Most animal species reproduce sexually and fully parthenogenetic lineages are usually short lived in evolution. Still, parthenogenesis may be advantageous as it avoids the cost of sex and permits colonization by single individuals. Panagrolaimid nematodes have colonized environments ranging from arid deserts to Arctic and Antarctic biomes. Many are obligatory meiotic parthenogens, and most have cryptobiotic abilities, being able to survive repeated cycles of complete desiccation and freezing. To identify systems that may contribute to these striking abilities, we sequenced and compared the genomes and transcriptomes of parthenogenetic and outcrossing panagrolaimid species, including cryptobionts and non-cryptobionts. The parthenogens are triploids, most likely originating through hybridization. Adaptation to cryptobiosis shaped the genomes of panagrolaimid nematodes and is associated with the expansion of gene families and signatures of selection on genes involved in cryptobiosis. All panagrolaimids have acquired genes through horizontal gene transfer, some of which are likely to contribute to cryptobiosis.

Background: The free-living nematode Diploscapter coronatus is the closest known relative of Caenorhabditis elegans with parthenogenetic reproduction. It shows several developmental idiosyncracies, for example concerning the mode of reproduction, embryonic axis formation and early cleavage pattern (Lahl et al. in Int J Dev Biol 50:393-397, 2006). Our recent genome analysis (Hiraki et al. in BMC Genomics 18:478, 2017) provides a solid foundation to better understand the molecular basis of developmental idiosyncrasies in this species in an evolutionary context by comparison with selected other nematodes. Our genomic data also yielded indications for the view that D. coronatus is a product of interspecies hybridization. Results: In a genomic comparison between D. coronatus, C. elegans, other representatives of the genus Caenorhabditis and the more distantly related Pristionchus pacificus and Panagrellus redivivus, certain genes required for central developmental processes in C. elegans like control of meiosis and establishment of embryonic polarity were found to be restricted to the genus Caenorhabditis. The mRNA content of early D. coronatus embryos was sequenced and compared with similar stages in C. elegans and Ascaris suum. We identified 350 gene families transcribed in the early embryo of D. coronatus but not in the other two nematodes. Looking at individual genes transcribed early in D. coronatus but not in C. elegans and A. suum, we found that orthologs of most of these are present in the genomes of the latter species as well, suggesting heterochronic shifts with respect to expression behavior. Considerable genomic heterozygosity and allelic divergence lend further support to the view that D. coronatus may be the result of an interspecies hybridization. Expression analysis of early acting single-copy genes yields no indication for silencing of one parental genome. Conclusions: Our comparative cellular and molecular studies support the view that the genus Caenorhabditis differs considerably from the other studied nematodes in its control of development and reproduction. The easy-to-culture parthenogenetic D. coronatus, with its high-quality draft genome and only a single chromosome when haploid, offers many new starting points on the cellular, molecular and genomic level to explore alternative routes of nematode development and reproduction.

Sexual reproduction involving the fusion of egg and sperm is prevailing among eukaryotes. In contrast, the nematode Diploscapter coronatus, a close relative of the model Caenorhabditis elegans, reproduces parthenogenetically. Neither males nor sperm have been observed and some steps of meiosis are apparently skipped in this species. To uncover the genomic changes associated with the evolution of parthenogenesis in this nematode, we carried out a genome analysis.

Comparative studies of nematode embryogenesis among different clades revealed considerable variations. However, to what extent developmental differences exist between closely related species has mostly remained nebulous. Here, we explore the correlation between phylogenetic neighborhood and developmental variation in a restricted and morphologically particularly uniform taxonomic group (Panagrolaimidae) to determine to what extent (1) morphological and developmental characters go along with molecular data and thus can serve as diagnostic tools for the definition of kinship and (2) developmental system drift (DSD; modifications of developmental patterns without corresponding morphological changes) can be found within a small taxonomic unit. Our molecular approaches firmly support subdivision of Panagrolaimid nematodes into two monophyletic groups. These can be discriminated by distinct peculiarities in early embryonic cell lineages and a mirror-image expression pattern of the gene skn-1. This suggests major changes in the logic of cell specification and the action of DSD in the studied representatives of the two neighboring nematode taxa.

