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Mol Phylogenet Evol [journal]
- Phylogenetic Analysis at Deep Timescales: Unreliable Gene Trees, Bypassed Hidden Support, and the Coalescence/Concatalescence Conundrum. [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 21.
Large datasets that include many taxa and many genes are required to solve difficult phylogenetic problems that are deep in the Tree of Life. Currently, two divergent systematic methods are applicable and commonly applied to such datasets: the traditional supermatrix approach (= concatenation) and "shortcut" coalescence methods (= coalescence methods wherein gene trees and the species tree are not co-estimated). When applied to ancient clades, these contrasting frameworks often produce congruent results, but in recent phylogenetic analyses of Placentalia (placental mammals), this is not the case, with proponents of coalescence arguing that their novel approach robustly supports several interordinal clades that have resisted consistent resolution using standard concatenation methods. A recent series of papers has alternatively disputed and defended the utility of shortcut coalescence methods at deep phylogenetic scales (Meredith et al., 2011; Song et al., 2012; Gatesy and Springer, 2013; Wu et al., 2013; Zhong et al., 2013, 2014; Springer and Gatesy, 2014). Here, we examine this exchange in the context of published phylogenomic data from Mammalia (183 loci; McCormack et al., 2012); in particular we explore two critical and related issues - the delimitation of data partitions ("genes") in coalescence analysis and hidden support that emerges with the combination of such partitions in phylogenetic studies. Hidden support - increased support for a clade in combined analysis of all data partitions relative to the support evident in separate analyses of the various data partitions, is a hallmark of the supermatrix approach and a primary rationale for concatenating all characters into a single matrix. In the most extreme cases of hidden support, relationships that are contradicted by all gene trees are supported when all of the genes are analyzed together. A valid fear is that shortcut coalescence methods might bypass or distort character support that is hidden in individual loci because small gene fragments are analyzed in isolation. Given the extensive database of molecular, phenotypic, and fossil data for Mammalia, the assumptions and applicability of shortcut coalescence methods can be assessed with rigor to complement a small but growing body of simulation work that has directly compared these methods to concatenation. We document several remarkable cases of hidden support in both supermatrix and coalescence paradigms and argue that in most instances, the emergent support in the shortcut coalescence analyses is an artifact. By referencing rigorous molecular clock studies of Mammalia, we suggest that inaccurate gene trees that imply unrealistically deep coalescences debilitate shortcut coalescence analyses of the placental dataset. We document contradictory coalescence results for Placentalia, and outline a critical conundrum that challenges the general utility of shortcut coalescence methods at deep phylogenetic scales. In particular, the basic unit of analysis in coalescence analysis, the coalescence-gene (a minimal non-recombining stretch of aligned genomes) is expected to shrink in size as more taxa are analyzed, but as the amount of data for reconstruction of a gene tree ratchets downward, the number of nodes in the gene tree that need to be resolved ratchets upward. One possible solution to this inevitable equation is to concatenate multiple coalescence-genes to yield "gene trees" that better match the species tree. However, this hybrid concatenation/coalescence approach, "concatalescence," contradicts the most basic biological rationale for performing a coalescence analysis in the first place. We discuss this reality in the context of recent simulation work that also suggests inaccurate reconstruction of gene trees is more problematic for shortcut coalescence methods than deep coalescence of independently segregating loci is for concatenation methods.
- Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa. [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 21.
Animals and fungi independently evolved from the protozoan phylum Choanozoa, these three groups constituting a major branch of the eukaryotic evolutionary tree known as opisthokonts. Opisthokonts and the protozoan phylum Amoebozoa (amoebae plus slime moulds) were previously argued to have evolved independently from the little-studied, largely flagellate, protozoan phylum, Sulcozoa. Sulcozoa are a likely evolutionary link between opisthokonts and the more primitive excavate flagellates that have ventral feeding grooves and the most primitive known mitochondria. To extend earlier sparse evidence for the ancestral (paraphyletic) nature of Sulcozoa, we sequenced transcriptomes from six gliding flagellates (two apusomonads; three planomonads; Mantamonas). Phylogenetic analyses of 173-192 genes and 73-122 eukaryote-wide taxa show Sulcozoa as deeply paraphyletic, confirming that opisthokonts and Amoebozoa independently evolved from sulcozoans by losing their ancestral ventral groove and dorsal pellicle: Apusozoa (apusomonads plus anaerobic breviate amoebae) are robustly sisters to opisthokonts and probably paraphyletic, breviates diverging before apusomonads; Varisulca (planomonads, Mantamonas, and non-gliding flagellate Collodictyon) are sisters to opisthokonts plus Apusozoa and Amoebozoa, and possibly holophyletic; Glissodiscea (planomonads, Mantamonas) may be holophyletic, but Mantamonas sometimes groups with Collodictyon instead. Taxon and gene sampling slightly affects tree topology; for the closest branches in Sulcozoa and opisthokonts, proportionally reducing missing data eliminates conflicts between homogeneous-model maximum-likelihood trees and evolutionarily more realistic site-heterogeneous trees. Sulcozoa, opisthokonts, and Amoebozoa constitute an often-pseudopodial 'podiate' clade, one of only three eukaryotic 'supergroups'. Our trees indicate that evolution of sulcozoan dorsal pellicle, ventral pseudopodia, and ciliary gliding (probably simultaneously) generated podiate eukaryotes from Malawimonas-like excavate flagellates.
