Andreas Wallberg

Acoelomorph flatworms are deuterostomes related to Xenoturbella

Xenoturbellida and Acoelomorpha are marine worms with contentious ancestry. Both were originally associated with the flatworms (Platyhelminthes), but molecular data have revised their phylogenetic positions, generally linking Xenoturbellida to the deuterostomes and positioning the Acoelomorpha as the most basally branching bilaterian group(s). Recent phylogenomic data suggested that Xenoturbellida and Acoelomorpha are sister taxa and together constitute an early branch of Bilateria. Here we assemble three independent data sets—mitochondrial genes, a phylogenomic data set of 38,330 amino-acid positions and new microRNA (miRNA) complements—and show that the position of Acoelomorpha is strongly affected by a long-branch attraction (LBA) artefact. When we minimize LBA we find consistent support for a position of both acoelomorphs and Xenoturbella within the deuterostomes. The most likely phylogeny links Xenoturbella and Acoelomorpha in a clade we call Xenacoelomorpha. The Xenacoelomorpha is the sister group of the Ambulacraria (hemichordates and echinoderms). We show that analyses of miRNA complements have been affected by character loss in the acoels and that both groups possess one miRNA and the gene Rsb66 otherwise specific to deuterostomes. In addition, Xenoturbella shares one miRNA with the ambulacrarians, and two with the acoels. This phylogeny makes sense of the shared characteristics of Xenoturbellida and Acoelomorpha, such as ciliary ultrastructure and diffuse nervous system, and implies the loss of various deuterostome characters in the Xenacoelomorpha including coelomic cavities, through gut and gill slits.

A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera.

The honeybee Apis mellifera has major ecological and economic importance. We analyze patterns of genetic variation at 8.3 million SNPs, identified by sequencing 140 honeybee genomes from a worldwide sample of 14 populations at a combined total depth of 634×. These data provide insight into the evolutionary history and genetic basis of local adaptation in this species. We find evidence that population sizes have fluctuated greatly, mirroring historical fluctuations in climate, although contemporary populations have high genetic diversity, indicating the absence of domestication bottlenecks. Levels of genetic variation are strongly shaped by natural selection and are highly correlated with patterns of gene expression and DNA methylation. We identify genomic signatures of local adaptation, which are enriched in genes expressed in workers and in immune system– and sperm motility–related genes that might underlie geographic variation in reproduction, dispersal and disease resistance. This study provides a framework for future investigations into responses to pathogens and climate change in honeybees.

The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling

The transition to a vermiform body shape is one of the most important events in animal evolution, having led to the impressive radiation of Bilateria. However, the sister group of Bilateria has remained obscure. Cladistic analyses of morphology indicate that Ctenophora is the sister group of Bilateria. Previous analyses of SSU rRNA sequences have yielded conflicting results; in many studies Ctenophora forms the sister group of Cnidaria + Bilateria, but in others the ctenophores group with poriferans. Here we re‐examine the SSU sequence by analyzing a dataset with 528 metazoan + outgroup sequences, including almost 120 poriferan and diploblast sequences. We use parsimony ratchet and jackknife methods, as well as Bayesian methods, to analyze the data. The results indicate strong phylogenetic signals for a cnidarian + bilaterian group and for the comb jellies to have branched off early within a group uniting all epithelial animals [(Ct,(Cn,Bi))]. We demonstrate the importance of inclusive taxonomic coverage of ribosomal sequences for resolving this problematic part of the metazoan tree: topological stability increases dramatically with the addition of taxa, and the jackknife frequencies of the internal nodes uniting the lineages [(Cn,Bi) and ((Ct,(Cn,Bi))] also increase. We consider the reconstructed topology to represent the current best hypothesis of the interrelationships of these old lineages. Some morphological features supporting alternative hypotheses are discussed in the light of this result.

