“Jack‐of‐all‐trades” is parthenogenetic

Sex is evolutionarily more costly than parthenogenesis, evolutionary ecologists therefore wonder why sex is much more frequent than parthenogenesis in the majority of animal lineages. Intriguingly, parthenogenetic individuals and species are as common as or even more common than sexuals in some major and putative ancient animal lineages such as oribatid mites and rotifers. Here, we analyzed oribatid mites (Acari: Oribatida) as a model group because these mites are ancient (early Paleozoic), widely distributed around the globe, and include a high number of parthenogenetic species, which often co‐exist with sexual oribatid mite species. There is evidence that the reproductive mode is phylogenetically conserved in oribatid mites, which makes them an ideal model to test hypotheses on the relationship between reproductive mode and species'' ecological strategies. We used oribatid mites to test the frozen niche variation hypothesis; we hypothesized that parthenogenetic oribatid mites occupy narrow specialized ecological niches. We used the geographic range of species as a proxy for specialization as specialized species typically do have narrower geographic ranges than generalistic species. After correcting for phylogenetic signal in reproductive mode and demonstrating that geographic range size has no phylogenetic signal, we found that parthenogenetic lineages have a higher probability to have broader geographic ranges than sexual species arguing against the frozen niche variation hypothesis. Rather, the results suggest that parthenogenetic oribatid mite species are more generalistic than sexual species supporting the general‐purpose genotype hypothesis. The reason why parthenogenetic oribatid mite species are generalists with wide geographic range sizes might be that they are of ancient origin reflecting that they adapted to varying environmental conditions during evolutionary history. Overall, our findings indicate that parthenogenetic oribatid mite species possess a widely adapted general‐purpose genotype and therefore might be viewed as “Jack‐of‐all‐trades.”     

Rheostat functional outcomes occur when substitutions are introduced at nonconserved positions that diverge with speciation

When amino acids vary during evolution, the outcome can be functionally neutral or biologically‐important. We previously found that substituting a subset of nonconserved positions, “rheostat” positions, can have surprising effects on protein function. Since changes at rheostat positions can facilitate functional evolution or cause disease, more examples are needed to understand their unique biophysical characteristics. Here, we explored whether “phylogenetic” patterns of change in multiple sequence alignments (such as positions with subfamily specific conservation) predict the locations of functional rheostat positions. To that end, we experimentally tested eight phylogenetic positions in human liver pyruvate kinase (hLPYK), using 10–15 substitutions per position and biochemical assays that yielded five functional parameters. Five positions were strongly rheostatic and three were non‐neutral. To test the corollary that positions with low phylogenetic scores were not rheostat positions, we combined these phylogenetic positions with previously‐identified hLPYK rheostat, “toggle” (most substitution abolished function), and “neutral” (all substitutions were like wild‐type) positions. Despite representing 428 variants, this set of 33 positions was poorly statistically powered. Thus, we turned to the in vivo phenotypic dataset for E. coli lactose repressor protein (LacI), which comprised 12–13 substitutions at 329 positions and could be used to identify rheostat, toggle, and neutral positions. Combined hLPYK and LacI results show that positions with strong phylogenetic patterns of change are more likely to exhibit rheostat substitution outcomes than neutral or toggle outcomes. Furthermore, phylogenetic patterns were more successful at identifying rheostat positions than were co‐evolutionary or eigenvector centrality measures of evolutionary change.     

Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis

For more than a century, the origin of metazoan animals has been debated. One aspect of this debate has been centered on what the hypothetical “urmetazoon” bauplan might have been. The morphologically most simply organized metazoan animal, the placozoan Trichoplax adhaerens, resembles an intriguing model for one of several “urmetazoon” hypotheses: the placula hypothesis. Clear support for a basal position of Placozoa would aid in resolving several key issues of metazoan-specific inventions (including, for example, head–foot axis, symmetry, and coelom) and would determine a root for unraveling their evolution. Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question. Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa. Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized “urmetazoon” hypothesis.     

Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis

For more than a century, the origin of metazoan animals has been debated. One aspect of this debate has been centered on what the hypothetical “urmetazoon” bauplan might have been. The morphologically most simply organized metazoan animal, the placozoan Trichoplax adhaerens, resembles an intriguing model for one of several “urmetazoon” hypotheses: the placula hypothesis. Clear support for a basal position of Placozoa would aid in resolving several key issues of metazoan-specific inventions (including, for example, head–foot axis, symmetry, and coelom) and would determine a root for unraveling their evolution. Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question. Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa. Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized “urmetazoon” hypothesis.     

Evolution of Pentameric Ligand-Gated Ion Channels: Pro-Loop Receptors

Pentameric ligand-gated ion channels (pLGICs) are ubiquitous neurotransmitter receptors in Bilateria, with a small number of known prokaryotic homologues. Here we describe a new inventory and phylogenetic analysis of pLGIC genes across all kingdoms of life. Our main finding is a set of pLGIC genes in unicellular eukaryotes, some of which are metazoan-like Cys-loop receptors, and others devoid of Cys-loop cysteines, like their prokaryotic relatives. A number of such “Cys-less” receptors also appears in invertebrate metazoans. Together, those findings draw a new distribution of pLGICs in eukaryotes. A broader distribution of prokaryotic channels also emerges, including a major new archaeal taxon, Thaumarchaeota. More generally, pLGICs now appear nearly ubiquitous in major taxonomic groups except multicellular plants and fungi. However, pLGICs are sparsely present in unicellular taxa, suggesting a high rate of gene loss and a non-essential character, contrasting with their essential role as synaptic receptors of the bilaterian nervous system. Multiple alignments of these highly divergent sequences reveal a small number of conserved residues clustered at the interface between the extracellular and transmembrane domains. Only the “Cys-loop” proline is absolutely conserved, suggesting the more fitting name “Pro loop” for that motif, and “Pro-loop receptors” for the superfamily. The infered molecular phylogeny shows a Cys-loop and a Cys-less clade in eukaryotes, both containing metazoans and unicellular members. This suggests new hypotheses on the evolutionary history of the superfamily, such as a possible origin of the Cys-loop cysteines in an ancient unicellular eukaryote. Deeper phylogenetic relationships remain uncertain, particularly around the split between bacteria, archaea, and eukaryotes.     

Predicting protein function with hierarchical phylogenetic profiles: the Gene3D Phylo-Tuner method applied to eukaryotic genomes

“Phylogenetic profiling” is based on the hypothesis that during evolution functionally or physically interacting genes are likely to be inherited or eliminated in a codependent manner. Creating presence–absence profiles of orthologous genes is now a common and powerful way of identifying functionally associated genes. In this approach, correctly determining orthology, as a means of identifying functional equivalence between two genes, is a critical and nontrivial step and largely explains why previous work in this area has mainly focused on using presence–absence profiles in prokaryotic species. Here, we demonstrate that eukaryotic genomes have a high proportion of multigene families whose phylogenetic profile distributions are poor in presence–absence information content. This feature makes them prone to orthology mis-assignment and unsuited to standard profile-based prediction methods. Using CATH structural domain assignments from the Gene3D database for 13 complete eukaryotic genomes, we have developed a novel modification of the phylogenetic profiling method that uses genome copy number of each domain superfamily to predict functional relationships. In our approach, superfamilies are subclustered at ten levels of sequence identity—from 30% to 100%—and phylogenetic profiles built at each level. All the profiles are compared using normalised Euclidean distances to identify those with correlated changes in their domain copy number. We demonstrate that two protein families will “auto-tune” with strong co-evolutionary signals when their profiles are compared at the similarity levels that capture their functional relationship. Our method finds functional relationships that are not detectable by the conventional presence–absence profile comparisons, and it does not require a priori any fixed criteria to define orthologous genes.     

