Multispecies Coalescent Approach Research Articles

The Identification of the Closest Living Relative(s) of Tetrapods: Phylogenomic Lessons for Resolving Short Ancient Internodes.

Identifying the closest living relative(s) of tetrapods is an important, yet still contested question in vertebrate phylogenetics. Three hypotheses are possible and ruling out alternatives has proven difficult even with large molecular data sets due to weak phylogenetic signal coupled nonphylogenetic noise resulting from relatively rapid speciation events that occurred a long time ago ([Formula: see text]400 Ma). Here, we revisit the identity of the closest living relative of land vertebrates from a phylogenomic perspective and include new genomic data for all extant lungfish genera. RNA-seq proves to be a great alternative to genomic sequencing, which currently is technically not feasible in lungfishes due to their huge (50-130 Gb) and repetitive genomes. We examined the most important sources of systematic error, namely long-branch attraction (LBA), compositional heterogeneity and distribution of missing data and applied different correction techniques. A multispecies coalescent approach is used to account for deep coalescence that might come from the short and deep internodes separating early sarcopterygian splits. Concatenation methods favored lungfishes as the closest living relatives of tetrapods with strong statistical support. Amino acid profile mixture models can unambiguously resolve this difficult internode thanks to their ability to avoid systematic error. We assessed the performance of different site-heterogeneous models and data partitioning and compared the ability of different strategies designed to overcome LBA, including taxon manipulation, reduction of among-lineage rate heterogeneity and removal of fast-evolving or compositionally heterogeneous positions. The identification of lungfish as sister group of tetrapods is robust regarding the effects of nonstationary composition and distribution of missing data. The multispecies coalescent method reconstructed strongly supported topologies that were congruent with concatenation, despite pervasive gene tree heterogeneity. We reject alternative topologies for early sarcopterygian relationships by increasing the signal-to-noise ratio in our alignments. The analytical pipeline outlined here combines probabilistic phylogenomic inference with methods for evaluating data quality, model adequacy, and assessing systematic error, and thus is likely to help resolve similarly difficult internodes in the tree of life. [Coalescence; coelacanth; compositional heterogeneity; gene tree; long-branch attraction; lungfish; missing data; model misspecification; phylogenomic; species tree; systematic error.].

North or south? Phylogenetic and biogeographic origins of a globally distributed avian clade

Establishing phylogenetic relationships within a clade can help to infer ancestral origins and indicate how widespread species reached their current biogeographic distributions. The small plovers, genus Charadrius, are cosmopolitan shorebirds, distributed across all continents except Antarctica. Here we present a global, species-level molecular phylogeny of this group based on four nuclear (ADH5, FIB7, MYO2 and RAG1) and two mitochondrial (COI and ND3) genes, and use the phylogeny to examine the biogeographic origin of the genus. A Bayesian multispecies coalescent approach identified two major clades (CRD I and CRD II) within the genus. Clade CRD I contains three species (Thinornis novaeseelandiae, Thinornis rubricollis and Eudromias morinellus), and CRD II one species (Anarhynchus frontalis), that were previously placed outside the Charadrius genus. In contrast to earlier work, ancestral area analyses using parsimony and Bayesian methods supported an origin of the Charadrius plovers in the Northern hemisphere. We propose that major radiations in this group were associated with shifts in the range of these ancestral plover species, leading to colonisation of the Southern hemisphere.

Influence of gene flow on divergence dating - implications for the speciation history of Takydromus grass lizards.

Dating the time of divergence and understanding speciation processes are central to the study of the evolutionary history of organisms but are notoriously difficult. The difficulty is largely rooted in variations in the ancestral population size or in the genealogy variation across loci. To depict the speciation processes and divergence histories of three monophyletic Takydromus species endemic to Taiwan, we sequenced 20 nuclear loci and combined with one mitochondrial locus published in GenBank. They were analysed by a multispecies coalescent approach within a Bayesian framework. Divergence dating based on the gene tree approach showed high variation among loci, and the divergence was estimated at an earlier date than when derived by the species-tree approach. To test whether variations in the ancestral population size accounted for the majority of this variation, we conducted computer inferences using isolation-with-migration (IM) and approximate Bayesian computation (ABC) frameworks. The results revealed that gene flow during the early stage of speciation was strongly favoured over the isolation model, and the initiation of the speciation process was far earlier than the dates estimated by gene- and species-based divergence dating. Due to their limited dispersal ability, it is suggested that geographical isolation may have played a major role in the divergence of these Takydromus species. Nevertheless, this study reveals a more complex situation and demonstrates that gene flow during the speciation process cannot be overlooked and may have a great impact on divergence dating. By using multilocus data and incorporating Bayesian coalescence approaches, we provide a more biologically realistic framework for delineating the divergence history of Takydromus.

