Everything old is new again: (linc)RNAs make proteins!

Long non‐coding RNAs have become the focus of considerable interest over the past few years. Intriguing novel functions have been reported for lincRNAs. Three recent papers identify lincRNAs that work in a more conventional way—encoding protein—in each case a small polypeptide with an interesting biological activity (Magny et al, 2013 ; Pauli et al, 2014 ), (Bazzini et al, 2014 ).     

Bacteriophage exclusion,a new defense system

The ability to withstand viral predation is critical for survival of most microbes. Accordingly, a plethora of phage resistance systems has been identified in bacterial genomes (Labrie et al, 2010 ), including restriction‐modification systems (R‐M) (Tock & Dryden, 2005 ), abortive infection (Abi) (Chopin et al, 2005 ), Argonaute‐based interference (Swarts et al, 2014 ), as well as clustered regularly interspaced short palindromic repeats (CRISPR) and associated protein (Cas) adaptive immune system (CRISPR‐Cas) (Barrangou & Marraffini, 2014 ; Van der Oost et al, 2014 ). Predictably, the dark matter of bacterial genomes contains a wealth of genetic gold. A study published in this issue of The EMBO Journal by Goldfarb et al ( 2015 ) unveils bacteriophage exclusion (BREX) as a novel, widespread bacteriophage resistance system that provides innate immunity against virulent and temperate phage in bacteria.     

Standing and flowing: the complex origins of adaptive variation

A population faced with a new selection pressure can only adapt if appropriate genetic variation is available. This genetic variation might come from new mutations or from gene exchange with other populations or species, or it might already segregate in the population as standing genetic variation (which might itself have arisen from either mutation or gene flow). Understanding the relative importance of these sources of adaptive variation is a fundamental issue in evolutionary genetics (Orr & Betancourt 2001 ; Barrett & Schluter 2008 ; Gladyshev et al. 2008 ) and has practical implications for conservation, plant and animal breeding, biological control and infectious disease prevention (e.g. Robertson 1960 ; Soulé & Wilcox 1980 ; Prentis et al. 2008 ; Pennings 2012 ). In this issue of Molecular Ecology, Roesti et al. ( 2014 ) make an important contribution to this longstanding debate.     

Homomorphic plant sex chromosomes are coming of age

Sex chromosomes are a very peculiar part of the genome that have evolved independently in many groups of animals and plants (Bull 1983 ). Major research efforts have so far been focused on large heteromorphic sex chromosomes in a few animal and plant species (Chibalina & Filatov 2011 ; Zhou & Bachtrog 2012 ; Bellott et al. 2014 ; Hough et al. 2014 ; Zhou et al. 2014 ), while homomorphic (cytologically indistinguishable) sex chromosomes have largely been neglected. However, this situation is starting to change. In this issue, Geraldes et al. ( 2015 ) describe a small (~100 kb long) sex‐determining region on the homomorphic sex chromosomes of poplars (Populus trichocarpa and related species, Fig.  1 ). All species in Populus and its sister genus Salix are dioecious, suggesting that dioecy and the sex chromosomes, if any, should be relatively old. Contrary to this expectation, Geraldes et al. ( 2015 ) demonstrate that the sex‐determining region in poplars is of very recent origin and probably evolved within the genus Populus only a few million years ago.     

Host plant richness explains diversity of ectomycorrhizal fungi: Response to the comment of Tedersoo et al. (2014)

Exploring the relationships between the biodiversity of groups of interacting organisms yields insight into ecosystem stability and function (Hooper et al. 2000 ; Wardle 2006 ). We demonstrated positive relationships between host plant richness and ectomycorrhizal (EM) fungal diversity both in a field study in subtropical China (Gutianshan) and in a meta‐analysis of temperate and tropical studies (Gao et al. 2013 ). However, based on re‐evaluation of our data sets, Tedersoo et al. ( 2014 ) argue that the observed positive correlation between EM fungal richness and EM plant richness at Gutianshan and also in our metastudies was based mainly from (i) a sampling design with inconsistent species pool and (ii) poor data compilation for the meta‐analysis. Accordingly, we checked our data sets and repeated the analysis performed by Tedersoo et al. ( 2014 ). In contrast to Tedersoo et al. ( 2014 ), our re‐analysis still confirms a positive effect of plant richness on EM fungal diversity in Gutianshan, temperate and tropical ecosystems, respectively.     