Biologie in unserer ZeitVolume 44, Issue 2 p. 137-137 Bücher Wunderbare Welt der Ontogenese Einhard Schierenberg, Einhard Schierenberg Universität zu KölnSearch for more papers by this author Einhard Schierenberg, Einhard Schierenberg Universität zu KölnSearch for more papers by this author First published: 15 April 2014 https://doi.org/10.1002/biuz.201490020Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat No abstract is available for this article. Volume44, Issue2April 2014Pages 137-137 RelatedInformation

Background Despite its status as a model organism, the development of Caenorhabditis elegans is not necessarily archetypical for nematodes. The phylum Nematoda is divided into the Chromadorea (indcludes C. elegans) and the Enoplea. Compared to C. elegans, enoplean nematodes have very different patterns of cell division and determination. Embryogenesis of the enoplean Romanomermis culicivorax has been studied in great detail, but the genetic circuitry underpinning development in this species is unknown. Results We created a draft genome of R. culicivorax and compared its developmental gene content with that of two nematodes, C. elegans and Trichinella spiralis (another enoplean), and a representative arthropod Tribolium castaneum. This genome evidence shows that R. culicivorax retains components of the conserved metazoan developmental toolkit lost in C. elegans. T. spiralis has independently lost even more of the toolkit than has C. elegans. However, the C. elegans toolkit is not simply depauperate, as many genes essential for embryogenesis in C. elegans are unique to this lineage, or have only extremely divergent homologues in R. culicivorax and T. spiralis. These data imply fundamental differences in the genetic programmes for early cell specification, inductive interactions, vulva formation and sex determination. Conclusions Thus nematodes, despite their apparent phylum-wide morphological conservatism, have evolved major differences in the molecular logic of their development. R. culicivorax serves as a tractable, contrasting model to C. elegans for understanding how divergent genomic and thus regulatory backgrounds can generate a conserved phenotype. The availability of the draft genome will promote use of R. culicivorax as a research model.

Background The genetics of development in the nematode Caenorhabditis elegans has been described in exquisite detail. The phylum Nematoda has two classes: Chromadorea (which includes C. elegans ) and the Enoplea. While the development of many chromadorean species resembles closely that of C. elegans , enoplean nematodes show markedly different patterns of early cell division and cell fate assignment. Embryogenesis of the enoplean Romanomermis culicivorax has been studied in detail, but the genetic circuitry underpinning development in this species has not been explored. Results We generated a draft genome for R. culicivorax and compared its gene content with that of C. elegans , a second enoplean, the vertebrate parasite Trichinella spiralis , and a representative arthropod, Tribolium castaneum . This comparison revealed that R. culicivorax has retained components of the conserved ecdysozoan developmental gene toolkit lost in C. elegans . T. spiralis has independently lost even more of this toolkit than has C. elegans . However, the C. elegans toolkit is not simply depauperate, as many novel genes essential for embryogenesis in C. elegans are not found in, or have only extremely divergent homologues in R. culicivorax and T. spiralis . Our data imply fundamental differences in the genetic programmes not only for early cell specification but also others such as vulva formation and sex determination. Conclusions Despite the apparent morphological conservatism, major differences in the molecular logic of development have evolved within the phylum Nematoda. R. culicivorax serves as a tractable system to contrast C. elegans and understand how divergent genomic and thus regulatory backgrounds nevertheless generate a conserved phenotype. The R. culicivorax draft genome will promote use of this species as a research model.

The great majority of metazoans belong to bilaterian phyla. They diversified during a short interval in Earth’s history known as the Cambrian explosion, ∼540 million years ago. However, the genetic basis of these events is poorly understood. Here we argue that the vertebrate genome organizer CTCF (CCCTC-binding factor) played an important role for the evolution of bilaterian animals. We provide evidence that the CTCF protein and a genome-wide abundance of CTCF-specific binding motifs are unique to bilaterian phyla, but absent in other eukaryotes. We demonstrate that CTCF-binding sites within vertebrate and Drosophila Hox gene clusters have been maintained for several hundred million years, suggesting an ancient origin of the previously known interaction between Hox gene regulation and CTCF. In addition, a close correlation between the presence of CTCF and Hox gene clusters throughout the animal kingdom suggests conservation of the Hox-CTCF link across the Bilateria. On the basis of these findings, we propose the existence of a Hox-CTCF kernel as principal organizer of bilaterian body plans. Such a kernel could explain ( i ) the formation of Hox clusters in Bilateria, ( ii ) the diversity of bilaterian body plans, and ( iii ) the uniqueness and time of onset of the Cambrian explosion.

