Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts

A dynamic continuum exists from free-living environmental microbes to strict host-associated symbionts that are vertically inherited. However, knowledge of the forces that drive transitions in symbiotic lifestyle and transmission mode is lacking. Arsenophonus is a diverse clade of bacterial symbionts, comprising reproductive parasites to coevolving obligate mutualists, in which the predominant mode of transmission is vertical. We describe a symbiosis between a member of the genus Arsenophonus and the Western honey bee. The symbiont shares common genomic and predicted metabolic properties with the male-killing symbiont Arsenophonus nasoniae, however we present multiple lines of evidence that the bee Arsenophonus deviates from a heritable model of transmission. Field sampling uncovered spatial and seasonal dynamics in symbiont prevalence, and rapid infection loss events were observed in field colonies and laboratory individuals. Fluorescent in situ hybridisation showed Arsenophonus localised in the gut, and detection was rare in screens of early honey bee life stages. We directly show horizontal transmission of Arsenophonus between bees under varying social conditions. We conclude that honey bees acquire Arsenophonus through a combination of environmental exposure and social contacts. These findings uncover a key link in the Arsenophonus clades trajectory from free-living ancestral life to obligate mutualism, and provide a foundation for studying transitions in symbiotic lifestyle.Subject terms: Microbial ecology, Molecular evolution, Bacterial evolution, Bacterial genetics, Phylogenetics     

Phylogeny and adaptive radiation within the Anomopoda: a preliminary exploration

The distinctness of the Anomopoda and the polyphyletic nature of the so-called Cladocera are emphasized.An attempt is made to reconstruct the ancestral anomopod, which probably lived in Palaeozoic times. This task is facilitated by the availability of detailed information on extant forms, which includes functional as well as purely morphological considerations and enables us to understand the means whereby complex mechanisms were transformed during evolution. Comparative studies on the ecology and habits of extant forms also throw light on the probable way of life of the ancestral anomopod.Adaptive radiation within the Anomopoda is briefly surveyed and an outline of the suggested phylogeny of the order is indicated.Institute of Environmental and Biological Sciences, University of Lancaster     

Phylogeny of replication initiator protein TrfA reveals a highly divergent clade of incompatibility group P1 plasmids

Incompatibility group P1 (IncP-1) plasmid diversity was evaluated based on replication initiator protein (TrfA) phylogeny. A new and highly divergent clade was identified. Replication assays indicated that TrfA of recently discovered IncP-1 plasmids from Xylella fastidiosa and Verminephrobacter eiseniae initiated plasmid replication using cognate or heterologous origins of replication.     

Aldehyde dehydrogenases: widespread structural and functional diversity within a shared framework.

Sequences of 16 NAD and/or NADP-linked aldehyde oxidoreductases are aligned, including representative examples of all aldehyde dehydrogenase forms with wide substrate preferences as well as additional types with distinct specificities for certain metabolic aldehyde intermediates, particularly semialdehydes, yielding pairwise identities from 15 to 83%. Eleven of 23 invariant residues are glycine and three are proline, indicating evolutionary restraint against alteration of peptide chain-bending points. Additionally, another 66 positions show high conservation of residue type, mostly hydrophobic residues. Ten of these occur in predicted beta-strands, suggesting important interior-packing interactions. A single invariant cysteine residue is found, further supporting its catalytic role. A previously identified essential glutamic acid residue is conserved in all but methyl malonyl semialdehyde dehydrogenase, which may relate to formation by that enzyme of a CoA ester as a product rather than a free carboxylate species. Earlier, similarity to a GXGXXG segment expected in the NAD-binding site was noted from alignments with fewer sequences. The same region continues to be indicated, although now only the first glycine residue is strictly conserved and the second (usually threonine) is not present at all, suggesting greater variance in coenzyme-binding interactions.     

Communality in microbial stress response and differential metabolic interactions revealed by time-series analysis of sponge symbionts

The diversity and function of sponge-associated symbionts is now increasingly understood; however, we lack an understanding of how they dynamically behave to ensure holobiont stability in the face of environmental variation. Here, we performed a metatransciptomic analysis on three microbial symbionts of the sponge Cymbastela concentrica in situ over 14 months and through differential gene expression and correlation analysis to environmental variables uncovered differences that speak to their metabolic activities and level of symbiotic and environmental interactions. The nitrite-oxidizing Ca. Porinitrospira cymbastela maintained a seemingly stable metabolism, with the few differentially expressed genes related only to stress responses. The heterotrophic Ca. Porivivens multivorans displayed differential use of holobiont-derived compounds and respiration modes, while the ammonium-oxidizing archaeon Ca. Nitrosopumilus cymbastelus differentially expressed genes related to phosphate metabolism and symbiosis effectors. One striking similarity between the symbionts was their similar variation in expression of stress-related genes. Our time-series study showed that the microbial community of C. concentrica undertakes dynamic gene expression adjustments in response to the surroundings, tuned to deal with general stress and metabolic interactions between holobiont members. The success of these dynamic adjustments likely underpins the stability of the sponge holobiont and may provide resilience against environmental change.     

Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution

Background  

The genus Arsenophonus is a group of symbiotic, mainly insect-associated bacteria with rapidly increasing number of records. It is known from a broad spectrum of hosts and symbiotic relationships varying from parasitic son-killers to coevolving mutualists.     

Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively eusocial clade of bees (Hymenoptera: Halictidae)

We performed a phylogenetic analysis of the species, species groups, and subgenera within the predominantly eusocial lineage of Lasioglossum (the Hemihalictus series) based on three protein coding genes: mitochondrial cytochrome oxidase I, nuclear elongation factor 1alpha and long-wavelength rhodopsin. The entire data set consisted of 3421 aligned nucleotide sites, 854 of which were parsimony informative. Analyses by equal weights parsimony, maximum likelihood, and Bayesian methods yielded good resolution among the 53 taxa/populations, with strong bootstrap support and high posterior probabilities for most nodes. There was no significant incongruence among genes, and parsimony, maximum likelihood, and Bayesian methods yielded congruent results. We mapped social behavior onto the resulting tree for 42 of the taxa/populations to infer the likely history of social evolution within Lasioglossum. Our results indicate that eusociality had a single origin within Lasioglossum. Within the predominantly eusocial clade, however, there have been multiple (six) reversals from eusociality to solitary nesting, social polymorphism, or social parasitism, suggesting that these reversals may be more common in primitively eusocial Hymenoptera than previously anticipated. Our results support the view that eusociality is hard to evolve but easily lost. This conclusion is potentially important for understanding the early evolution of the advanced eusocial insects, such as ants, termites, and corbiculate bees.     

Multiple Ig-like featuring genes divergent within and among individuals of the marine sponge Geodia cydonium

The receptor tyrosine kinase of the marine sponge Geodia cydonium features two extracellular Ig-like domains in which we recently documented RT-PCR polymorphism among individuals. Genomic-PCR analysis presented here revealed 14 unique sequences from four sponges, differing predominantly in the sequence of an intron which splits the Ig-like domains. Nevertheless, analysis of putative coding regions in 19 distinct clones (156–159 aa) from seven sponges revealed 69 positions of nucleotide substitutions, 67.6% of them non-synonymous, translating into 43 positions of divergent residues. Excluding aa deletions, these 19 sequences share pairwise aa identities of 89–99%. In three sponges, four or five unique Ig-like coding regions were scored. PCR amplification across this intron revealed multiple bands, polymorphic among five of six sponges. Further substantiated by Southern and Northern blots, it is evident that the genome of G. cydonium harbors multicopies of moderately divergent Ig-like domains. Presently, this only appears paralleled by the human KIR multigene family of NK cells MHC class I-specific receptors, which consist of two or three moderately divergent extracellular Ig-like domains.     

Deeply divergent lineages of the widespread New Zealand amphipod Paracalliope fluviatilis revealed using allozyme and mitochondrial DNA analyses

1. We evaluated the population genetic structure of the common New Zealand amphipod Paracalliope fluviatilis using eight allozyme loci, and the mitochondrial cytochrome oxidase c subunit I (COI) gene locus. Morphological analyses were also conducted to evaluate any phenotypic differences. Individuals belonging to P. fluviatilis were collected from a total of 14 freshwater fluvial habitats on the North and South Islands, New Zealand. 2. We found evidence for strong genetic differentiation among locations (Wright's F_ST > 0.25), and fixed differences (non‐shared alleles) at two of the eight allozyme loci indicating the possibility of previously unknown species. Analysis of a 545‐bp fragment of the COI locus was mostly congruent with the allozyme data and revealed the same deeply divergent lineages (sequence divergences up to 26%). 3. Clear genetic breaks were identified between North Island and South Island populations. North Island populations separated by <100 km also showed genetic differences between east and west draining watersheds (sequence divergence >12%). Accordingly, present‐day dispersal among hydrologically isolated habitats appears minimal for this taxon. 4. Although population differences were clearly shown by allozyme and mtDNA analyses, individuals were morphologically indistinguishable. This suggests that, as in North American and European taxa (e.g. Hyalella and Gammarus), morphological conservatism may be prevalent among New Zealand's freshwater amphipods. We conclude that molecular techniques, particularly the COI gene locus, may be powerful tools for resolving species that show no distinctive morphological differences.     