Tending a complex microbiota requires major immune complexity

Animals maintain complex microbial communities within their guts that fill important roles in the health and development of the host. To what degree a host's genetic background influences the establishment and maintenance of its gut microbial communities is still an open question. We know from studies in mice and humans that external factors, such as diet and environmental sources of microbes, and host immune factors play an important role in shaping the microbial communities (Costello et al. 2012 ). In this issue of Molecular Ecology, Bolnick et al. ( 2014a ) sample the gut microbial community from 150 genetically diverse stickleback isolated from a single lake to provide evidence that another part of the adaptive immune response, the major histocompatibility complex class II (MHCII) receptors of antigen‐presenting cells, may play a role in shaping the gut microbiota of the threespine stickleback, Gasterosteus aculeatus (Bolnick et al. 2014a ). Bolnick et al. ( 2014a ) provide insight into natural, interindividual variation in the diversity of both stickleback MHCII alleles and their gut microbial communities and correlate changes in the diversity of MHCII receptor alleles with changes in the microbiota.     

Demystifying the RAD fad

We are writing in response to the population and phylogenomics meeting review by Andrews & Luikart ( 2014 ) entitled ‘Recent novel approaches for population genomics data analysis’. Restriction‐site‐associated DNA (RAD) sequencing has become a powerful and useful approach in molecular ecology, with several different published methods now available to molecular ecologists, none of which can be considered the best option in all situations. A&L report that the original RAD protocol of Miller et al. ( 2007 ) and Baird et al. ( 2008 ) is superior to all other RAD variants because putative PCR duplicates can be identified (see Baxter et al. 2011 ), thereby reducing the impact of PCR artefacts on allele frequency estimates (Andrews & Luikart 2014 ). In response, we (i) challenge the assertion that the original RAD protocol minimizes the impact of PCR artefacts relative to that of other RAD protocols, (ii) present additional biases in RADseq that are at least as important as PCR artefacts in selecting a RAD protocol and (iii) highlight the strengths and weaknesses of four different approaches to RADseq which are a representative sample of all RAD variants: the original RAD protocol (mbRAD, Miller et al. 2007 ; Baird et al. 2008 ), double digest RAD (ddRAD, Peterson et al. 2012 ), ezRAD (Toonen et al. 2013 ) and 2bRAD (Wang et al. 2012 ). With an understanding of the strengths and weaknesses of different RAD protocols, researchers can make a more informed decision when selecting a RAD protocol.     

Using RAD‐seq to recognize sex‐specific markers and sex chromosome systems

Next‐generation sequencing methods have initiated a revolution in molecular ecology and evolution (Tautz et al. 2010 ). Among the most impressive of these sequencing innovations is restriction site‐associated DNA sequencing or RAD‐seq (Baird et al. 2008 ; Andrews et al. 2016 ). RAD‐seq uses the Illumina sequencing platform to sequence fragments of DNA cut by a specific restriction enzyme and can generate tens of thousands of molecular genetic markers for analysis. One of the many uses of RAD‐seq data has been to identify sex‐specific genetic markers, markers found in one sex but not the other (Baxter et al. 2011 ; Gamble & Zarkower 2014 ). Sex‐specific markers are a powerful tool for biologists. At their most basic, they can be used to identify the sex of an individual via PCR. This is useful in cases where a species lacks obvious sexual dimorphism at some or all life history stages. For example, such tests have been important for studying sex differences in life history (Sheldon 1998 ; Mossman & Waser 1999 ), the management and breeding of endangered species (Taberlet et al. 1993 ; Griffiths & Tiwari 1995 ; Robertson et al. 2006 ) and sexing embryonic material (Hacker et al. 1995 ; Smith et al. 1999 ). Furthermore, sex‐specific markers allow recognition of the sex chromosome system in cases where standard cytogenetic methods fail (Charlesworth & Mank 2010 ; Gamble & Zarkower 2014 ). Thus, species with male‐specific markers have male heterogamety (XY) while species with female‐specific markers have female heterogamety (ZW). In this issue, Fowler & Buonaccorsi ( 2016 ) illustrate the ease by which RAD‐seq data can generate sex‐specific genetic markers in rockfish (Sebastes). Moreover, by examining RAD‐seq data from two closely related rockfish species, Sebastes chrysomelas and Sebastes carnatus (Fig.  1 ), Fowler & Buonaccorsi ( 2016 ) uncover shared sex‐specific markers and a conserved sex chromosome system.     

