Ecology has contrasting effects on genetic variation within species versus rates of molecular evolution across species in water beetles

Comparative analysis is a potentially powerful approach to study the effects of ecological traits on genetic variation and rate of evolution across species. However, the lack of suitable datasets means that comparative studies of correlates of genetic traits across an entire clade have been rare. Here, we use a large DNA-barcode dataset (5062 sequences) of water beetles to test the effects of species ecology and geographical distribution on genetic variation within species and rates of molecular evolution across species. We investigated species traits predicted to influence their genetic characteristics, such as surrogate measures of species population size, latitudinal distribution and habitat types, taking phylogeny into account. Genetic variation of cytochrome oxidase I in water beetles was positively correlated with occupancy (numbers of sites of species presence) and negatively with latitude, whereas substitution rates across species depended mainly on habitat types, and running water specialists had the highest rate. These results are consistent with theoretical predictions from nearly-neutral theories of evolution, and suggest that the comparative analysis using large databases can give insights into correlates of genetic variation and molecular evolution.     

Deep mtDNA subdivision within Linnean species in an endemic radiation of tiger beetles from New Zealand (genus Neocicindela)

The invertebrate fauna of New Zealand is of great interest as a geologically tractable model for the study of species diversification, but direct comparisons with closely related lineages elsewhere are lacking. Integrating population-level analyses with studies of taxonomy and clade diversification, we performed mtDNA analysis on Neocicindela (Cicindelidae, tiger beetles) for a broad sample of populations from 11 of 12 known species and 161 specimens (three loci, 1883 nucleotides), revealing 123 distinct haplotypes. Phylogenetic reconstruction recovered two main lineages, each composed of 5-6 Linnean species whose origin was dated to 6.66 and 7.26 Mya, while the Neocicindela stem group was placed at 10.82 ± 0.48 Mya. Species delimitation implementing a character-based (diagnostic) species concept recognized 19 species-level groups that were in general agreement with Linnean species but split some of these into mostly allopatric subgroups. Tree-based methods of species delimitation using a mixed Yule-coalescence model were inconclusive, and recognized 32-51 entities (including singletons), splitting existing species into up to 8 partially sympatric groups. These findings were different from patterns in the Australian sister genus Rivacindela, where character-based and tree-based methods were previously shown to produce highly congruent groupings. In Neocicindela, the pattern of mtDNA variation was characterized by high intra-population and intra-species haplotype divergence, the coexistence of divergent haplotypes in sympatry, and a poor correlation of genetic and geographic distance. These observations combined suggest a scenario of phylogeographic divergence and secondary contact driven by orogenetic and climatic changes of the Pleistocene/Pliocene. The complex evolutionary history of most species of Neocicindela due to the relative instability of the New Zealand biota resulted in populations of mixed ancestry but not in a general loss of genetic variation.     

Integrating ecology into macroevolutionary research

On 9 March, over 150 biologists gathered in London for the Centre for Ecology and Evolution spring symposium, 'Integrating Ecology into Macroevolutionary Research'. The event brought together researchers from London-based institutions alongside others from across the UK, Europe and North America for a day of talks. The meeting highlighted methodological advances and recent analyses of exemplar datasets focusing on the exploration of the role of ecological processes in shaping macroevolutionary patterns.     

S100A4 downregulates filopodia formation through increased dynamic instability

Cell migration requires the initial formation of cell protrusions, lamellipodia and/or filopodia, the attachment of the leading lamella to extracellular cues and the formation and efficient recycling of focal contacts at the leading edge. The small calcium binding EF-hand protein S100A4 has been shown to promote cell motility but the direct molecular mechanisms responsible remain to be elucidated. In this work, we provide new evidences indicating that elevated levels of S100A4 affect the stability of filopodia and prevent the maturation of focal complexes. Increasing the levels of S100A4 in a rat mammary benign tumor derived cell line results in acquired cellular migration on the wound healing scratch assay. At the cellular levels, we found that high levels of S100A4 induce the formation of many nascent filopodia, but that only a very small and limited number of those can stably adhere and mature, as opposed to control cells, which generate fewer protrusions but are able to maintain these into more mature projections. This observation was paralleled by the fact that S100A4 overexpressing cells were unable to establish stable focal adhesions. Using different truncated forms of the S100A4 proteins that are unable to bind to myosin II A, our data suggests that this newly identified functions of S100A4 is myosin-dependent, providing new understanding on the regulatory functions of S100A4 on cellular migration.Key words: filopodia, S100A4, cell migration, focal adhesion, cancer progression, myosin IIA     