- Multigene phylogeny resolves deep branching of Amoebozoa. [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 20.
Amoebozoa is a key phylum for eukaryote phylogeny and evolutionary history, but its phylogenetic validity has been questioned since included species are very diverse: amoebo-flagellate slime-moulds, naked and testate amoebae, and some flagellates. 18S rRNA gene trees have not firmly established its internal topology. To rectify this we sequenced cDNA libraries for seven diverse Amoebozoa and conducted phylogenetic analyses for 109 eukaryotes (17-18 Amoebozoa) using 60-188 genes. We conducted Bayesian inferences with the evolutionarily most realistic site-heterogeneous CAT-GTR model and maximum likelihood analyses. These unequivocally establish the monophyly of Amoebozoa, showing a primary dichotomy between the previously contested subphyla Lobosa and Conosa. Lobosa, the entirely non-flagellate lobose amoebae, are robustly partitioned into the monophyletic classes Tubulinea, with predominantly tube-shaped pseudopodia, and Discosea with flattened cells and different locomotion. Within Conosa 60/70-gene trees with very little missing data show a primary dichotomy between the aerobic infraphylum Semiconosia (Mycetozoa and Variosea) and secondarily anaerobic Archamoebae. These phylogenetic features are entirely congruent with the most recent major amoebozoan classification emphasising locomotion modes, pseudopodial morphology, and ultrastructure. However, 188-gene trees where proportionally more taxa have sparser gene-representation weakly place Archamoebae as sister to Macromycetozoa instead, possibly a tree reconstruction artefact of differentially missing data.
- Tracing the Evolution of FERM domain of Kindlins. [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 19.
Kindlin proteins represent a novel family of evolutionarily conserved FERM domain containing proteins (FDCPs) and are members of B4.1 superfamily. Kindlins consist of three conserved protein homologs in vertebrates: Kindlin-1, Kindlin-2 and Kindlin-3. All three homologs are associated with focal adhesions and are involved in integrin activation. FERM domain of each Kindlin is bipartite and plays a key role in integrin activation. A single ancestral Kindlin protein can be traced back to earliest metazoans, e.g., to Parazoa. This protein underwent multiple rounds of duplication in vertebrates, leading to the present Kindlin family. In this study, we trace phylogenetic and evolutionary history of Kindlin FERM domain with respect to FERM domain of other FDCPs. We show that FERM domain in Kindlin homologs is conserved among Kindlins but amount of conservation is less in comparison with FERM domain of other members in B4.1 superfamily. Furthermore, insertion of Pleckstrin Homology like domain in Kindlin FERM domain has important evolutionary and functional consequences. Important residues in Kindlins are traced and ranked according to their evolutionary significance. The structural and functional significance of high ranked residues is highlighted and validated by their known involvement in Kindlin associated diseases. In light of these findings, we hypothesize that FERM domain originated from a proto-Talin protein in unicellular or proto-multicellular organism and advent of multi-cellularity was accompanied by burst of FDCPs, which supported multi-cellularity functions required for complex organisms. This study helps in developing a better understanding of evolutionary history of FERM domain of FDCPs and the role of FERM domain in metazoan evolution.
- When everything converges: Integrative taxonomy with shell, DNA and venomic data reveals Conus conco, a new species of cone snails (Gastropoda: Conoidea). [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 13.