Phylogeny of Gaertnera Lam. (Rubiaceae) based on multiple DNA markers: evidence of a rapid radiation in a widespread, morphologically diverse genus

Phylogenetic relationships among 28 of the 68 species of the paleotropical genus Gaertnera (Rubiaceae) and two related genera were inferred from nucleotide sequence variation in four nuclear DNA (nDNA) markers: the internal transcribed spacers of nuclear rDNA (ITS), the large and small copies of phosphoenolpyruvate carboxylase (PepC-large and PepC-small), and triose phosphate isomerase (Tpi). Phylogenetic analysis of the combined nDNA dataset suggested that Gaertnera is monophyletic, but genetic variation among species was insufficient to reconstruct well-supported relationships within the genus. This was counter to expectations based on the very distinct morphologies and widespread distribution of the genus (West Africa to Sulawesi). Molecular clock analyses suggested variable dates of origin for Gaertnera depending upon the calibration method used. The most plausible calibration implies that Gaertnera migrated to Africa during the early Tertiary, possibly via a boreotropical land bridge and suggests that Gaertnera started to radiate 5.21 +/- 0.14 million years ago. This implies that range expansion in the group has occurred via a number of long-distance dispersal events rather than vicariance. The molecular clock estimate in turn estimated an unusually rapid lineage diversification rate within the radiation of 0.717-0.832 species/million years, comparable to those estimated for radiations on oceanic islands. Although low interspecific competition levels may have contributed to the diversification of Gaertnera on Mauritius, the mechanisms driving the rapid radiation of the group in other parts of its range remain elusive.     

Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome

The leafhoppers (Insecta: Hemiptera: Cicadellidae) are the most species-rich group of invertebrates in which intracellular symbionts are usual. Here we present the first molecular characterization of bacteriome-associates in the leafhoppers, with focus on the subfamily Cicadellinae (sharpshooters). Phylogenetic analyses of 16S rDNA sequences from intracellular symbionts residing in the bacteriomes of five host species indicate that these symbionts form a well-defined clade within the gamma-3 Proteobacteria, consistent with an ancient colonization and strict vertical transmission. More extensive gene sequence information is reported for the symbiont of Homalodisca coagulata (Say). The genome size, as determined by pulsed field gel electrophoresis, is approximately 680 kb. This finding, when combined with published results for symbionts of aphids, ants, psyllids and tsetse flies, adds to an emerging pattern which suggests that bacteriome associates often descend from ancient infections by gamma Proteobacteria, and that these lineages have undergone pronounced genome reduction. A new genus and species name, 'Candidatus Baumannia cicadellinicola' (sp. nov.) is proposed for this newly characterized clade of symbiotic bacteria.     

Phylogeny of Arvicolinae (Mammalia,Cricetidae): utility of morphological and molecular data sets in a recently radiating clade

Phylogenetic relationships within the Arvicolinae are examined based on two genes (mitochondrial cytb, nuclear GHR exon 10) and 296 morphological, developmental, behavioural, ecological and cytogenetic characters. To inspect the phylogenetic ‘behaviour’ of individual taxa, basic maximum‐parsimony and Bayesian phylogenetic analyses were accompanied by experiments based on different data‐partition combinations, ‘slow–fast’ character weighting, and inclusion/exclusion of individual problematic taxa. Ellobius, Prometheomys and Lagurus are the most basal arvicolines; Dicrostonyx, Phenacomys and Arborimus form a clade (Dicrostonychini s.lat.); the ‘core arvicolines’ include three subclades: Lemmini (Synaptomys, Lemmus, Myopus), Clethrionomyini (Eothenomys, Myodes) and Arvicolini (Arvicola, Chionomys, Stenocranius and Microtus, the last with six monophyletic subgenera: Alexandromys, ‘Neodon’, Mynomes, Lasiopodomys, Terricola, and Microtus s.str.). Position of Ondatra and Dinaromys is uncertain, probably compromised by highly homoplastic morphological characters.     

