scholarly journals Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)

PLoS Genetics ◽  
2021 ◽  
Vol 17 (2) ◽  
pp. e1009095
Author(s):  
Thomas C. Nelson ◽  
Angela M. Stathos ◽  
Daniel D. Vanderpool ◽  
Findley R. Finseth ◽  
Yao-wu Yuan ◽  
...  
Keyword(s):  
Evolutionary History ◽  
Gene Tree ◽  
Nuclear Gene ◽  
Evolutionary Genetics ◽  
Species Tree ◽  
Pollination Syndrome ◽  
Gene Trees ◽  
Genome Wide ◽  
Hummingbird Pollination ◽  
History Of

Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele-sharing (Patterson’s D-statistic and related tests) indicate that gene-tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.

scholarly journals Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)

2020 ◽  
Author(s):  
Thomas C. Nelson ◽  
Angela M. Stathos ◽  
Daniel D. Vanderpool ◽  
Findley R. Finseth ◽  
Yao-wu Yuan ◽  
...  
Keyword(s):  
Gene Flow ◽  
Evolutionary History ◽  
Species Tree ◽  
Sister Species ◽  
Pollination Syndrome ◽  
Gene Trees ◽  
Trait Evolution ◽  
Genome Wide ◽  
Hummingbird Pollination ◽  
History Of

AbstractInferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele-sharing (Patterson’s D-statistic and related tests) indicate that gene-tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.Author SummaryAdaptive radiations, which involve both divergent evolution of new traits and recurrent trait evolution, provide insight into the processes that generate and maintain organismal diversity. However, rapid radiations also generate particular challenges for inferring the evolutionary history and mechanistic basis of adaptation and speciation, as multiple processes can cause different parts of the genome to have distinct phylogenetic trees. Thus, inferences about the mode and timing of divergence and the causes of parallel trait evolution require a fine-grained understanding of the flow of genomic variation through time. In this study, we used genome-wide sampling of thousands of genes to re-construct the evolutionary histories of a model plant radiation, the monkeyflowers of Mimulus section Erythranthe. Work over the past half-century has established the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated, as are three other species in the section) as textbook examples of both rapid speciation via shifts in pollination syndrome and convergent evolution of floral syndromes. Our phylogenomic analyses re-write both of these stories, placing M. cardinalis in a clade with other hummingbird-pollinated taxa and demonstrating that abundant introgression between ancestral lineages as well as in areas of current sympatry contributes to the real (but misleading) affinities between M. cardinalis and M. lewisii. This work illustrates the pervasive influence of gene flow and introgression during adaptive radiation and speciation, and underlines the necessity of a gene-scale and genome-wide phylogenomics framework for understanding trait divergence, even among well-established species.

scholarly journals A Linear-Time Algorithm for the Isometric Reconciliation of Unrooted Trees

Algorithms ◽  
2020 ◽  
Vol 13 (9) ◽  
pp. 225
Author(s):  
Broňa Brejová ◽  
Rastislav Královič
Keyword(s):  
Family History ◽  
Gene Family ◽  
Phylogenetic Trees ◽  
Evolutionary History ◽  
Linear Time ◽  
Gene Tree ◽  
Time Algorithm ◽  
Species Tree ◽  
Linear Time Algorithm ◽  
History Of

In the reconciliation problem, we are given two phylogenetic trees. A species tree represents the evolutionary history of a group of species, and a gene tree represents the history of a family of related genes within these species. A reconciliation maps nodes of the gene tree to the corresponding points of the species tree, and thus helps to interpret the gene family history. In this paper, we study the case when both trees are unrooted and their edge lengths are known exactly. The goal is to root them and to find a reconciliation that agrees with the edge lengths. We show a linear-time algorithm for finding the set of all possible root locations, which is a significant improvement compared to the previous O(N3logN) algorithm.

scholarly journals Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression

2020 ◽  
Author(s):  
Dan Vanderpool ◽  
Bui Quang Minh ◽  
Robert Lanfear ◽  
Daniel Hughes ◽  
Shwetha Murali ◽  
...  
Keyword(s):  
World Monkey ◽  
Gene Tree ◽  
Species Tree ◽  
Molecular Dating ◽  
Macaca Nemestrina ◽  
Gene Trees ◽  
Individual Gene ◽  
Black And White ◽  
Fossil Evidence ◽  
History Of