Cone snails have long been studied both by taxonomists for the diversity of their shells and by biochemists for the potential therapeutic applications of their toxins. Phylogenetic approaches have revealed that different lineages of Conus evolved divergent venoms, a property that is exploited to enhance the discovery of new conotoxins, but is rarely used in taxonomy. Specimens belonging to the Indo-West Pacific Conus lividus species complex were analyzed using phenetic and phylogenetic methods based on shell morphology, COI and 28S rRNA gene sequences and venom mRNA expression and protein composition. All methods converged to reveal a new species, C. conco n. sp. (described in Supplementary data), restricted to the Marquesas Islands, where it diverged recently (∼3mya) from C. lividus. The geographical distribution of C. conco and C. lividus and their phylogenetic relationships suggest that the two species diverged in allopatry. Furthermore, the diversity of the transcript sequences and toxin molecular masses suggest that C. conco evolved unique toxins, presumably in response to new selective pressure, such as the availability of new preys and ecological niches. Furthermore, this new species evolved new transcripts giving rise to original toxin structures, probably each carrying specific biological activity.
- Mitochondrial genomes reveal the pattern and timing of marten (Martes), wolverine (Gulo), and fisher (Pekania) diversification. [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 12.
Despite recent advances in understanding the pattern and timescale of evolutionary diversification in the marten, wolverine, fisher, and tayra subfamily Guloninae (Mustelidae, Carnivora), several important issues still remain contentious. Among these are the phylogenetic position of Gulo relative to the subgenera of Martes (Martes and Charronia), the phylogenetic relationships within the subgenus Martes, and the timing of gulonine divergences. To elucidate these issues we explored nucleotide variation in 11 whole mitochondrial genomes (mitogenomes) from eight gulonine species and two outgroup meline species. Parsimony, maximum likelihood, and Bayesian phylogenetic analyses yielded fully resolved and identical patterns of relationships with high support for all divergences. The generic status of Pekania (P. pennanti), the monophyly of the genus Martes containing M. flavigula (subgenus Charronia) to the exclusion of the genus Gulo (G. gulo), and the M. foina (M. americana (M. melampus (M. zibellina, M. martes))) phylogeny of the subgenus Martes were strongly supported. Dating analyses (BEAST) using a set of five newly applied fossil calibrations provided divergence times considerably younger than previous multigene mitochondrial estimates, but similar to multigene nuclear and nuclear-mitochondrial estimates. The 95% confidence (highest posterior density) intervals of our divergence times fell within those inferred from nuclear and nuclear-mitochondrial sequence data, and were markedly narrower than in earlier studies (whether nuclear, mitochondrial, or combined). Notably, and contrary to long-held beliefs, our findings indicate that fossils older than the Tortonian-Messinian transition (late Late Miocene) do not represent Martes, excluding from this genus its putative members from the Early, Middle, and early Late Miocene. This study demonstrates the high informativeness of the mitogenome for phylogenetic inference and divergence time estimation within Guloninae, and suggests that mitogenomes can be highly informative also for other clades at similar levels of evolutionary divergence.
- Metapopulations in temporary streams - The role of drought-flood cycles in promoting high genetic diversity in a critically endangered freshwater fish and its consequences for the future. [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 12.
Genetic factors have direct and indirect impacts in the viability of endangered species. Assessing their genetic diversity levels and population structure is thus fundamental for conservation and management. In this paper we use mitochondrial and nuclear markers to address phylogeographic and demographic data on the critically endangered Anaecypris hispanica, using a broad sampling set which covered its known distribution area in the Iberian Peninsula. Our results showed that the populations of A. hispanica are strongly differentiated (high and significant ФST and FST values, corroborated by the results from AMOVA and SAMOVA) and genetically diversified. We suggest that the restricted gene flow between populations may have been potentiated by ecological, hydrological and anthropogenic causes. Bayesian skyline plots revealed a signal for expansion for all populations (tMRCA between 68kya and 1.33Mya) and a genetic diversity latitudinal gradient was detected between the populations from the Upper (more diversified) and the Lower (less diversified) Guadiana river basin. We postulate a Pleistocenic westwards colonization route for A. hispanica in the Guadiana river basin, which is in agreement with the tempo and mode of paleoevolution of this drainage. The colonization of River Guadalquivir around 60kya with migrants from the Upper Guadiana, most likely by stream capture, is also suggested. This study highlights the view that critically endangered species facing range retreats (about 47% of its known populations have disappeared in the last 15years) are not necessarily small and genetically depleted. However, the extinction risk is not negligible since A. hispanica faces the combined effect of several deterministic and stochastic negative factors and, moreover, recolonization events after localized extinctions are very unlikely to occur due to the strong isolation of populations and to the patchily ecologically-conditioned distribution of fish. The inferred species distribution models highlight the significant contribution of temperature seasonality and isothermality to A. hispanica occurrence in Guadiana environments and emphasize the importance of stable climatic conditions for the preservation of this species. Given the strong population structure, high percentage of private haplotypes and virtual absence of inter-basin gene flow we suggest that each A. hispanica population should be considered as an independent Operational Conservation Unit and that ex-situ and in-situ actions should be conducted in parallel to allow for the long-term survival of the species and the preservation of the genetic integrity of its populations.