Reproductive phenology of Melastomataceae species with contrasting reproductive systems: contemporary and historical drivers

• Flowering and fruiting are key events in the life history of plants, and both are critical to their reproductive success. Besides the role of evolutionary history, plant reproductive phenology is regulated by abiotic factors and shaped by biotic interactions with pollinators and seed dispersers. In Melastomataceae, a dominant Neotropical family, the reproductive systems vary from allogamous with biotic pollination to apomictic, and seed dispersal varies from dry (self‐dispersed) to fleshy (animal‐dispersed) fruits. Such variety in reproductive strategies is likely to affect flowering and fruiting phenologies.
• In this study, we described the reproductive phenology of 81 Melastomataceae species occurring in two biodiversity hotspots: the Atlantic rain forest and the campo rupestre. We aim to disentangle the role of abiotic and biotic factors defining flowering and fruiting times of Melastomataceae species, considering the contrasting breeding and seed dispersal systems, and their evolutionary history.
• In both vegetation types, pollinator‐dependent species had higher flowering seasonality than pollinator‐independent ones. Flowering patterns presented phylogenetic signal regardless of vegetation type. Fruiting of fleshy‐fruited species was seasonal in campo rupestre but not in Atlantic rain forest; the fruiting of dry‐fruited species was also not seasonal in both vegetation types. Fruiting showed a low phylogenetic signal, probably because the influence of environment and dispersal agents on fruiting time is stronger than the phylogenetic affinity.
• Considering these ecophylogenetic patterns, our results indicate that flowering may be shaped by the different reproductive strategies of Melastomataceae lineages, while fruiting patterns may be governed mainly by the seed dispersal strategy and flowering time, with less phylogenetic influence.

     

“Candidatus Midichloriaceae” fam. nov. (Rickettsiales), an Ecologically Widespread Clade of Intracellular Alphaproteobacteria

“Candidatus Midichloria mitochondrii” is an intramitochondrial bacterium of the order Rickettsiales associated with the sheep tick Ixodes ricinus. Bacteria phylogenetically related to “Ca. Midichloria mitochondrii” (midichloria and like organisms [MALOs]) have been shown to be associated with a wide range of hosts, from amoebae to a variety of animals, including humans. Despite numerous studies focused on specific members of the MALO group, no comprehensive phylogenetic and statistical analyses have so far been performed on the group as a whole. Here, we present a multidisciplinary investigation based on 16S rRNA gene sequences using both phylogenetic and statistical methods, thereby analyzing MALOs in the overall framework of the Rickettsiales. This study revealed that (i) MALOs form a monophyletic group; (ii) the MALO group is structured into distinct subgroups, verifying current genera as significant evolutionary units and identifying several subclades that could represent novel genera; (iii) the MALO group ranks at the level of described Rickettsiales families, leading to the proposal of the novel family “Candidatus Midichloriaceae.” In addition, based on the phylogenetic trees generated, we present an evolutionary scenario to interpret the distribution and life history transitions of these microorganisms associated with highly divergent eukaryotic hosts: we suggest that aquatic/environmental protista have acted as evolutionary reservoirs for members of this novel family, from which one or more lineages with the capacity of infecting metazoa have evolved.     

The Independent Evolution Method Is Not a Viable Phylogenetic Comparative Method

Phylogenetic comparative methods (PCMs) use data on species traits and phylogenetic relationships to shed light on evolutionary questions. Recently, Smaers and Vinicius suggested a new PCM, Independent Evolution (IE), which purportedly employs a novel model of evolution based on Felsenstein’s Adaptive Peak Model. The authors found that IE improves upon previous PCMs by producing more accurate estimates of ancestral states, as well as separate estimates of evolutionary rates for each branch of a phylogenetic tree. Here, we document substantial theoretical and computational issues with IE. When data are simulated under a simple Brownian motion model of evolution, IE produces severely biased estimates of ancestral states and changes along individual branches. We show that these branch-specific changes are essentially ancestor-descendant or “directional” contrasts, and draw parallels between IE and previous PCMs such as “minimum evolution”. Additionally, while comparisons of branch-specific changes between variables have been interpreted as reflecting the relative strength of selection on those traits, we demonstrate through simulations that regressing IE estimated branch-specific changes against one another gives a biased estimate of the scaling relationship between these variables, and provides no advantages or insights beyond established PCMs such as phylogenetically independent contrasts. In light of our findings, we discuss the results of previous papers that employed IE. We conclude that Independent Evolution is not a viable PCM, and should not be used in comparative analyses.     