Phylogenetic signal and evolutionary correlates of urban tolerance in a widespread neotropical lizard clade*

Urbanization is intensifying worldwide, and while some species tolerate and even exploit urban environments, many others are excluded entirely from this new habitat. Understanding the factors that underlie tolerance of urbanization is thus of rapidly growing importance. Here, we examine urban tolerance across a diverse group of lizards: Caribbean members of the neotropical genus Anolis. Our analyses reveal that urban tolerance has strong phylogenetic signal, suggesting that closely related species tend to respond similarly to urban environments. We propose that this characteristic of urban tolerance in anoles may be used to forecast the possible responses of species to increasing urbanization. In addition, we identified several key ecological and morphological traits that tend to be associated with tolerance in Anolis. Specifically, species experiencing hot and dry conditions in their natural environment and those that maintain higher body temperatures tend to have greater tolerance of urban habitats. We also found that tolerance of urbanization is positively associated with toepad lamella number and negatively associated with ventral scale density and relative hindlimb length. The identification of factors that predispose a species to be more or less urban tolerant can provide a starting point for conservation and sustainable development in our increasingly urbanized world.     

Phylogeny of woodcreepers of the genus Lepidocolaptes (Aves,Furnariidae), a widespread Neotropical taxon

Arbeláez‐Cortés, E., Navarro‐Sigüenza, A. G. & García‐Moreno J. (2012). Phylogeny of woodcreepers of the genus Lepidocolaptes (Aves, Furnariidae), a widespread Neotropical taxon. —Zoologica Scripta, 41, 363–373. Phylogeny of woodcreepers of the genus Lepidocolaptes (Aves, Furnariidae), a widespread Neotropical taxon. The phylogeny of the genus Lepidocolaptes was reconstructed based on three mitochondrial DNA regions and one nuclear DNA intron, using Bayesian analysis. A general pattern of diversification among the lowland species followed by the diversification of highland species, and a close relationship among montane species with the two Atlantic Forest endemics, seem to depict the history of this genus. Results also showed that the two Mesoamerican species are sister‐taxa with high support. Finally, our data also suggest the existence of previously unknown intraspecific genetic structure within some taxa, especially among populations of Lepidocolaptes souleyetii.     

Common structural features of MAPEG -- a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism

A novel superfamily designated MAPEG (Membrane Associated Proteins in Eicosanoid and Glutathione metabolism), including members of widespread origin with diversified biological functions is defined according to enzymatic activities, sequence motifs, and structural properties. Two of the members are crucial for leukotriene biosynthesis, and three are cytoprotective exhibiting glutathione S-transferase and peroxidase activities. Expression of the most recently recognized member is strongly induced by p53, and may therefore play a role in apoptosis or cancer development. In spite of the different biological functions, all six proteins demonstrate common structural characteristics typical of membrane proteins. In addition, homologues are identified in plants, fungi, and bacteria, demonstrating this superfamily to be generally occurring.     

Phylogeny of Saxifragales (angiosperms,eudicots): analysis of a rapid,ancient radiation

Rapid, ancient radiations pose one of the most difficult challenges for phylogenetic estimation. We used DNA sequence data of 9,006 aligned base pairs from five genes (chloroplast atpB, matK, rbcL, and 18S and 26S nrDNA) to elucidate relationships among major lineages of Saxifragales (angiosperms, eudicots). These relationships were poorly supported in previous studies, apparently because the lineages originated in rapid succession. Using an array of methods that explicitly incorporate assumptions about evolutionary process (weighted maximum parsimony, maximum likelihood, LogDet/paralinear transformed distances), we show that the initial diversification of Saxifragales was indeed rapid. We suggest that the poor resolution of our best phylogenetic estimate is not due to violations of assumptions or to combining data partitions having conflicting histories or processes. We show that estimated branch lengths during the initial diversification are exceedingly short, and we estimate that acquiring sufficient sequence data to resolve these relationships would require an extraordinary effort (approximately 10(7) bp), assuming a linear increase in branch support with branch length. However, our simulation of much larger data sets containing a distribution of phylogenetic signal similar to that of the five sampled gene sequences suggests a limit to achievable branch support. Using statistical tests of differences in the likelihoods of topologies, we evaluated whether the initial radiation of Saxifragales involved the simultaneous origin of major lineages. Our results are consistent with predictions that resolving the branching order of rapid, ancient radiations requires sampling characters that evolved rapidly at the time of the radiation but have since experienced a slower evolutionary rate.