- Reconstructing the colonization history of lost wolf lineages by the analysis of the mitochondrial genome. [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 12.
The grey wolves (Canis lupus) originally inhabited major parts of the Northern hemisphere, but many local populations became extinct. Two lineages of wolves in Japan, namely, Japanese or Honshu (C. l. hodophilax) and Ezo or Hokkaido (C. l. hattai) wolves, rapidly went extinct between 100 and 120years ago. Here we analyse the complete mitochondrial genome sequences from ancient specimens and reconstruct the colonization history of the two extinct subspecies. We show a unique status of Japanese wolves in wolf phylogeny, suggesting their long time separation from other grey wolf populations. Japanese wolves appeared to have colonized the Japanese archipelago in the Late Pleistocene (ca. 25,000-125,000years ago). By contrast, Ezo wolves, which are clearly separated from Japanese wolves in phylogeny, are likely to have arrived at Japan relatively recently (<14,000years ago). Interestingly, their colonization history to Japan tallies well with the dynamics of wolf populations in Europe and America during the last several millennia. Our analyses suggest that at least several thousands of wolves once inhabited in the Japanese archipelago. Our analyses also show that an enigmatic clade of domestic dogs is likely to have originated from rare admixture events between male dogs and female Japanese wolves.
- Delphinid systematics and biogeography with a focus on the current genus Lagenorhynchus: Multiple pathways for antitropical and trans-oceanic radiation. [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 15.
The six species currently classified within the genus Lagenorhynchus exhibit a pattern of antitropical distribution common among marine taxa. In spite of their morphological similarities they are now considered an artificial grouping, and include both recent and the oldest representatives of the Delphinidae radiation. They are, therefore, a good model for studying questions about the evolutionary processes that have driven dolphin speciation, dispersion and distribution. Here we used two different approaches. First we constructed a multigenic phylogeny with a minimum amount of missing data (based on 9 genes, 11,030bp, using the 6 species of the genus and their closest relatives) to infer their relationships. Second, we built a supermatrix phylogeny (based on 33 species and 27 genes) to test the effect of taxon sampling on the phylogeny of the genus, to provide inference on biogeographic history, and provide inference on the main events shaping the dispersion and radiation of delphinids. Our analyses suggested an early evolutionary history of marine dolphins in the North Atlantic Ocean and revealed multiple pathways of migration and radiation, probably guided by paleoceanographic changes during the Miocene and Pliocene. L. acutus and L. albirostris likely shared a common ancestor that arose in the North Atlantic around the Middle Miocene, predating the radiation of subfamilies Delphininae, Globicephalinae and Lissodelphininae.
- Should genes with missing data be excluded from phylogenetic analyses? [JOURNAL ARTICLE]
- Mol Phylogenet Evol 2014 Aug 11.
Phylogeneticists often design their studies to maximize the number of genes included but minimize the overall amount of missing data. However, few studies have addressed the costs and benefits of adding characters with missing data, especially for likelihood analyses of multiple loci. In this paper, we address this topic using two empirical data sets (in yeast and plants) with well-resolved phylogenies. We introduce varying amounts of missing data into varying numbers of genes and test whether the benefits of excluding genes with missing data outweigh the costs of excluding the non-missing data that are associated with them. We also test if there is a proportion of missing data in the incomplete genes at which they cease to be beneficial or harmful, and whether missing data consistently bias branch length estimates. Our results indicate that adding incomplete genes generally increases the accuracy of phylogenetic analyses relative to excluding them, especially when there is a high proportion of incomplete genes in the overall dataset (and thus few complete genes). Detailed analyses suggest that adding incomplete genes is especially helpful for resolving poorly supported nodes. Given that we find that excluding genes with missing data often decreases accuracy relative to including these genes (and that decreases are generally of greater magnitude than increases), there is little basis for assuming that excluding these genes is necessarily the safer or more conservative approach. We also find no evidence that missing data consistently bias branch length estimates.