It's a family act: the geminin triplets take center stage in motile ciliogenesis

The balance between proliferation and differentiation is a fundamental aspect of multicellular life. Perhaps nowhere is this delicate balance more palpable than in the multiciliated cells (MCCs) that line the respiratory tract, the ependyma, and the oviduct. These cells contain dozens to hundreds of motile cilia that beat in a concerted fashion to generate directed fluid flow over the tissue surface. Although MCCs have exited the cell cycle, remarkably, they retain the ability to duplicate their centrioles and to mature those centrioles into ciliary basal bodies—two features, which are known to be normally under strict cell cycle control (Firat‐Karalar & Stearns, 2014 ). How post‐mitotic MCCs retain this ability, remains unclear. In the past several months, four research articles, including one from Terré et al in this issue of The EMBO Journal, have described a vital role for the geminin coiled‐coil domain‐containing protein (Gemc1) in the MCC gene expression program in multiple tissues and organisms, that bring us closer to understanding this question (Kyrousi et al, 2015 ; Zhou et al, 2015 ; Arbi et al, 2016 ; Terré et al, 2016 ).     

Two are better than one: combining landscape genomics and common gardens for detecting local adaptation in forest trees

Predicting likely species responses to an alteration of their local environment is key to decision‐making in resource management, ecosystem restoration and biodiversity conservation practice in the face of global human‐induced habitat disturbance. This is especially true for forest trees which are a dominant life form on Earth and play a central role in supporting diverse communities and structuring a wide range of ecosystems. In Europe, it is expected that most forest tree species will not be able to migrate North fast enough to follow the estimated temperature isocline shift given current predictions for rapid climate warming. In this context, a topical question for forest genetics research is to quantify the ability for tree species to adapt locally to strongly altered environmental conditions (Kremer et al. 2012 ). Identifying environmental factors driving local adaptation is, however, a major challenge for evolutionary biology and ecology in general but is particularly difficult in trees given their large individual and population size and long generation time. Empirical evaluation of local adaptation in trees has traditionally relied on fastidious long‐term common garden experiments (provenance trials) now supplemented by reference genome sequence analysis for a handful of economically valuable species. However, such resources have been lacking for most tree species despite their ecological importance in supporting whole ecosystems. In this issue of Molecular Ecology, De Kort et al. ( 2014 ) provide original and convincing empirical evidence of local adaptation to temperature in black alder, Alnus glutinosa L. Gaertn, a surprisingly understudied keystone species supporting riparian ecosystems. Here, De Kort et al. ( 2014 ) use an innovative empirical approach complementing state‐of‐the‐art landscape genomics analysis of A. glutinosa populations sampled in natura across a regional climate gradient with phenotypic trait assessment in a common garden experiment (Fig. 1 ). By combining the two methods, De Kort et al. ( 2014 ) were able to detect unequivocal association between temperature and phenotypic traits such as leaf size as well as with genetic loci putatively under divergent selection for temperature. The research by De Kort et al. ( 2014 ) provides valuable insight into adaptive response to temperature variation for an ecologically important species and demonstrates the usefulness of an integrated approach for empirical evaluation of local adaptation in nonmodel species (Sork et al. 2013 ).     

Population genomic analyses reveal possible drivers of population divergence

Recent advances in sequencing technology and efficiency enable new and improved methods to investigate how populations diverge and species evolve. Fungi have relatively small and simple genomes and can often be cultured in the laboratory. Fungal populations can thus be sequenced for a relatively low cost, which makes them ideal for population genomic analyses. In several recent population genomic studies, wild populations of fungal model organisms and human pathogens have been analysed, for example Neurospora crassa (Ellison et al. 2011 ), Saccharomyces uvarum (Almeida et al. 2014 ), Coccidioides spp. (Neafsey et al. 2010 ) and Cryptococcus gatti (Engelthaler et al. 2014 ). In this issue of Molecular Ecology, Branco et al. ( 2015 ) apply population genomic tools to understand population divergence and adaptation in a symbiotic (mycorrhizal) fungus. This study exemplifies the possibilities of diving deeper into the genomic features involved in population divergence and speciation, also for nonmodel organisms, and how molecular and analytical tools will improve our understanding of the patterns and mechanisms that underlie adaptation to habitats, population divergence and dispersal limitation of fungi.     