Global remodelling of cellular microenvironment due to loss of collagen VII

The mammalian cellular microenvironment is shaped by soluble factors and structural components, the extracellular matrix, providing physical support, regulating adhesion and signalling. A global, quantitative mass spectrometry strategy, combined with bioinformatics data processing, was developed to assess proteome differences in the microenvironment of primary human fibroblasts. We studied secreted proteins of fibroblasts from normal and pathologically altered skin and their post‐translational modifications. The influence of collagen VII, an important structural component, which is lost in genetic skin fragility, was used as model. Loss of collagen VII had a global impact on the cellular microenvironment and was associated with proteome alterations highly relevant for disease pathogenesis including decrease in basement membrane components, increase in dermal matrix proteins, TGF‐β and metalloproteases, but not higher protease activity. The definition of the proteome of fibroblast microenvironment and its plasticity in health and disease identified novel disease mechanisms and potential targets of intervention.     

Evidence for inefficient selection against deleterious mutations in cytochrome oxidase I of asexual bdelloid rotifers

Evolutionary theory predicts that natural selection should be less efficient in asexually than in sexually reproducing organisms. Obligate asexuals are expected to adapt slowly to changing environments and to accumulate mildly deleterious mutations to their genomes, potentially explaining their typically short evolutionary lifespans. One group of animals that appear to challenge these ideas is the bdelloid rotifers, a large and ancient clade of obligate asexuals. Previous work has found no evidence for inefficient selection against deleterious mutations in protein-coding genes of bdelloids. However, these studies relied mostly on between-species comparisons and were therefore unable to detect mildly deleterious mutations that persist within populations but are removed by selection over longer time periods. Here, we test for inefficient purifying selection acting on the cytochrome oxidase I (cox1) mitochondrial gene in 3 clades of bdelloids. Patterns of variation are compared to those of two facultatively sexual clades: a monogonont rotifer (Brachionus) and a branchiopod crustacean (Daphnia). As predicted due to the strict linkage between mitochondrial and nuclear genomes, bdelloids exhibit higher frequencies of putatively deleterious amino acid polymorphism within populations than the two facultatively sexual clades. While the monophyly and age of bdelloids makes it hard to rule out other explanations for the observed differences, several possible confounding factors, such as differences in effective population size or patterns of codon usage, are shown not to explain the observed differences. We therefore conclude that bdelloid mitochondrial DNA variation does display the signature of inefficient selection expected of obligate asexuals.     

The geographical pattern of speciation and floral diversification in the neotropics: the tribe sinningieae (gesneriaceae) as a case study

The geographical pattern of speciation and the relationship between floral variation and species ranges were investigated in the tribe Sinningieae (Gesneriaceae), which is found mainly in the Atlantic forests of Brazil. Geographical distribution data recorded on a grid system of 0.5 x 0.5 degree intervals and a near-complete species-level phylogenetic tree of Sinningieae inferred from a simultaneous analysis of seven DNA regions were used to address the role of geographical isolation in speciation. Geographical range overlaps between sister lineages were measured across all nodes in the phylogenetic tree and analyzed in relation to relative ages estimated from branch lengths. Although there are several cases of species sympatry in Sinningieae, patterns of sympatry between sister taxa support the predominance of allopatric speciation. The pattern of sympatry between sister taxa is consistent with range shifts following allopatric speciation, except in one clade, in which the overlapping distribution of recent sister species indicates speciation within a restricted geographical area and involving changes in pollinators and habitats. The relationship between floral divergence and regional sympatry was also examined by analyzing floral contrasts, phenological overlap, and the degree of sympatry between sister clades. Morphological contrast between flowers is not increased in sympatry and phenological divergence is more apparent between allopatric clades than between sympatric clades. Therefore, our results failed to indicate a tendency for sympatric taxa to minimize morphological and phenological overlap (geographic exclusion and/or character displacement hypotheses). Instead, they point toward adaptation in phenology to local conditions and buildup of sympatries at random with respect to flower morphology. Additional studies at a lower geographical scale are needed to identify truely coexisting species and the components of their reproductive isolation.     