Delimiting cryptic pathogen species causing apple Valsa canker with multilocus data.

Fungal diseases are posing tremendous threats to global economy and food safety. Among them, Valsa canker, caused by fungi of Valsa and their Cytospora anamorphs, has been a serious threat to fruit and forest trees and is one of the most destructive diseases of apple in East Asia, particularly. Accurate and robust delimitation of pathogen species is not only essential for the development of effective disease control programs, but also will advance our understanding of the emergence of plant diseases. However, species delimitation is especially difficult in Valsa because of the high variability of morphological traits and in many cases the lack of the teleomorph. In this study, we delimitated species boundary for pathogens causing apple Valsa canker with a multifaceted approach. Based on three independent loci, the internal transcribed spacer (ITS), β-tubulin (Btu), and translation elongation factor-1 alpha (EF1α), we inferred gene trees with both maximum likelihood and Bayesian methods, estimated species tree with Bayesian multispecies coalescent approaches, and validated species tree with Bayesian species delimitation. Through divergence time estimation and ancestral host reconstruction, we tested the possible underlying mechanisms for fungal speciation and host-range change. Our results proved that two varieties of the former morphological species V. mali represented two distinct species, V. mali and V. pyri, which diverged about 5 million years ago, much later than the divergence of their preferred hosts, excluding a scenario of fungi–host co-speciation. The marked different thermal preferences and contrasting pathogenicity in cross-inoculation suggest ecological divergences between the two species. Apple was the most likely ancestral host for both V. mali and V. pyri. Host-range expansion led to the occurrence of V. pyri on both pear and apple. Our results also represent an example in which ITS data might underestimate species diversity.

A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora

The most recent phylogenetic analysis of the genus Phytophthora was completed in 2008 (Blair et al., 2008) and utilized 8.1kb of sequence data from seven nuclear loci. Given the large number of species that have recently been described, this study was undertaken to broaden the available information on the phylogeny of the genus. A total of 166 isolates representing 92 recognized species and 17 provisional species were analyzed, including many of the same isolates used in the nuclear multilocus study of Blair et al. (2008). Four mitochondrial genes (cox2, nad9, rps10 and secY) were sequenced with a total of 2373bp used in the analysis; the species relationships recovered with mitochondrial data were largely consistent with those observed previously in the nuclear analysis. Combining the new mitochondrial data with the nuclear data from Blair et al. (2008) generated a dataset of 10,828bp representing 11 loci, however resolution of basal clade relationships was still low. We therefore implemented a modified multispecies coalescent approach with a subset of the data, and recovered increased resolution and moderate to high support for clade relationships. A more detailed analysis of species from clades 2 and 8 identified an additional seven phylogenetic lineages that warrant further investigation to determine if they represent distinct species. As has been reported in other phylogenetic studies of the genus, there was no consistent correlation between phylogenetic relatedness and morphological features or ecology.

Phylogeny of the Oenanthe lugens complex (Aves, Muscicapidae: Saxicolinae): Paraphyly of a morphologically cohesive group within a recent radiation of open-habitat chats

The morphologically inferred Oenanthe lugens complex comprises nine taxa of open-habitat chats which occur in rocky and/or mountainous areas adjacent to the Saharo-Sindian desert belt. It has traditionally been divided into the lugubris group of north-east Africa, the lugentoides group of the southern part of the Arabian Peninsula and the lugens group of North Africa and the Middle East. Previous molecular phylogenetic studies have shown that the O. lugens complex might not be monophyletic. However, it remained unclear how this result might have been affected by incomplete taxon sampling, as the lugentoides group and two out of three taxa of the lugubris group have not been analyzed so far. In this study, we present a phylogenetic hypothesis of the O. lugens complex based on two mitochondrial genes and one nuclear intron using, for the first time, a complete taxon sampling. The application of a multispecies coalescent approach allowed us to simultaneously estimate the sequence and timing of speciation events. The O. lugens complex was consistently revealed as a polyphyletic assemblage and the traditionally recognized groups should be treated as at least three different species: O. lugens, Oenanthelugubris, and Oenanthelugentoides. While O. lugubris and O. lugentoides were revealed to be sister groups, O. lugens was found to be closely related to the species pair Oenanthechrysopygia/Oenanthexanthoprymna. The latter differ quite strongly in morphology and have traditionally not been associated with members of the lugens complex. We thus corroborate the results of previous studies, which demonstrated that morphology seems to be a poor predictor of phylogenetic relationships in Oenanthe. In contrast to the mtDNA markers analyzed, it was revealed that differences among taxa were not fixed in the nuclear intron. In the case of the taxa persica of the lugens group, an influence of introgression in autosomal markers cannot be excluded and deserves further study. The three species O. lugens, O. lugubris, and O. lugentoides and their associated taxa comprise a comparatively young radiation, which started to diversify in the Pliocene with major diversification events during the Pleistocene. The different taxa seem to have evolved during periods of increased aridity in isolation in rocky mountainous areas adjacent to hyper arid regions.