Mitochondrial DNA mutations in iPS cells: mtDNA integrity as standard iPSC selection criteria?

Somatic cells harbor random heteroplasmic mitochondrial DNA mutations, which are considered to contribute to aging. In this issue of The EMBO Journal, Perales‐Clemente et al ( 2016 ) show that mtDNA mutations, present at low levels in the starting fibroblasts, become enriched in iPS cells and lead to functional defects in iPS‐derived cells. In another recent study, Kang et al ( 2016 ) demonstrated that accumulation of mtDNA mutations of somatic origin in iPSCs is age related.     

Mock communities highlight the diversity of host‐associated eukaryotes

Host‐associated microbes are ubiquitous. Every multicellular eukaryote, and even many unicellular eukaryotes (protists), hosts a diverse community of microbes. High‐throughput sequencing (HTS) tools have illuminated the vast diversity of host‐associated microbes and shown that they have widespread influence on host biology, ecology and evolution (McFall‐Ngai et al. 2013 ). Bacteria receive most of the attention, but protists are also important components of microbial communities associated with humans (Parfrey et al. 2011 ) and other hosts. As HTS tools are increasingly used to study eukaryotes, the presence of numerous and diverse host‐associated eukaryotes is emerging as a common theme across ecosystems. Indeed, HTS studies demonstrate that host‐associated lineages account for between 2 and 12% of overall eukaryotic sequences detected in soil, marine and freshwater data sets, with much higher relative abundances observed in some samples (Ramirez et al. 2014 ; Simon et al. 2015 ; de Vargas et al. 2015 ). Previous studies in soil detected large numbers of predominantly parasitic lineages such as Apicomplexa, but did not delve into their origin [e.g. (Ramirez et al. 2014 )]. In this issue of Molecular Ecology, Geisen et al. ( 2015 ) use mock communities to show that many of the eukaryotic organisms detected by environmental sequencing in soils are potentially associated with animal hosts rather than free‐living. By isolating the host‐associated fraction of soil microbial communities, Geisen and colleagues help explain the surprisingly high diversity of parasitic eukaryotic lineages often detected in soil/terrestrial studies using high‐throughput sequencing (HTS) and reinforce the ubiquity of these host‐associated microbes. It is clear that we can no longer assume that organisms detected in bulk environmental sequencing are free‐living, but instead need to design studies that specifically enumerate the diversity and function of host‐associated eukaryotes. Doing so will allow the field to determine the role host‐associated eukaryotes play in soils and other environments and to evaluate hypotheses on assembly of host‐associated communities, disease ecology and more.     

Enalikter is not an annelid: homology,autapomorphies and the interpretation of problematic fossils

A megacheiran arthropod, Enalikter aphson, was recently described by Siveter et al. (2014) from the mid‐Silurian (late Wenlock) of Herefordshire. Previously, megacheirans had only been recognized from the Cambrian. Struck et al. (2015) considered the body plan of Enalikter to be incompatible with this affinity, arguing that many of the arthropod features were either not present or misinterpreted. Instead, they compared Enalikter to polychaete annelids, identifying characters from numerous polychaete lineages which they considered to be present in Enalikter. A reply to this critique by Siveter et al. (2015) reaffirmed arthropod affinities for Enalikter by presenting additional evidence for key arthropod features, such as arthropodized appendages. Here, we augment Siveter et al. by critically addressing the putative annelid characters of Enalikter presented by Struck et al. and additionally explore the morphological and phylogenetic implications of their hypothesis. We conclude that similarities between Enalikter and polychaetes are superficial and that character combinations proposed by Struck et al. are not present in any annelid, living or extinct. This taxon highlights the importance of using a phylogenetic framework for interpreting fossils that present unusual morphologies, such that proposed shared characters are hypotheses of homology rather than merely phenotypic similarities. Crucially, we argue that autapomorphic characters of subgroups of large taxa (like families or classes within phyla) should not be used to diagnose problematic fossils.     

