High-Throughput Sequencing of 5S-IGS rDNA in Fagus L. (Fagaceae) reveals complex evolutionary patterns and hybrid origin of modern species

Standard models of speciation assume strictly dichotomous genealogies in which a species, the ancestor, is replaced by two offspring species. The reality is more complex: plant species can evolve from other species via isolation when genetic drift exceeds gene flow; lineage mixing can give rise to new species (hybrid taxa such as nothospecies and allopolyploids). The multi–copy, potentially multi–locus 5S rDNA is one of few gene regions conserving signal from dichotomous and reticulate evolutionary processes down to the level of intra-genomic recombination. Here, we provide the first high-throughput sequencing (HTS) 5S intergenic spacer (5S – IGS) data for a lineage of wind-pollinated subtropical to temperate trees, the Fagus crenata – F. sylvatica s.l. lineage, and its distant relative F. japonica. The observed 4,963 unique 5S – IGS variants reflect a long history of repeated incomplete lineage sorting and lineage mixing since the early Cenozoic of two or more paralogous-homoeologous 5S rDNA lineages. Extant species of Fagus are genetic mosaics and, at least to some part, of hybrid origin.

Download Full-text

Robustness of RADseq for evolutionary network reconstruction from gene trees

10.1101/414243 ◽

2018 ◽

Author(s):

José Luis Blanco-Pastor ◽

Yann J.K. Bertrand ◽

Isabel María Liberal ◽

Yanling Wei ◽

E.Charles Brummer ◽

...

Keyword(s):

High Throughput Sequencing ◽

Incomplete Lineage Sorting ◽

Molecular Data ◽

Hybrid Origin ◽

Gene Trees ◽

Lineage Sorting ◽

Network Analyses ◽

Evolutionary Network ◽

Complex Patterns ◽

Evolutionary Networks

AbstractAlthough hybridization has played an important role in the evolution of many species, phylogenetic reconstructions that include hybridizing lineages have been historically constrained by the available models and data. Recently, the combined development of high-throughput sequencing and evolutionary network models offer new opportunities for phylogenetic inference under complex patterns of hybridization in the context of incomplete lineage sorting. Restriction site associated DNA sequencing (RADseq) has been a popular sequencing technique for evolutionary reconstructions of close relatives in the Next Generation Sequencing (NGS) era. However, the utility of RADseq data for the reconstruction of complex evolutionary networks has not been thoroughly discussed. Here, we used new molecular data collected from diploid perennial Medicago species using single-digest RADseq to reconstruct evolutionary networks from gene trees, an approach that is computationally tractable with datasets that include several species and complex patterns of hybridization. Our analyses revealed that complex network reconstructions from RADseq-derived gene trees were not robust under variations of the assembly parameters and filters. Filters to exclusively select loci with high phylogenetic information created datasets that retrieved the most anomalous topologies. Conversely, alternative clustering thresholds or filters on the number of samples per locus affected the level of missing data but had a lower impact on networks. When most anomalous networks were discarded, all remaining network analyses consistently supported a hybrid origin for M. carstiensis and M. cretacea.

Download Full-text

Hybridization preceded radiation in diploid wheats

10.1101/599068 ◽

2019 ◽

Author(s):

Stella Huynh ◽

Thomas Marcussen ◽

François Felber ◽

Christian Parisod

Keyword(s):

