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

Author(s):  
Leonardo S Miranda ◽  
Bernardo O Prestes ◽  
Alexandre Aleixo

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.

2021 ◽  
Author(s):  
Tomasz Mamos ◽  
Krzysztof Jazdzewski ◽  
Zuzana Ciamporova-Zatovicova ◽  
Fedor Ciampor ◽  
Michal Grabowski

Abstract The Carpathians are one of the key biodiversity hotspots in Europe. The mountain chain uplifted during Alpine orogenesis and is characterised by a complex geological history. Its current biodiversity was highly influenced by Pleistocene glaciations. The goal of the current study was to examine the phylogenetic and demographic history of Gammarus balcanicus species complex in the Carpathians using multiple markers as well as to delimit, using an integrative approach, and describe new species hidden so far under the name G. balcanicus. Results shown that divergence of the studied lineages reaches back to the Miocene, which supports the hypothesis of their survival in multiple micro refugia. Moreover, the increase of their diversification rate in the Pleistocene suggests that glaciation was the driving force of their speciation. The climatic changes during and after the Pleistocene also played a major role in the demography of the local Carpathian lineages. Comparison of diversity patterns and phylogenetic relationships of both, the mitochondrial and nuclear markers, provide evidence of putative hybridisation and retention of ancient polymorphism (i.e., incomplete lineage sorting). The morphological examination supported the existence of two morphological types; one we describe as G. stasiuki sp. nov. and another we redescribe as G. tatrensis (S. Karaman, 1931).


Author(s):  
Maddie E. James ◽  
Henry Arenas-Castro ◽  
Jeffery S. Groh ◽  
Jan Engelstädter ◽  
Daniel Ortiz-Barrientos

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.


2021 ◽  
Author(s):  
Tomasz Mamos ◽  
Krzysztof Jazdzewski ◽  
Zuzana Ciamporova-Zatovicova ◽  
Fedor Ciampor ◽  
Michal Grabowski

Abstract The Carpathians are one of the key biodiversity hotspots in Europe. The mountain chain uplifted during Alpine orogenesis and is characterised by a complex geological history. Its current biodiversity was highly influenced by Pleistocene glaciations. The goal of the current study was to examine the phylogenetic and demographic history of Gammarus balcanicus species complex in the Carpathians using multiple markers as well as to delimit, using an integrative approach, and describe new species hidden so far under the name G. balcanicus. Results shown that divergence of the studied lineages reaches back to the Miocene, which supports the hypothesis of their survival in multiple micro refugia. Moreover, the increase of their diversification rate in the Pleistocene suggests that glaciation was the driving force of their speciation. The climatic changes during and after the Pleistocene also played a major role in the demography of the local Carpathian lineages. Comparison of diversity patterns and phylogenetic relationships of both, the mitochondrial and nuclear markers, provide evidence of putative hybridisation and retention of ancient polymorphism (i.e., incomplete lineage sorting). The morphological examination supported the existence of two morphological types; one we describe as G. stasiuki sp. nov. and another we redescribe as G. tatrensis (S. Karaman, 1931).


2020 ◽  
Vol 70 (1) ◽  
pp. 162-180
Author(s):  
Jeffrey P Rose ◽  
Cassio A P Toledo ◽  
Emily Moriarty Lemmon ◽  
Alan R Lemmon ◽  
Kenneth J Sytsma