Phylogeny and divergence times of Australian Sphenomorphus group skinks (Scincidae, Squamata)

The Australian Sphenomorphus group is a diverse clade (c. 250 species) of scincid lizards (skinks) incorporating more than half of the Australian scincid fauna. Previous phylogenetic analyses of mitochondrial and nuclear gene sequence data for selected Australian Sphenomorphus group scincids have provided support for several morphologically- and ecologically-distinct clades; however, the relationships among these clades are only incompletely resolved. This paper presents a new phylogenetic analysis of the Australian Sphenomorphus group, based on nucleotide sequences for three regions of the mitochondrial genome and four nuclear genes (5645 aligned sites in total). Phylogenies generated using standard concatenation and multi-species coalescent approaches are generally similar, and nearly all conflicting nodes are weakly supported. Monophyly of a number of genera and other (informal) supra-specific taxa, including Calyptotis, Ctenotus, Eremiascincus, Hemiergis, Lerista, Notoscincus, the ‘Eulamprus’ quoyii group, and the ‘Glaphyromorphus’ crassicaudis group is well supported in all analyses. There is significant support for a clade including the ‘Eulamprus’ tenuis group, Gnypetoscincus, and Nangura, and a clade comprising Coeranoscincus, Coggeria, Ophioscincus, and Saiphos receives at least marginal support (posterior probabilities above 0.93). All analyses indicate that Anomalopus is polyphyletic, although topology tests suggest that support for this result is equivocal. Divergence times inferred using relaxed molecular clock methods are consistent with an Oligocene origin of the Australian Sphenomorphus group following trans-oceanic dispersal from Asia. Age estimates for clades distributed primarily in arid habitats (c. 9–17million years) are generally younger than those for clades occurring in mesic environments (c. 15–22million years); however, arid-zone clades are substantially more diverse, including nearly 80% of all Australian Sphenomorphus group scincids. This pattern conforms well with reconstructions of Australian palaeo-environments during the Cenozoic, which indicate a progressive shift from widespread mesic habitats in the Early Miocene (prior to 16Mya) to predominantly arid environments 4–2Mya.

Biogeography of scorpions in thePseudouroctonus minimuscomplex (Vaejovidae) from south‐western North America: implications of ecological specialization for pre‐Quaternary diversification

AbstractAimThe aim of this study was to assess the impact of pre‐Quaternary tectonics and orogeny relative to that of Pleistocene climate change on diversification within thePseudouroctonus minimuscomplex, a group of vaejovid scorpions with stenotopic habitat requirements.LocationSouth‐western North America (United States and Mexico).MethodsMultilocus sequence data (1899 base pairs from two mitochondrial and two nuclear genes) were generated from 65 samples of scorpions in theminimuscomplex. Phylogeographical structure within theminimuscomplex was explored using model‐based phylogenetic methods and a general mixed Yule coalescent model to identify independent geographical clusters. A time‐calibrated multilocus species tree was reconstructed using a multispecies coalescent approach. Ancestral areas were estimated at divergence events across the tree using a probabilistic Bayesian approach.ResultsExtensive geographical structure was evident within two well‐supported clades. These clades probably diverged over 25 million years ago (Ma), based on estimated mean divergence dates, followed by 14 divergences in the Miocene (25–5 Ma) and 4 divergences in the Pliocene and Pleistocene (< 5 Ma). The ancestral origin of theminimuscomplex was reconstructed to be across California and the Mexican Highlands. The Chihuahuan Desert was colonized twice from the Mexican Highlands, and one dispersal event occurred from the Mexican Highlands back to California.Main conclusionsSpatial and temporal patterns of evolution in theminimuscomplex support predictions that stenotopy promoted pre‐Quaternary diversification. Miocene and Pliocene geomorphology, perhaps in concert with climate change, induced allopatric divergence across the heterogeneous landscape of south‐western North America. Stenotopic scorpions such as theminimuscomplex provide a model for exploring correlations between Earth history and biological diversification.

Species tree estimation for the late blight pathogen, Phytophthora infestans, and close relatives.