High Throughput Sequencing ◽

Incomplete Lineage Sorting ◽

Phylogenetic Analyses ◽

Reticulate Evolution ◽

Hybrid Origin ◽

Lineage Sorting ◽

D Genome ◽

B Genome ◽

Tree Compression ◽

A Genome

SummaryEvolutionary relationships among theAegilops-Triticumrelatives of cultivated wheats have been difficult to resolve owing to incomplete lineage sorting and reticulate evolution. Recent studies have suggested that the wheat D-genome lineage (progenitor ofAe. tauschii) originated through homoploid hybridization between the A-genome lineage (progenitor ofTriticums.str.) and the B-genome lineage (progenitor ofAe. speltoides). Scenarios of reticulation have been debated, calling for adequate phylogenetic analyses based on comprehensive sampling. To reconstruct the evolution ofAegilops-Triticumdiploids, we here combined high-throughput sequencing of 38 nuclear low-copy loci of multiple accessions of all 13 species with inferences of the species phylogeny using the full-parameterized MCMC_SEQ method. Phylogenies recovered a monophyleticAegilops-Triticumlineage that began diversifying ~6.5 Ma ago and gave rise to four sublineages, i.e. the A- (2 species), B- (1 species), D- (9 species) and T- (Ae. mutica) genome lineage. Full-parameterized phylogenies as well as patterns of tree dilation and tree compression supported a hybrid origin of the D-genome lineage from A and B ~4.1 Ma ago, and did not indicate additional hybridization events. This comprehensive and dated phylogeny of wheat relatives indicates that the origin of the hybrid D-genome was followed by intense diversification into almost all diploid as well as allopolyploid wild wheats.

Download Full-text

Interrogating Phylogenetic Discordance Resolves Deep Splits in the Rapid Radiation of Old World Fruit Bats (Chiroptera: Pteropodidae)

Systematic Biology ◽

10.1093/sysbio/syab013 ◽

2021 ◽

Author(s):

Nicolas Nesi ◽

Georgia Tsagkogeorga ◽

Susan M Tsang ◽

Violaine Nicolas ◽

Aude Lalis ◽

...

Keyword(s):

Information Content ◽

Incomplete Lineage Sorting ◽

Gene Tree ◽

Fruit Bats ◽

Lineage Sorting ◽

Protein Coding ◽

Old World ◽

Nectar Feeding ◽

Extant Species ◽

Evolutionary Distinctiveness

Abstract The family Pteropodidae (Old World fruit bats) comprises $>$200 species distributed across the Old World tropics and subtropics. Most pteropodids feed on fruit, suggesting an early origin of frugivory, although several lineages have shifted to nectar-based diets. Pteropodids are of exceptional conservation concern with $>$50% of species considered threatened, yet the systematics of this group has long been debated, with uncertainty surrounding early splits attributed to an ancient rapid diversification. Resolving the relationships among the main pteropodid lineages is essential if we are to fully understand their evolutionary distinctiveness, and the extent to which these bats have transitioned to nectar-feeding. Here we generated orthologous sequences for $>$1400 nuclear protein-coding genes (2.8 million base pairs) across 114 species from 43 genera of Old World fruit bats (57% and 96% of extant species- and genus-level diversity, respectively), and combined phylogenomic inference with filtering by information content to resolve systematic relationships among the major lineages. Concatenation and coalescent-based methods recovered three distinct backbone topologies that were not able to be reconciled by filtering via phylogenetic information content. Concordance analysis and gene genealogy interrogation show that one topology is consistently the best supported, and that observed phylogenetic conflicts arise from both gene tree error and deep incomplete lineage sorting. In addition to resolving long-standing inconsistencies in the reported relationships among major lineages, we show that Old World fruit bats have likely undergone at least seven independent dietary transitions from frugivory to nectarivory. Finally, we use this phylogeny to identify and describe one new genus. [Chiroptera; coalescence; concordance; incomplete lineage sorting; nectar feeder; species tree; target enrichment.]

Download Full-text

Embracing heterogeneity: Building the Tree of Life and the future of phylogenomics

10.7287/peerj.preprints.26449 ◽

2018 ◽

Author(s):

Gustavo A Bravo ◽

Alexandre Antonelli ◽

Christine D Bacon ◽

Krzysztof Bartoszek ◽

Mozes Blom ◽

...

Keyword(s):