AbstractOur understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here we present new reference genome assemblies for three Old World Monkey species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place.

scholarly journals Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression

PLoS Biology ◽  
2020 ◽  
Vol 18 (12) ◽  
pp. e3000954
Author(s):  
Dan Vanderpool ◽  
Bui Quang Minh ◽  
Robert Lanfear ◽  
Daniel Hughes ◽  
Shwetha Murali ◽  
...  
Keyword(s):  
World Monkey ◽  
Gene Tree ◽  
Species Tree ◽  
Molecular Dating ◽  
Macaca Nemestrina ◽  
Gene Trees ◽  
Individual Gene ◽  
Black And White ◽  
Fossil Evidence ◽  
History Of

Our understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here, we present new reference genome assemblies for 3 Old World monkey (OWM) species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place.

scholarly journals Reconstruction of time-consistent species trees

2020 ◽  
Author(s):  
Manuel Lafond ◽  
Marc Hellmuth
Keyword(s):  
Time Complexity ◽  
Gene Tree ◽  
Time Consistency ◽  
Gene Families ◽  
Time Algorithm ◽  
Species Tree ◽  
Gene Trees ◽  
Species Trees ◽  
Evolutionary Event ◽  
History Of

Abstract Background: The history of gene families -- which are equivalent to event-labeled gene trees -- can to some extent be reconstructed from empirically estimated evolutionary event-relations containing pairs of orthologous, paralogous or xenologous genes. The question then arises as whether inferred event-labeled gene trees are "biologically feasible" which is the case if one can find a species tree with which the gene tree can be reconciled in a time-consistent way.Results: In this contribution, we consider event-labeled gene trees that contain speciations, duplications as well as horizontal gene transfer (HGT) and we assume that the species tree is unknown. Although many problems become NP-hard as soon as HGT and time-consistency are involved, we show, in contrast, that the problem of finding a time-consistent species tree for a given event-labeled gene can be solved in polynomial-time. We provide a cubic-time algorithm to decide whether a "time-consistent" species for a given event-labeled gene tree exists and, in the affirmative case, to construct the species tree within the same time-complexity.

scholarly journals Different behaviour of mitochondrial and nuclear markers: introgression and the evolutionary history of Chrysocarabus (Coleoptera: Carabidae)

2006 ◽  
Vol 17 (3) ◽  
Author(s):  
Andreas Düring ◽  
Martina Brückner ◽  
Dietrich Mossakowski
Keyword(s):  
Phylogenetic Trees ◽  
Evolutionary History ◽  
Phylogenetic Analyses ◽  
Mitochondrial Gene ◽  
Gene Tree ◽  
Gene Trees ◽  
Nuclear Markers ◽  
Mitochondrial Haplotypes ◽  
History Of ◽  
Mitochondrial And Nuclear Markers

Phylogenetic analyses of Chrysocarabus taxa using different markers result in different phylogenetic trees. In particular, the mitochondrial gene tree contradicts the results of morphological and inbreeding studies. Two very different haplotypes of Carabus splendens Olivier, 1790 do not form a clade within this phylogenetic tree. We have earlier proposed that contradictory results are due to introgression. To verify our hypothesis, we analysed the internal transcribed spacer 2. No substitutions were observed in these nuclear sequences between the individuals of Carabus splendens, which contain the different mitochondrial haplotypes in question. The differences in the gene trees based on mitochondrial and nuclear sequences can be explained with at least two introgression events.

scholarly journals Inferring Patterns of Hybridization and Polyploidy in the Plant Genus Penstemon (Plantaginaceae)

2020 ◽  
Author(s):  
Paul D. Blischak ◽  
Coleen E. Thompson ◽  
Emiko M. Waight ◽  
Laura S. Kubatko ◽  
Andrea D. Wolfe
Keyword(s):  
Evolutionary History ◽  
Incomplete Lineage Sorting ◽  
Phylogenetic Analyses ◽  
Gene Tree ◽  
The United States ◽  
Gene Trees ◽  
Species Trees ◽  
Ploidy Levels ◽  
Plant Phylogeny ◽  
History Of