Integration of microenvironmental and stress signaling antagonizes colorectal cancer progression

Genetic alterations can drive oncogenic events and cancer development. However, this is only half of the story. It is now evident that tumor progression only occurs if powerful stress signaling pathways and microenvironmental signals are overcome. Two recent Nature Cell Biology papers study how niche signals of primary and target organ barriers have to be overridden for oncogenes to allow for colorectal cancer (CRC) initiation and metastasis (Urosevic et al, 2014 ; Whissell et al, 2014 ).     

Trade‐offs and utility of alternative RADseq methods: Reply to Puritz et al.

Puritz et al. provide a review of several RADseq methodological approaches in response to our ‘Population Genomic Data Analysis’ workshop (Sept 2013) review (Andrews & Luikart 2014). We agree with Puritz et al. on the importance for researchers to thoroughly understand RADseq library preparation and data analysis when choosing an approach for answering their research questions. Some of us are currently using multiple RADseq protocols, and we agree that the different methods may offer advantages in different cases. Our workshop review did not intend to provide a thorough review of RADseq because the workshop covered a broad range of topics within the field of population genomics. Similarly, neither the response of Puritz et al. nor our comments here provide sufficient space to thoroughly review RADseq. Nonetheless, here we address some key points that we find unclear or potentially misleading in their evaluation of techniques.     

Ready,Set…Poised!: Polycomb target genes are bound by poised RNA polymerase II throughout differentiation

In embryonic stem cells (ESCs), silent genes with major developmental functions display a unique epigenetic state in which strong and broad binding by Polycomb repressive complexes (PRCs) is accompanied by the presence of poised RNA polymerase II (RNAPII) and activating histone marks (e.g. H3K4me3) (Azuara et al, 2006 ; Bernstein et al, 2006 ; Stock et al, 2007 ; Brookes et al, 2012 ). It has been suggested that the plasticity and broad differentiation potential of pluripotent cells might rely, at least partly, on this unique epigenetic state (Bernstein et al, 2006 ; Stock et al, 2007 ). In their recent study, Pombo and colleagues (Ferrai et al, 2017 ) show that a similar epigenetic state can be found at a subset of major developmental genes throughout the differentiation of ESCs into neurons, providing novel and exciting insights into the molecular basis of cellular plasticity in differentiated cells.     

Prmt5: a guardian of the germline protects future generations

Primordial germ cells (PGCs) are the embryonic precursors of the germ cell lineage that form sperm and egg cells. It is of great importance to preserve the germline from DNA damage and potentially from epimutations in order to ensure the survival of future generations. Recent research highlights the role of the protein arginine methyltransferase 5 (PRMT5) as an important player in DNA protection during germline development in the mouse (Kim et al, 2014 & Li et al, 2015 ).     

A tale of two lineages: unexpected,long‐term persistence of the amphibian‐killing fungus in Brazil

For the past 17 years, scientists have been compiling a list of amphibian species susceptible to infection by the amphibian‐killing chytrid fungus, Batrachochytrium dendrobatidis (Bd), all over the world, with >500 species infected on every continent except Antarctica (Olson et al. 2013 ). Where Bd has been found, the impacts on amphibians has been one of two types: either Bd arrives into a naïve amphibian population followed by a mass die‐off and population declines (e.g. Lips et al. 2006 ), or Bd is present at some moderate prevalence, usually infecting many species but at apparently nonlethal intensities for a long time. In this issue of Molecular Ecology, Rodriguez et al. ( 2014 ) discover that the Atlantic Coastal Forest of Brazil is home to two Bd lineages: the Global Pandemic Lineage (Bd‐GPL) – the strain responsible for mass die‐offs and population declines – and a lineage endemic to Brazil (Bd‐Bz). Even more surprising was that both lineages have been present in this area for the past 100 years, making these the oldest records of Bd infecting amphibians. The team also described a moderate but steady prevalence of ~20% across all sampled anuran families for over 100 years, indicating that Brazil has been in an enzootic disease state for over a century. Most amphibians were infected with Bd‐GPL, suggesting this lineage may be a better competitor than Bd‐Bz or may be replacing the Bd‐Bz lineage. Rodriguez et al. ( 2014 ) also detected likely hybridization of the two Bd lineages, as originally described by Schloegel et al. ( 2012 ).