Large Scale ◽

High Throughput Sequencing ◽

Incomplete Lineage Sorting ◽

Tree Of Life ◽

Lineage Sorting ◽

Modern Biology ◽

Multispecies Coalescent ◽

The Many ◽

Genomic Signals ◽

Character Mapping

Building the Tree of Life (ToL) is a major challenge of modern biology, requiring major advances in cyberinfrastructure, data collection, theory, and more. Here, we argue that phylogenomics stands to benefit by embracing the many heterogeneous genomic signals emerging from the first decade of large-scale phylogenetic analysis spawned by High-throughput sequencing (HTS). Such signals include those most commonly encountered in phylogenomic datasets, such as incomplete lineage sorting, but also those reticulate processes emerging with greater frequency, such as recombination and introgression. We suggest that methods of data acquisition and the types of markers used in phylogenomics will remain restricted until a posteriori methods of marker choice are made possible with routine whole-genome sequencing of taxa of interest. We discuss limitations and potential extensions of a major model supporting innovation in phylogenomics today, the multispecies coalescent model. Macroevolutionary models that use phylogenies, such as character mapping, often ignore the heterogeneity on which building phylogenies increasingly rely, and suggest that assimilating such heterogeneity is an important goal moving forward. Finally, we argue that an integrative cyberinfrastructure linking all steps of the process of building the ToL, from specimen acquisition in the field to publication and tracking of phylogenomic data, as well as a culture that values contributors to each step, are essential for progress.

Download Full-text

Target enrichment improves phylogenetic resolution in the genus Zanthoxylum (Rutaceae) and indicates both incomplete lineage sorting and hybridization events

10.1101/2021.04.12.439519 ◽

2021 ◽

Author(s):

Niklas Reichelt ◽

Jun Wen ◽

Claudia Paetzold ◽

Marc Appelhans

Keyword(s):

High Throughput Sequencing ◽

Incomplete Lineage Sorting ◽

Phylogenetic Analyses ◽

Gene Tree ◽

Single Copy ◽

Reticulate Evolution ◽

Gene Trees ◽

Target Enrichment ◽

Lineage Sorting ◽

Phylogenetic Resolution

Background and aims: Zanthoxylum L. is the only pantropical genus within Rutaceae, with a few species native to temperate eastern Asia and North America. Efforts using Sanger sequencing failed to resolve the backbone phylogeny of Zanthoxylum. In this study, we employed target enrichment high-throughput sequencing to improve resolution. Gene trees were examined for concordance and sectional classifications of Zanthoxylum were evaluated. Off-target reads were investigated to identify putative single-copy markers for bait refinement, and low-copy markers for evidence of putative hybridization events. Methods: We developed a custom bait set for target enrichment of 745 exons in Zanthoxylum and applied it to 45 Zanthoxylum species and one Tetradium species as the outgroup. Illumina reads were processed via the HybPhyloMaker pipeline. Phylogenetic inferences were conducted using coalescent and concatenated methods. Concordance was assessed using quartet sampling. Off-target reads were assembled and putative single- and low-copy genes were extracted. Additional phylogenetic analyses were performed based on these alignments. Key results: Four major clades are supported within Zanthoxylum: the African clade, the Z. asiaticum clade, the Asian-Pacific-Australian clade, and the American-eastern Asian clade. While overall support has improved, regions of conflict are similar to those previously observed. Gene tree discordances indicate a hybridization event in the ancestor of the Hawaiian lineage, and incomplete lineage sorting for the American backbone. Off-target putative single-copy genes largely confirm on-target results, and putative low-copy genes provide additional evidence for hybridization in the Hawaiian lineage. Only two of the five sections of Zanthoxylum are resolved as monophyletic. Conclusion: Target enrichment is suitable to assess phylogenetic relationships in Zanthoxylum. Our phylogenetic analyses reveal that current sectional classifications need revision. Quartet tree concordance indicates several instances of reticulate evolution. Off-target reads are proven useful to identify additional phylogenetically informative regions for bait refinement or gene tree based approaches.

Download Full-text

The Legacy of Recurrent Introgression during the Radiation of Hares

Systematic Biology ◽

10.1093/sysbio/syaa088 ◽

2020 ◽

Author(s):

Mafalda S Ferreira ◽

Matthew R Jones ◽

Colin M Callahan ◽

Liliana Farelo ◽

Zelalem Tolesa ◽

...