Abstract Phylogenomic data from a rapidly increasing number of studies provide new evidence for resolving relationships in recently radiated clades, but they also pose new challenges for inferring evolutionary histories. Most existing methods for reconstructing phylogenetic hypotheses rely solely on algorithms that only consider incomplete lineage sorting (ILS) as a cause of intra- or intergenomic discordance. Here, we utilize a variety of methods, including those to infer phylogenetic networks, to account for both ILS and introgression as a cause for nuclear and cytoplasmic-nuclear discordance using phylogenomic data from the recently radiated flowering plant genus Polemonium (Polemoniaceae), an ecologically diverse genus in Western North America with known and suspected gene flow between species. We find evidence for widespread discordance among nuclear loci that can be explained by both ILS and reticulate evolution in the evolutionary history of Polemonium. Furthermore, the histories of organellar genomes show strong discordance with the inferred species tree from the nuclear genome. Discordance between the nuclear and plastid genome is not completely explained by ILS, and only one case of discordance is explained by detected introgression events. Our results suggest that multiple processes have been involved in the evolutionary history of Polemonium and that the plastid genome does not accurately reflect species relationships. We discuss several potential causes for this cytoplasmic-nuclear discordance, which emerging evidence suggests is more widespread across the Tree of Life than previously thought. [Cyto-nuclear discordance, genomic discordance, phylogenetic networks, plastid capture, Polemoniaceae, Polemonium, reticulations.]


2018 ◽  
Author(s):  
Julie Marin ◽  
Guillaume Achaz ◽  
Anton Crombach ◽  
Amaury Lambert

AbstractEvolutionary relationships between species are traditionally represented in the form of a tree, the species tree. Its reconstruction from molecular data is hindered by frequent conflicts between gene genealogies. Usually, these disagreements are explained by incomplete lineage sorting (ILS) due to random coalescences of gene lineages inside the edges of the species tree. This paradigm, the multi-species coalescent (MSC), is constantly violated by the ubiquitous presence of gene flow, leading to incongruences between gene trees that cannot be explained by ILS alone. Here we argue instead in favor of a vision acknowledging the importance of gene flow and where gene histories shape the species tree rather than the opposite. We propose a new framework for modeling the joint evolution of gene and species lineages relaxing the hierarchy between the species tree and gene trees. We implement this framework in two mathematical models called the gene-based diversification models (GBD): 1) GBD-forward following all evolving genomes and 2) GBD-backward based on coalescent theory. They feature four parameters tuning colonization, gene flow, genetic drift and genetic differentiation. We propose a quick inference method based on differences between gene trees. Applied to two empirical data-sets prone to gene flow, we find a better support for the GBD model than for the MSC model. Along with the increasing awareness of the extent of gene flow, this work shows the importance of considering the richer signal contained in genomic histories, rather than in the mere species tree, to better apprehend the complex evolutionary history of species.


2018 ◽  
Author(s):  
Richard J. Wang ◽  
Matthew W. Hahn

AbstractSpeciation genes are responsible for reproductive isolation between species. By directly participating in the process of speciation, the genealogies of isolating loci have been thought to more faithfully represent species trees. The unique properties of speciation genes may provide valuable evolutionary insights and help determine the true history of species divergence. Here, we formally analyze whether genealogies from loci participating in Dobzhansky-Muller (DM) incompatibilities are more likely to be concordant with the species tree under incomplete lineage sorting (ILS). Individual loci differ stochastically from the true history of divergence with a predictable frequency due to ILS, and these expectations—combined with the DM model of intrinsic reproductive isolation from epistatic interactions—can be used to examine the probability of concordance at isolating loci. Contrary to existing verbal models, we find that reproductively isolating loci that follow the DM model are often more likely to have discordant gene trees. These results are dependent on the pattern of isolation observed between three species, the time between speciation events, and the time since the last speciation event. Results supporting a higher probability of discordance are found for both derived-derived and derived-ancestral DM pairs, and regardless of whether incompatibilities are allowed or prohibited from segregating in the same population. Our overall results suggest that DM loci are unlikely to be especially useful for reconstructing species relationships, even in the presence of gene flow between incipient species, and may in fact be positively misleading.


2020 ◽  
Author(s):  
Liming Cai ◽  
Zhenxiang Xi ◽  
Emily Moriarty Lemmon ◽  
Alan R Lemmon ◽  
Austin Mast ◽  
...  

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.


The Auk ◽  
2019 ◽  
Vol 136 (4) ◽  
Author(s):  
Catalina Palacios ◽  
Silvana García-R ◽  
Juan Luis Parra ◽  
Andrés M Cuervo ◽  
F Gary Stiles ◽  
...  

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.


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