AbstractReticulate evolutionary events are hallmarks of plant phylogeny, and are increasingly recognized as common occurrences in other branches of the Tree of Life. However, inferring the evolutionary history of admixed lineages presents a difficult challenge for systematists due to genealogical discordance caused by both incomplete lineage sorting (ILS) and hybridization. Methods that accommodate both of these processes are continuing to be developed, but they often do not scale well to larger numbers of species. An additional complicating factor for many plant species is the occurrence of whole genome duplication (WGD), which can have various outcomes on the genealogical history of haplotypes sampled from the genome. In this study, we sought to investigate patterns of hybridization and WGD in two subsections from the genus Penstemon (Plantaginaceae; subsect. Humiles and Proceri), a speciose group of angiosperms that has rapidly radiated across North America. Species in subsect. Humiles and Proceri occur primarily in the Pacific Northwest of the United States, occupying habitats such as mesic, subalpine meadows, as well as more well-drained substrates at varying elevations. Ploidy levels in the subsections range from diploid to hexaploid, and it is hypothesized that most of the polyploids are hybrids (i.e., allopolyploids). To estimate phylogeny in these groups, we first developed a method for estimating quartet concordance factors (QCFs) from multiple sequences sampled per lineage, allowing us to model all haplotypes from a polyploid. QCFs represent the proportion of gene trees that support a particular species quartet relationship, and are used for species network estimation in the program SNaQ (Solís-Lemus & Ané. 2016. PLoS Genet. 12:e1005896). Using phased haplotypes for nuclear amplicons, we inferred species trees and networks for 38 taxa from P. subsect. Humiles and Proceri. Our phylogenetic analyses recovered two clades comprising a mix of taxa from both subsections, indicating that the current taxonomy for these groups is inconsistent with our estimates of phylogeny. In addition, there was little support for hypotheses regarding the formation of putative allopolyploid lineages. Overall, we found evidence for the effects of both ILS and admixture on the evolutionary history of these species, but were able to evaluate our taxonomic hypotheses despite high levels of gene tree discordance. Our method for estimating QCFs from multiple haplotypes also allowed us to include species of varying ploidy levels in our analyses, which we anticipate will help to facilitate estimation of species networks in other plant groups as well.

scholarly journals Bayes Estimation of Species Divergence Times and Ancestral Population Sizes Using DNA Sequences From Multiple Loci

Genetics ◽  
2003 ◽  
Vol 164 (4) ◽  
pp. 1645-1656 ◽  
Author(s):  
Bruce Rannala ◽  
Ziheng Yang
Keyword(s):  
Dna Sequences ◽  
Gene Tree ◽  
Species Tree ◽  
Bayes Estimation ◽  
Ancestral Population ◽  
Divergence Times ◽  
Gene Trees ◽  
Species Divergence ◽  
Multiple Loci ◽  
Population Sizes

Abstract The effective population sizes of ancestral as well as modern species are important parameters in models of population genetics and human evolution. The commonly used method for estimating ancestral population sizes, based on counting mismatches between the species tree and the inferred gene trees, is highly biased as it ignores uncertainties in gene tree reconstruction. In this article, we develop a Bayes method for simultaneous estimation of the species divergence times and current and ancestral population sizes. The method uses DNA sequence data from multiple loci and extracts information about conflicts among gene tree topologies and coalescent times to estimate ancestral population sizes. The topology of the species tree is assumed known. A Markov chain Monte Carlo algorithm is implemented to integrate over uncertain gene trees and branch lengths (or coalescence times) at each locus as well as species divergence times. The method can handle any species tree and allows different numbers of sequences at different loci. We apply the method to published noncoding DNA sequences from the human and the great apes. There are strong correlations between posterior estimates of speciation times and ancestral population sizes. With the use of an informative prior for the human-chimpanzee divergence date, the population size of the common ancestor of the two species is estimated to be ∼20,000, with a 95% credibility interval (8000, 40,000). Our estimates, however, are affected by model assumptions as well as data quality. We suggest that reliable estimates have yet to await more data and more realistic models.