Inference of Transposable Element Ancestry

Most common methods for inferring transposable element (TE) evolutionary relationships are based on dividing TEs into subfamilies using shared diagnostic nucleotides. Although originally justified based on the “master gene” model of TE evolution, computational and experimental work indicates that many of the subfamilies generated by these methods contain multiple source elements. This implies that subfamily-based methods give an incomplete picture of TE relationships. Studies on selection, functional exaptation, and predictions of horizontal transfer may all be affected. Here, we develop a Bayesian method for inferring TE ancestry that gives the probability that each sequence was replicative, its frequency of replication, and the probability that each extant TE sequence came from each possible ancestral sequence. Applying our method to 986 members of the newly-discovered LAVA family of TEs, we show that there were far more source elements in the history of LAVA expansion than subfamilies identified using the CoSeg subfamily-classification program. We also identify multiple replicative elements in the AluSc subfamily in humans. Our results strongly indicate that a reassessment of subfamily structures is necessary to obtain accurate estimates of mutation processes, phylogenetic relationships and historical times of activity.     

Abstract Profiles of Structural Stability Point to Universal Tendencies,Family-Specific Factors,and Ancient Connections between Languages

Language is the best example of a cultural evolutionary system, able to retain a phylogenetic signal over many thousands of years. The temporal stability (conservatism) of basic vocabulary is relatively well understood, but the stability of the structural properties of language (phonology, morphology, syntax) is still unclear. Here we report an extensive Bayesian phylogenetic investigation of the structural stability of numerous features across many language families and we introduce a novel method for analyzing the relationships between the “stability profiles” of language families. We found that there is a strong universal component across language families, suggesting the existence of universal linguistic, cognitive and genetic constraints. Against this background, however, each language family has a distinct stability profile, and these profiles cluster by geographic area and likely deep genealogical relationships. These stability profiles seem to show, for example, the ancient historical relationships between the Siberian and American language families, presumed to be separated by at least 12,000 years, and possible connections between the Eurasian families. We also found preliminary support for the punctuated evolution of structural features of language across families, types of features and geographic areas. Thus, such higher-level properties of language seen as an evolutionary system might allow the investigation of ancient connections between languages and shed light on the peopling of the world.     

Human Quadrupeds,Primate Quadrupedalism,and Uner Tan Syndrome

Since 2005, an extensive literature documents individuals from several families afflicted with “Uner Tan Syndrome (UTS),” a condition that in its most extreme form is characterized by cerebellar hypoplasia, loss of balance and coordination, impaired cognitive abilities, and habitual quadrupedal gait on hands and feet. Some researchers have interpreted habitual use of quadrupedalism by these individuals from an evolutionary perspective, suggesting that it represents an atavistic expression of our quadrupedal primate ancestry or “devolution.” In support of this idea, individuals with “UTS” are said to use diagonal sequence quadrupedalism, a type of quadrupedal gait that distinguishes primates from most other mammals. Although the use of primate-like quadrupedal gait in humans would not be sufficient to support the conclusion of evolutionary “reversal,” no quantitative gait analyses were presented to support this claim. Using standard gait analysis of 518 quadrupedal strides from video sequences of individuals with “UTS”, we found that these humans almost exclusively used lateral sequence–not diagonal sequence–quadrupedal gaits. The quadrupedal gait of these individuals has therefore been erroneously described as primate-like, further weakening the “devolution” hypothesis. In fact, the quadrupedalism exhibited by individuals with UTS resembles that of healthy adult humans asked to walk quadrupedally in an experimental setting. We conclude that quadrupedalism in healthy adults or those with a physical disability can be explained using biomechanical principles rather than evolutionary assumptions.     

