Deciding GWH's species status is difficult. GWH and GBH meet in an ecotone where some gene flow occurs, but behavior and habitat largely isolate them. We argue in favor of splitting GWH from GBH. Regardless of how it is ultimately classified, the GWH's small population needs to be actively managed as an isolate in an extremely vulnerable environment.

scholarly journals Genomic architecture and introgression shape a butterfly radiation

Science ◽  
2019 ◽  
Vol 366 (6465) ◽  
pp. 594-599 ◽  
Author(s):  
Nathaniel B. Edelman ◽  
Paul B. Frandsen ◽  
Michael Miyagi ◽  
Bernardo Clavijo ◽  
John Davey ◽  
...  
Keyword(s):  
Gene Flow ◽  
Adaptive Radiation ◽  
Phylogenetic Relationships ◽  
De Novo ◽  
Incomplete Lineage Sorting ◽  
Color Pattern ◽  
Lineage Sorting ◽  
Genome Sequences ◽  
Genomic Architecture ◽  
Genome Assemblies

We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation.

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