Keyword(s):

Incomplete Lineage Sorting ◽

Introgressive Hybridization ◽

Lineage Sorting ◽

Whole Exome ◽

Extant Species ◽

The Last Glacial Maximum ◽

Shared Genetic ◽

The Last Glacial ◽

Shared Variation

Abstract Hybridization may often be an important source of adaptive variation, but the extent and long-term impacts of introgression have seldom been evaluated in the phylogenetic context of a radiation. Hares (Lepus) represent a widespread mammalian radiation of 32 extant species characterized by striking ecological adaptations and recurrent admixture. To understand the relevance of introgressive hybridization during the diversification of Lepus, we analyzed whole exome sequences (61.7 Mb) from 15 species of hares (1- 4 individuals per species), spanning the global distribution of the genus, and two outgroups. We used a coalescent framework to infer species relationships and divergence times, despite extensive genealogical discordance. We found high levels of allele sharing among species and show that this reflects extensive incomplete lineage sorting and temporally layered hybridization. Our results revealed recurrent introgression at all stages along the Lepus radiation, including recent gene flow between extant species since the last glacial maximum, but also pervasive ancient introgression occurring since near the origin of the hare lineages. We show that ancient hybridization between northern hemisphere species has resulted in shared variation of potential adaptive relevance to highly seasonal environments, including genes involved in circadian rhythm regulation, pigmentation, and thermoregulation. Our results illustrate how the genetic legacy of ancestral hybridization may persist across a radiation, leaving a long-lasting signature of shared genetic variation that may contribute to adaptation.

Download Full-text

Phylogeny and evolution of the green lizards, Lacerta spp. (Squamata: Lacertidae) based on mitochondrial and nuclear DNA sequences

Amphibia-Reptilia ◽

10.1163/156853805774408667 ◽

2005 ◽

Vol 26 (3) ◽

pp. 271-285 ◽

Cited By ~ 49

Author(s):

D. James Harris ◽

Nuno Ferrand ◽

Eduardo Crespo ◽

Raquel Godinho

Keyword(s):

Dna Sequences ◽

Phylogenetic Relationships ◽

Nuclear Dna ◽

Incomplete Lineage Sorting ◽

Bird Species ◽

Rrna Genes ◽

12S Rrna ◽

Lineage Sorting ◽

Extant Species ◽

Mitochondrial Cytochrome B

AbstractPartial DNA sequences from three mitochondrial (cytochrome b, 12S rRNA and 16S rRNA) and two nuclear (β-fibrinogen intron 7 and C-mos) genes were used to estimate the phylogenetic relationships among all eight extant species of green lizards, Lacerta sensu stricto, and many currently recognized subspecies. All eight species form a monophyletic group. L. agilis, L. schreiberi and L. strigata are genetically well differentiated species. L. trilineata and L. pamphylica are not monophyletic units based on analyses of the β-fibrinogen intron 7. Lacerta media is closely related to some Lacerta trilineata. L. bilineata and L. viridis are closely related, and recognition of L. bilineata as a distinct species makes L. viridis paraphyletic also. For both L. bilineata and L. viridis, some subspecies appear to remain in their southern glacial refugia, while a single genetic entity shows successfully postglacial expansion. The topology derived from C-mos variation is concordant with that derived from mtDNA, with substitutions occurring at a similar rate to that of transversions in the rRNA genes. Although C-mos is typically used at deeper taxonomic levels it is also phylogenetically informative within green lizards. β-fibrinogen intron 7, typically used for assessing phylogenetic relationships among bird species, is a useful phylogenetic marker for reptiles also, showing considerable variation between species. There is not complete concordance between estimates of relationships derived from the mtDNA and nuclear markers, probably because rapid diversification led to incomplete lineage sorting in the green lizards. Introgression could also be occuring between some species.

Download Full-text

Genome-wide data for effective conservation of manta and devil ray species

10.1101/458141 ◽

2018 ◽

Cited By ~ 5

Author(s):

Jane Hosegood ◽

Emily Humble ◽

Rob Ogden ◽

Mark de Bruyn ◽

Si Creer ◽

...

Keyword(s):