scholarly journals Phylogenomic Discordance in the Eared Seals is best explained by Incomplete Lineage Sorting following Explosive Radiation in the Southern Hemisphere

2020 ◽  
Author(s):  
Fernando Lopes ◽  
Larissa R Oliveira ◽  
Amanda Kessler ◽  
Yago Beux ◽  
Enrique Crespo ◽  
...  
Keyword(s):  
Incomplete Lineage Sorting ◽  
Gene Tree ◽  
Molecular Data ◽  
Species Tree ◽  
Gene Trees ◽  
Lineage Sorting ◽  
Data Types ◽  
High Coverage ◽  
Sea Lions ◽  
The Family

Abstract The phylogeny and systematics of fur seals and sea lions (Otariidae) have long been studied with diverse data types, including an increasing amount of molecular data. However, only a few phylogenetic relationships have reached acceptance because of strong gene-tree species tree discordance. Divergence times estimates in the group also vary largely between studies. These uncertainties impeded the understanding of the biogeographical history of the group, such as when and how trans-equatorial dispersal and subsequent speciation events occurred. Here we used high-coverage genome-wide sequencing for 14 of the 15 species of Otariidae to elucidate the phylogeny of the family and its bearing on the taxonomy and biogeographical history. Despite extreme topological discordance among gene trees, we found a fully supported species tree that agrees with the few well-accepted relationships and establishes monophyly of the genus Arctocephalus. Our data support a relatively recent trans-hemispheric dispersal at the base of a southern clade, which rapidly diversified into six major lineages between 3 to 2.5 Ma. Otaria diverged first, followed by Phocarctos and then four major lineages within Arctocephalus. However, we found Zalophus to be non-monophyletic, with California (Z. californianus) and Steller sea lions (Eumetopias jubatus) grouping closer than the Galapagos sea lion (Z. wollebaeki) with evidence for introgression between the two genera. Overall, the high degree of genealogical discordance was best explained by incomplete lineage sorting resulting from quasi-simultaneous speciation within the southern clade with introgresssion playing a subordinate role in explaining the incongruence among and within prior phylogenetic studies of the family.

Molecular phylogeny of diploid Hordeum species and incongruence between chloroplast and nuclear datasets

Genome ◽  
2011 ◽  
Vol 54 (12) ◽  
pp. 986-992 ◽  
Author(s):  
Huan Wang ◽  
Dongfa Sun ◽  
Genlou Sun
Keyword(s):  
Evolutionary History ◽  
Nuclear Gene ◽  
Intergenic Spacer ◽  
Molecular Data ◽  
Genome Species ◽  
Different Types ◽  
History Of ◽  
Morphological And Molecular Data ◽  
Hordeum Species ◽  
Eurasian Species

The phylogeny of diploid Hordeum species has been studied using both chloroplast and nuclear gene sequences. However, the studies of different nuclear datasets of Hordeum species often arrived at similar conclusions, whereas the studies of different chloroplast DNA data generally resulted in inconsistent conclusions. Although the monophyly of the genus is well supported by both morphological and molecular data, the intrageneric phylogeny is still a matter of controversy. To better understand the evolutionary history of Hordeum species, two chloroplast gene loci (trnD-trnT intergenic spacer and rps16 gene) and one nuclear marker (thioreoxin-like gene (HTL)) were used to explore the phylogeny of Hordeum species. Two obviously different types of trnD-trnT sequences were observed, with an approximately 210 base pair difference between these two types: one for American species, another for Eurasian species. The trnD-trnT data generally separated the diploid Hordeum species into Eurasian and American clades, with the exception of Hordeum marinum subsp. gussoneanum. The rps16 data also grouped most American species together and suggested that Hordeum flexuosum has a different plastid type from the remaining American species. The nuclear gene HTL data clearly divided Hordeum species into two clades: the Xu + H genome clade and the Xa + I genome clade. Within clades, H genome species were well separated from the Xu species, and the I genome species were well separated from the Xa genome species. The incongruence between chloroplast and nuclear datasets was found and discussed.

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