The role of recombination,niche‐specific gene pools and flexible genomes in the ecological speciation of bacteria

Bacteria diversify into genetic clusters analogous to those observed in sexual eukaryotes, but the definition of bacterial species is an ongoing problem. Recent work has focused on adaptation to distinct ecological niches as the main driver of clustering, but there remains debate about the role of recombination in that process. One view is that homologous recombination occurs too rarely for gene flow to constrain divergent selection. Another view is that homologous recombination is frequent enough in many bacterial populations that barriers to gene flow are needed to permit divergence. Niche‐specific gene pools have been proposed as a general mechanism to limit gene flow. We use theoretical models to evaluate additional hypotheses that evolving genetic architecture, specifically the effect sizes of genes and gene gain and loss, can limit gene flow between diverging populations. Our model predicts that (a) in the presence of gene flow and recombination, ecological divergence is concentrated in few loci of large effect and (b) high rates of gene flow plus recombination promote gene loss and favor the evolution of niche‐specific genes. The results show that changing genetic architecture and gene loss can facilitate ecological divergence, even without niche‐specific gene pools. We discuss these results in the context of recent studies of sympatric divergence in microbes.     

Species interactions alter evolutionary responses to a novel environment

Studies of evolutionary responses to novel environments typically consider single species or perhaps pairs of interacting species. However, all organisms co-occur with many other species, resulting in evolutionary dynamics that might not match those predicted using single species approaches. Recent theories predict that species interactions in diverse systems can influence how component species evolve in response to environmental change. In turn, evolution might have consequences for ecosystem functioning. We used experimental communities of five bacterial species to show that species interactions have a major impact on adaptation to a novel environment in the laboratory. Species in communities diverged in their use of resources compared with the same species in monocultures and evolved to use waste products generated by other species. This generally led to a trade-off between adaptation to the abiotic and biotic components of the environment, such that species evolving in communities had lower growth rates when assayed in the absence of other species. Based on growth assays and on nuclear magnetic resonance (NMR) spectroscopy of resource use, all species evolved more in communities than they did in monocultures. The evolutionary changes had significant repercussions for the functioning of these experimental ecosystems: communities reassembled from isolates that had evolved in polyculture were more productive than those reassembled from isolates that had evolved in monoculture. Our results show that the way in which species adapt to new environments depends critically on the biotic environment of co-occurring species. Moreover, predicting how functioning of complex ecosystems will respond to an environmental change requires knowing how species interactions will evolve.     

Exploring rate variation among and within sites in a densely sampled tree: species level phylogenetics of north american tiger beetles (genus cicindela)

Species-level phylogenetic studies require fast-evolving nucleotide positions to resolve relationships among close relatives, but these sites may be highly homoplastic and perhaps uninformative or even misleading deeper in the tree. Here we describe a species-level analysis of tiger beetles in the genus Cicindela (Coleoptera: Cicindelidae) for 132 terminal taxa and 1897 nucleotide positions from three regions of mtDNA, comprising 75% coverage of species occurring in North America. Evenly weighted parsimony analysis recovered four major clades representing radiations confined to North and Central America. Relationships near the tips were well supported but signal was contradictory at deeper nodes. Two major categories (3rd positions and all others) can be distinguished in likelihood analysis of character variation, of which only the fast-changing 3rd position characters were affected by saturation. However, their downweighting under a variety of criteria did not improve the tree topology at basal nodes. There was weak conflict between 3rd and non-3rd position characters deep in the tree, but support levels declined towards the root for all categories, even on trees that were reconstructed from 3rd and non-3rd positions separately. Statistical analysis of parsimony-based character transitions along branches showed a largely homogeneous distribution of change along the root-to-tip axis. The comparison of character transitions among the four major portions of the tree revealed deviations from stochastic distribution for the non-3rd positions, but not for 3rd positions. Hence, variability of functionally constrained non-3rd positions differs between clades and may be dependent on the character states at other sites, consistent with the covarion model of molecular evolution. The results suggest that some properties of 3rd positions are less problematic for phylogenetic reconstruction than other categories despite their high total homoplasy. In densely sampled data sets of closely related species, the disadvantages of weighting schemes according to homoplasy levels outweigh the benefits, showing the difficulty of devising meaningful weighting schemes that are applicable universally throughout the tree.