The Natural History of Biocatalytic Mechanisms

Phylogenomic analysis of the occurrence and abundance of protein domains in proteomes has recently showed that the α/β architecture is probably the oldest fold design. This holds important implications for the origins of biochemistry. Here we explore structure-function relationships addressing the use of chemical mechanisms by ancestral enzymes. We test the hypothesis that the oldest folds used the most mechanisms. We start by tracing biocatalytic mechanisms operating in metabolic enzymes along a phylogenetic timeline of the first appearance of homologous superfamilies of protein domain structures from CATH. A total of 335 enzyme reactions were retrieved from MACiE and were mapped over fold age. We define a mechanistic step type as one of the 51 mechanistic annotations given in MACiE, and each step of each of the 335 mechanisms was described using one or more of these annotations. We find that the first two folds, the P-loop containing nucleotide triphosphate hydrolase and the NAD(P)-binding Rossmann-like homologous superfamilies, were α/β architectures responsible for introducing 35% (18/51) of the known mechanistic step types. We find that these two oldest structures in the phylogenomic analysis of protein domains introduced many mechanistic step types that were later combinatorially spread in catalytic history. The most common mechanistic step types included fundamental building blocks of enzyme chemistry: “Proton transfer,” “Bimolecular nucleophilic addition,” “Bimolecular nucleophilic substitution,” and “Unimolecular elimination by the conjugate base.” They were associated with the most ancestral fold structure typical of P-loop containing nucleotide triphosphate hydrolases. Over half of the mechanistic step types were introduced in the evolutionary timeline before the appearance of structures specific to diversified organisms, during a period of architectural diversification. The other half unfolded gradually after organismal diversification and during a period that spanned ∼2 billion years of evolutionary history.     

Analysis of P-Loop and its Flanking Region Subsequence of Diverse NTPases Reveals Evolutionary Selected Residues

The P-loop NTPases are involved in diverse cellular functions. Members of the P-loop NTPase superfamily are characterized by presence of a highly conserved sequence pattern GxxxxGKS/T, known as Walker A motif. This motif adopts an archetypal P-loop conformation which allows accommodation of the triphosphate moiety of a bound nucleotide. Despite the presence of Walker A as a common sequence motif, P-loop NTPases exhibit extreme sequence divergence which hampers their phylogenetic or evolutionary classification. Here, we show that P-loop and its flanking region subsequence (termed as “extended-WalkerA motif”) contain distinct signatures that can be utilized to classify NTPase domain of functionally diverse proteins. We find a clearly classified group of diverse NTPases of Conserved Domain Database such as G-proteins, Ylqf, RecA like, DExDc, AAA, CPT, NK, ABC transporter and NifH proteins.     

Functional diversity of small-mammal postcrania is linked to both substrate preference and body size

Selective pressures favor morphologies that are adapted to distinct ecologies, resulting in trait partitioning among ecomorphotypes. However, the effects of these selective pressures vary across taxa, especially because morphology is also influenced by factors such as phylogeny, body size, and functional trade-offs. In this study, we examine how these factors impact functional diversification in mammals. It has been proposed that trait partitioning among mammalian ecomorphotypes is less pronounced at small body sizes due to biomechanical, energetic, and environmental factors that favor a “generalist” body plan, whereas larger taxa exhibit more substantial functional adaptations. We title this the Divergence Hypothesis (DH) because it predicts greater morphological divergence among ecomorphotypes at larger body sizes. We test DH by using phylogenetic comparative methods to examine the postcranial skeletons of 129 species of taxonomically diverse, small-to-medium-sized (<15 kg) mammals, which we categorize as either “tree-dwellers” or “ground-dwellers.” In some analyses, the morphologies of ground-dwellers and tree-dwellers suggest greater between-group differentiation at larger sizes, providing some evidence for DH. However, this trend is neither particularly strong nor supported by all analyses. Instead, a more pronounced pattern emerges that is distinct from the predictions of DH: within-group phenotypic disparity increases with body size in both ground-dwellers and tree-dwellers, driven by morphological outliers among “medium”-sized mammals. Thus, evolutionary increases in body size are more closely linked to increases in within-locomotor-group disparity than to increases in between-group disparity. We discuss biomechanical and ecological factors that may drive these evolutionary patterns, and we emphasize the significant evolutionary influences of ecology and body size on phenotypic diversity.     