A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi

The filamentous ascomycete genus Neurospora encompasses taxa with a wide range of reproductive modes. Sexual reproduction in this genus can be divided into three major modes; heterothallism (self-incompatibility), homothallism (self-compatibility) and pseudohomothallism (partial self-compatibility). In addition to the sexual pathway, most of the heterothallic taxa propagate with morphologically distinct, vegetative dissemination propagules (macroconidia), while this feature is undetected in the majority of the homothallic taxa. In this study, we used sequence information of seven nuclear gene loci from 43 taxa (295 of the possible 301 locus-by-taxon combinations) to create a phylogeny of Neurospora. The results suggest that transitions in reproductive mode have occurred at multiple times within this group of fungi. Although a homothallic ancestor would imply fewer switches in reproductive mode, we argue that the ancestor of Neurospora was likely heterothallic and that homothallism has evolved independently at least six times in the evolutionary history of the genus. Furthermore, the two pseudohomothallic taxa of Neurospora (N. tetrasperma and N. tetraspora) represent two independent origins of pseudohomothallism. Likelihood ratio tests of substitution rates among branches in the phylogeny indicate that reproductive mode is an important factor driving genome evolution in Neurospora. First, an increased level of non-synonymous/synonymous substitutions in branches delineating homothallic taxa was found, suggesting a reduced efficiency of purifying selection in these taxa. Furthermore, elevated nucleotide substitution rates were found in heterothallic, conidia-producing, lineages as compared to the homothallic non-conidiating lineages. The latter finding is likely due to the presence of conidia, i.e., a higher rate of mitotic divisions inducing mutations, and/or that the homothallic taxa have evolved a lower mutation rate to avoid genomic degeneration.

Dismissal of Acoelomorpha: Acoela and Nemertodermatida are separate early bilaterian clades

We used new 18S and 28S rRNA sequences analysed with parsimony, maximum likelihood and Bayesian methods of phylogenetic reconstruction to show that Nemertodermatida, generally classified as the sister group of Acoela within the recently proposed Phylum Acoelomorpha, are a separate basal bilaterian lineage. We used several analytical approaches to control for possible long branch attraction (LBA) artefacts in our results. Parsimony and the model based phylogenetic reconstruction methods that incorporate ‘corrections’ for substitution rate heterogenities yielded concordant results. When putative long branch taxa were experimentally removed the resulting topologies were consistent with our total evidence analysis. Deletion of fast‐evolving nucleotide sites decreased resolution and clade support, but did not support a topology conflicting with the total evidence analysis. Establishment of Acoela and Nemertodermatida as two early lineages facilitates reconstruction of ancestral bilaterian features. The ancestor of extant Bilateria was a small, benthic direct developer without coelom or a planktonic larval stage. The previously proposed Phylum Acoelomorpha is dismissed as paraphyletic.

Filling a gap in the phylogeny of flatworms: relationships within the Rhabdocoela (Platyhelminthes), inferred from 18S ribosomal DNA sequences

The phylogeny of the Rhabdocoela, a species‐rich taxon of free‐living flatworms, is reconstructed based on complete 18S rDNA sequences. The analysis includes 62 rhabdocoels and 102 representatives of all major flatworm taxa. In total, 46 new sequences are used, 41 of them from rhabdocoel species, five from proseriates. Phylogenetic analysis was performed using maximum parsimony and Bayesian inference. Clade support was evaluated with parsimony jackknifing, Bremer support indices and Bayesian posterior probabilities. The resulting cladogram corroborates that the Rhabdocoela is monophyletic, but its sister group remains uncertain. The ‘Dalyellioida’ and the ‘Typhloplanoida’, both former rhabdocoel subtaxa, are polyphyletic. Within the Rhabdocoela the monophyletic Kalyptorhynchia, characterized by a muscular proboscis, forms the sister group of all other rhabdocoels. The Schizorhynchia is a monophyletic subtaxon of the Kalyptorhynchia, with the split proboscis as a synapomorphy. Except for the Dalyelliidae and the Typhloplanidae, both freshwater taxa, none of the ‘families’ previously included in the ‘Typhloplanoida’ and the ‘Dalyellioida’ appears to be monophyletic. As a result of this analysis, three existing and four new taxon names are formally defined following the rules of the Phylocode.

Extreme recombination frequencies shape genome variation and evolution in the honeybee, Apis mellifera.