Species Delimitation ◽

High Throughput Sequencing ◽

Incomplete Lineage Sorting ◽

Conservation Strategy ◽

Morphological Observation ◽

Lineage Sorting ◽

Standing Variation ◽

Genome Wide ◽

Genome Wide Data ◽

Effective Conservation

AbstractPractical biodiversity conservation relies on delineation of biologically meaningful units, particularly with respect to global conventions and regulatory frameworks. Traditional approaches have typically relied on morphological observation, resulting in artificially broad delineations and non-optimal species units for conservation. More recently, species delimitation methods have been revolutionised with High-Throughput Sequencing approaches, allowing study of diversity within species radiations using genome-wide data. The highly mobile elasmobranchs, manta and devil rays (Mobulaspp.), are threatened globally by targeted and bycatch fishing pressures resulting in recent protection under several global conventions. However, a lack of global data, morphological similarities, a succession of recent taxonomic changes and ineffectual traceability measures combine to impede development and implementation of a coherent and enforceable conservation strategy. Here, we generate genome-wide Single Nucleotide Polymorphism (SNP) data from among the most globally and taxonomically representative set of mobulid tissues. The resulting phylogeny and delimitation of species units represents the most comprehensive assessment of mobulid diversity with molecular data to date. We find a mismatch between current species classifications, and optimal species units for effective conservation. Specifically, we find robust evidence for an undescribed species of manta ray in the Gulf of Mexico and show that species recently synonymised are reproductively isolated. Further resolution is achieved at the population level, where cryptic diversity is detected in geographically distinct populations, and indicates potential for future traceability work determining regional location of catch. We estimate the optimal species tree and uncover substantial incomplete lineage sorting, where standing variation in extinct ancestral populations is identified as a driver of phylogenetic uncertainty, with further conservation implications. Our study provides a framework for molecular genetic species delimitation that is relevant to wide-ranging taxa of conservation concern, and highlights the potential for genomic data to support effective management, conservation and law enforcement strategies.

Download Full-text

Phylogenomics supported by geometric morphometrics reveals delimitation of sexual species within the polyploid apomictic Ranunculus auricomus complex (Ranunculaceae)

10.1101/2020.01.07.896902 ◽

2020 ◽

Cited By ~ 1

Author(s):

Kevin Karbstein ◽

Salvatore Tomasello ◽

Ladislav Hodac ◽

Franz G. Dunkel ◽

Mareike Daubert ◽

...

Keyword(s):

Geometric Morphometrics ◽

Incomplete Lineage Sorting ◽

Hybrid Origin ◽

Target Enrichment ◽

Lineage Sorting ◽

Data Set ◽

Geometric Morphometric ◽

Genetic Lineages ◽

Sexual Species ◽

Species Complexes

AbstractSpecies are the basic units of biodiversity and evolution. Nowadays, they are widely considered as ancestor-descendant lineages. Their definition remains a persistent challenge for taxonomists due to lineage evolutionary role and circumscription, i.e., persistence in time and space, ecological niche or a shared phenotype of a lineage. Recognizing and delimiting species is particularly methodically challenging in fast-evolving, evolutionary young species complexes often characterized by low genetic divergence, hybrid origin, introgression and incomplete lineage sorting (ILS). Ranunculus auricomus is a large Eurasian apomictic polyploid complex that probably has arisen from the hybridization of a few sexual progenitor species. However, even delimitation and relationships of diploid sexual progenitors have been unclearly ranging from two to twelve species. Here, we present an innovative workflow combining phylogenomic methods based on 86,782 parameter-optimized RADseq loci and target enrichment of 663 nuclear genes together with geometric morphometrics to delimit sexual species in this evolutionary young complex (< 1 Mya). For the first time, we revealed a fully resolved and well-supported maximum likelihood (ML) tree phylogeny congruent to neighbor-net network and STRUCTURE results based on RADseq data. In a few clades, we found evidence of discordant patterns indicated by quartet sampling (QS) and reticulation events in the neighbor-net network probably caused by introgression and ILS. Together with coalescent-based species delimitation approaches based on target enrichment data, we found five main genetic lineages, with an allopatric distribution in Central and Southern Europe. A concatenated geometric morphometric data set including basal and stem leaves, as well as receptacles, revealed the same five main clusters. We accept those five morphologically differentiated, geographically isolated, genetic main lineages as species: R. cassubicifolius s.l. (incl. R. carpaticola), R. flabellifolius, R. envalirensis s.l. (incl. R. cebennensis), R. marsicus and R. notabilis s.l. (incl. R. austroslovenicus, R. calapius, R. mediocompositus, R. peracris and R. subcarniolicus). Our comprehensive workflow combing phylogenomic methods supported by geometric morphometrics proved to be successful in delimiting closely related sexual taxa and applying an evolutionary species concept, which is also transferable to other evolutionarily young species complexes.

Download Full-text