To better understand the evolutionary history of a group of organisms, an accurate estimate of the species phylogeny must be known. Traditionally, gene trees have served as a proxy for the species tree, although it was acknowledged early on that these trees represented different evolutionary processes. Discordances among gene trees and between the gene trees and the species tree are also expected in closely related species that have rapidly diverged, due to processes such as the incomplete sorting of ancestral polymorphisms. Recently, methods have been developed for the explicit estimation of species trees, using information from multilocus gene trees while accommodating heterogeneity among them. Here we have used three distinct approaches to estimate the species tree for five Phytophthora pathogens, including P. infestans, the causal agent of late blight disease in potato and tomato. Our concatenation-based “supergene” approach was unable to resolve relationships even with data from both the nuclear and mitochondrial genomes, and from multiple isolates per species. Our multispecies coalescent approach using both Bayesian and maximum likelihood methods was able to estimate a moderately supported species tree showing a close relationship among P. infestans, P. andina, and P. ipomoeae. The topology of the species tree was also identical to the dominant phylogenetic history estimated in our third approach, Bayesian concordance analysis. Our results support previous suggestions that P. andina is a hybrid species, with P. infestans representing one parental lineage. The other parental lineage is not known, but represents an independent evolutionary lineage more closely related to P. ipomoeae. While all five species likely originated in the New World, further study is needed to determine when and under what conditions this hybridization event may have occurred.

Molecular phylogenetics of Hydatellaceae (Nymphaeales): Sexual‐system homoplasy and a new sectional classification

Species relationships are unknown in Hydatellaceae, a small family of dwarf aquatics related to water lilies that arose near the base of angiosperm phylogeny. Here we use molecular evidence to infer a species tree for the family and apply this to reconstructing major transitions in morphology and sexual system in this early branch of angiosperms. We assembled plastid (atpB, matK, ndhF, rbcL) and nuclear (ribosomal ITS) data for 50 samples (including outgroups) and estimated a species tree for Hydatellaceae using a Bayesian multispecies coalescent approach. We reconstructed the evolution of several morphological characters, then tested for associations between sexual system and reproductive morphology using phylogenetic ANOVA. Dioecious species of Hydatellaceae have significantly greater stamen number and anther length than do cosexual species, suggesting changes in male function. The perennial habit that defines one subclade likely represents a reversion from annuality. Species relationships do not fall along traditional morphological divisions, but new sections proposed here are supported by fruit and seed synapomorphies. The earliest split in the family is reflected in geography and climate (i.e., tropical vs. subtropical/temperate clades). We found limited evidence of incongruence between plastid and nuclear trees, with one exception involving gene-tree nonmonophyly for two close relatives (Trithuria submersa, T. bibracteata). While the direction of sexual-system evolution is ambiguous, transitions are significantly associated with changes in involucral phyllome length and proxies of pollen production. We propose a new sectional circumscription based on fruit, seed, and DNA evidence.

The phylogenetic placement of sinipercid fishes (“Perciformes”) revealed by 11 nuclear loci

Sinipercids are freshwater fishes from East Asia assigned to the genera Siniperca (8–9 species) and Coreoperca (3 species). Although supported as a monophyletic group, the phylogenetic placement of sinipercids among percomorph fishes and the identification of their closest relatives have perplexed generations of taxonomists. Here, we collect and analyze new molecular evidence from 11 nuclear genes – six of them novel markers developed for this study – sampled from seven sinipercid species and several closely-related species that have been proposed as their putative sister taxa in the past. The concatenated alignment of the 11 loci included 10,560 bp that were split into 18 blocks for a partitioned analysis using Bayesian and Maximum Likelihood methods. Both approaches resulted in nearly identical topologies, in which the monophyly of the sinipercids was strongly supported (Bootstrap Support = 99; Posterior Probability = 1.0) with Centrarchidae as their sister taxon (BS = 87; PP = 1.0). Percichthyidae formed a sister group to the sinipercid–centrarchid clade (BS = 100; PP = 1.0). Tests for alternative hypotheses of relationships significantly rejected the placement of sinipercids within the Serranidae, Moronidae, or Centropomidae, or as sister taxon to Lateolabrax japonicus, Perca flavescens, or Pristigenys alta (SH test, p < 0.001,). The contribution of individual gene genealogies to support this result was explored further using a multispecies coalescent approach (BEST) to infer the species phylogeny. The sister-group relationship with Centrarchidae also is supported by this approach but relationships among species within the genus Siniperca showed a different pattern than the results obtained with the concatenated data set. Our study supports the designation of a distinct family, Sinipercidae, for this group of fishes ( Siniperca and Coreoperca).