Meiotic recombination is a fundamental cellular process, with important consequences for evolution and genome integrity. However, we know little about how recombination rates vary across the genomes of most species and the molecular and evolutionary determinants of this variation. The honeybee, Apis mellifera, has extremely high rates of meiotic recombination, although the evolutionary causes and consequences of this are unclear. Here we use patterns of linkage disequilibrium in whole genome resequencing data from 30 diploid honeybees to construct a fine-scale map of rates of crossing over in the genome. We find that, in contrast to vertebrate genomes, the recombination landscape is not strongly punctate. Crossover rates strongly correlate with levels of genetic variation, but not divergence, which indicates a pervasive impact of selection on the genome. Germ-line methylated genes have reduced crossover rate, which could indicate a role of methylation in suppressing recombination. Controlling for the effects of methylation, we do not infer a strong association between gene expression patterns and recombination. The site frequency spectrum is strongly skewed from neutral expectations in honeybees: rare variants are dominated by AT-biased mutations, whereas GC-biased mutations are found at higher frequencies, indicative of a major influence of GC-biased gene conversion (gBGC), which we infer to generate an allele fixation bias 5 – 50 times the genomic average estimated in humans. We uncover further evidence that this repair bias specifically affects transitions and favours fixation of CpG sites. Recombination, via gBGC, therefore appears to have profound consequences on genome evolution in honeybees and interferes with the process of natural selection. These findings have important implications for our understanding of the forces driving molecular evolution.

From where did the Western honeybee (Apis mellifera) originate

The native range of the honeybee Apis mellifera encompasses Europe, Africa, and the Middle East, whereas the nine other species of Apis are found exclusively in Asia. It is therefore commonly assumed that A. mellifera arose in Asia and expanded into Europe and Africa. However, other hypotheses for the origin of A. mellifera have also been proposed based on phylogenetic trees constructed from genetic markers. In particular, an analysis based on >1000 single-nucleotide polymorphism markers placed the root of the tree of A. mellifera subspecies among samples from Africa, suggestive of an out-of-Africa expansion. Here, we re-evaluate the evidence for this and other hypotheses by testing the robustness of the tree topology to different tree-building methods and by removing specimens with a potentially hybrid background. These analyses do not unequivocally place the root of the tree of A. mellifera subspecies within Africa, and are potentially consistent with a variety of hypotheses for honeybee evolution, including an expansion out of Asia. Our analyses also support high divergence between western and eastern European populations of A. mellifera, suggesting they are likely derived from two distinct colonization routes, although the sources of these expansions are still unclear.

A revision of the systematics of panther worms (Hofstenia spp., Acoela), with notes on color variation and genetic variation within the genus

Species of the genus Hofstenia are voracious predators and among the largest and most colorful of the Acoela. They are known from Japan, the Red Sea, the North Atlantic islands of Bermuda and the Bahamas, and the Caribbean and in a variety of habitats including the rocky intertidal, among Thalassia sea grass, on filamentous algae and decaying mangrove leaves. Certain color morphs associated with each of these habitats seem to have confused the taxonomy of the group. While brown-and-white banding and spotting patterns of Hofstenia miamia and Hofstenia giselae are distinctive for species associated with mangrove leaves and Thallasia sp. and are likely to be cryptic for these specific environments, we find some evidence to suggest that the coloration is mimicry of a nudibranch with aposematic coloration. The common plan in these patterns is one with three variously solid or spotted lighter cross bands on a dark background. Our examination of museum type material and live specimens of Hofstenia collected from Bahamas, Belize, Bermuda, and Panama revealed no internal morphological differences between the Hofstenia species occurring in the Caribbean. Similarly, our analyses of 18S and 28S molecular sequence data revealed no significant differences among specimens. Accordingly, we declare that Hofstenia giselae is a junior synonym of Hofstenia miamia, the three-banded panther worm.

Genomewide analysis of admixture and adaptation in the Africanized honeybee

Genetic exchange by hybridization or admixture can make an important contribution to evolution, and introgression of favourable alleles can facilitate adaptation to new environments. A small number of honeybees (Apis mellifera) with African ancestry were introduced to Brazil ~60 years ago, which dispersed and hybridized with existing managed populations of European origin, quickly spreading across much of the Americas in an example of a massive biological invasion. Here, we analyse whole‐genome sequences of 32 Africanized honeybees sampled from throughout Brazil to study the effect of this process on genome diversity. By comparison with ancestral populations from Europe and Africa, we infer that these samples have 84% African ancestry, with the remainder from western European populations. However, this proportion varies across the genome and we identify signals of positive selection in regions with high European ancestry proportions. These observations are largely driven by one large gene‐rich 1.4‐Mbp segment on chromosome 11 where European haplotypes are present at a significantly elevated frequency and likely confer an adaptive advantage in the Africanized honeybee population. This region has previously been implicated in reproductive traits and foraging behaviour in worker bees. Finally, by analysing the distribution of ancestry tract lengths in the context of the known time of the admixture event, we are able to infer an average generation time of 2.0 years. Our analysis highlights the processes by which populations of mixed genetic ancestry form and adapt to new environments.