Systematic Identification of Gene Families for Use as “Markers” for Phylogenetic and Phylogeny-Driven Ecological Studies of Bacteria and Archaea and Their Major Subgroups

With the astonishing rate that genomic and metagenomic sequence data sets are accumulating, there are many reasons to constrain the data analyses. One approach to such constrained analyses is to focus on select subsets of gene families that are particularly well suited for the tasks at hand. Such gene families have generally been referred to as “marker” genes. We are particularly interested in identifying and using such marker genes for phylogenetic and phylogeny-driven ecological studies of microbes and their communities (e.g., construction of species trees, phylogenetic based assignment of metagenomic sequence reads to taxonomic groups, phylogeny-based assessment of alpha- and beta-diversity of microbial communities from metagenomic data). We therefore refer to these as PhyEco (for phylogenetic and phylogenetic ecology) markers. The dual use of these PhyEco markers means that we needed to develop and apply a set of somewhat novel criteria for identification of the best candidates for such markers. The criteria we focused on included universality across the taxa of interest, ability to be used to produce robust phylogenetic trees that reflect as much as possible the evolution of the species from which the genes come, and low variation in copy number across taxa.We describe here an automated protocol for identifying potential PhyEco markers from a set of complete genome sequences. The protocol combines rapid searching, clustering and phylogenetic tree building algorithms to generate protein families that meet the criteria listed above. We report here the identification of PhyEco markers for different taxonomic levels including 40 for “all bacteria and archaea”, 114 for “all bacteria (greatly expanding on the ∼30 commonly used), and 100 s to 1000 s for some of the individual phyla of bacteria. This new list of PhyEco markers should allow much more detailed automated phylogenetic and phylogenetic ecology analyses of these groups than possible previously.     

Source-Sink Colonization as a Possible Strategy of Insects Living in Temporary Habitats

Continuous colonization and re-colonization is critical for survival of insect species living in temporary habitats. When insect populations in temporary habitats are depleted, some species may escape extinction by surviving in permanent, but less suitable habitats, in which long-term population survival can be maintained only by immigration from other populations. Such situation has been repeatedly described in nature, but conditions when and how this occurs and how important this phenomenon is for insect metapopulation survival are still poorly known, mainly because it is difficult to study experimentally. Therefore, we used a simulation model to investigate, how environmental stochasticity, growth rate and the incidence of dispersal affect the positive effect of permanent but poor (“sink”) habitats on the likelihood of metapopulation persistence in a network of high quality but temporary (“source”) habitats. This model revealed that permanent habitats substantially increase the probability of metapopulation persistence of insect species with poor dispersal ability if the availability of temporary habitats is spatio-temporally synchronized. Addition of permanent habitats to a system sometimes enabled metapopulation persistence even in cases in which the metapopulation would otherwise go extinct, especially for species with high growth rates. For insect species with low growth rates the probability of a metapopulation persistence strongly depended on the proportions of “source” to “source” and “sink” to “source” dispersal rates.     

Fast-Evolving Mitochondrial DNA in Ceriantharia: A Reflection of Hexacorallia Paraphyly?

The low evolutionary rate of mitochondrial genes in Anthozoa has challenged their utility for phylogenetic and systematic purposes, especially for DNA barcoding. However, the evolutionary rate of Ceriantharia, one of the most enigmatic “orders” within Anthozoa, has never been specifically examined. In this study, the divergence of mitochondrial DNA of Ceriantharia was compared to members of other Anthozoa and Medusozoa groups. In addition, nuclear markers were used to check the relative phylogenetic position of Ceriantharia in relation to other Cnidaria members. The results demonstrated a pattern of divergence of mitochondrial DNA completely different from those estimated for other anthozoans, and phylogenetic analyses indicate that Ceriantharia is not included within hexacorallians in most performed analyses. Thus, we propose that the Ceriantharia should be addressed as a separate clade.