Background Recent studies have challenged the widespread view that the pattern of embryogenesis found in Caenorhabditis elegans (clade 9) is characteristic of nematodes in general. To understand this still largely unexplored landscape of developmental events, we set out to examine more distantly related nematodes in detail for temporospatial differences in pattern formation and cell specification. Members of the genus Plectus (clade 6) seem to be suitable candidates to show variety, with certain idiosyncratic features during early development and the convenient availability of cultivatable species. Methods The study was conducted using 4-D lineage analysis, 3-D modeling of developing embryos and laser-induced ablation of individual blastomeres. Results Detailed cell lineage studies of several Plectus species reveal that pattern formation and cell fate assignment differ markedly from C. elegans . Descendants of the first somatic founder cell S1 (AB) - but not the progeny of other founder cells - demonstrate extremely variable spatial arrangements illustrating that here distinct early cell-cell interactions between invariant partners, as found in C. elegans , cannot take place. Different from C. elegans , in Plectus alternative positional variations among early S1 blastomeres resulting in a ‘situs inversus’ pattern, nevertheless give rise to adults with normal left-right asymmetries. In addition, laser ablations of early blastomeres uncover inductions between variable cell partners. Conclusions Our results suggest that embryonic cell specification in Plectus is not correlated with cell lineage but with position. With this peculiarity, Plectus appears to occupy an intermediate position between basal nematodes displaying a variable early development and the C. elegans -like invariant pattern. We suggest that indeterminate pattern formation associated with late, position-dependent fate assignment represents a plesiomorphic character among nematodes predominant in certain basal clades but lost in derived clades. Thus, the behavior of S1 cells in Plectus can be considered an evolutionary relict in a transition phase between two different developmental strategies.

Myolaimus byersi n. sp., a phoretic associate of the crane fly, Limonia (Rhipidia) schwarzi (Diptera: Limoniidae), was recovered from moist and decaying tissue from the crown shaft of a living spindle palm, Hyophorbe verschaffeltii, in southern Florida and is described herein. Dauers were carried in the abdominal folds of male and female L. schwarzi. Examination of the highly mobile crane fly larvae and pupae confirmed that the dauers were externally associated with the cuticle. Dauers from crane flies were culturable to adults on 1/20 strength TSB agar. The association appears to be relatively host specific. SEM studies, early embryonic development, dauers, molecular data and TEM ultrastructural comparisons of the stoma, sensory structures and sperm are used to discuss the relative placement of Myolaimus within the Nematoda. The stoma resembles diplogastrids in being strongly anisomorphic with an enlarged dorsal sector of the stegostom, yet also resembles rhabditids in having three triangular flaps in the metastegostom and matches cephalobs and panagrolaims in having a pharyngeal collar with two sets of three interradial muscles followed by two sets of six adradial muscles. The ultrastructure of the cheilostom epidermis shows a high degree of conservation with several Rhabditida. The sperm of M. byersi n. sp. is nearly identical to that of Caenorhabditis elegans. In early cell division, M. byersi n. sp. is closest to Parascaris equorum followed by C. elegans. Myolaimus apparently represents a divergent lineage that has followed a non-coalescing trajectory for a long time, allowing it to retain some highly conserved characters while also developing some surprisingly unique features, such as a baggy cuticle and males that lack a gubernaculum or spicules.

Background MAP (mitogen-activated protein) kinase activation is a prerequisite for oocyte maturation, ovulation and fertilisation in many animals. In the hermaphroditic nematode Caenorhabditis elegans , an MSP (major sperm protein) dependent pathway is utilised for MAP kinase activation and successive oocyte maturation with extracellular MSP released from sperm acting as activator. How oocyte-to-embryo transition is triggered in parthenogenetic nematode species that lack sperm, is not known. Results We investigated two key elements of oocyte-to-embryo transition, MSP expression and MAP kinase signaling, in two parthenogenetic nematodes and their close hermaphroditic relatives. While activated MAP kinase is present in all analysed nematodes irrespective of the reproductive mode, MSP expression differs. In contrast to hermaphroditic or bisexual species, we do not find MSP expression at the protein level in parthenogenetic nematodes. However, genomic sequence analysis indicates that functional MSP genes are present in several parthenogenetic species. Conclusions We present three alternative interpretations to explain our findings. (1) MSP has lost its function as a trigger of MAP kinase activation and is not expressed in parthenogenetic nematodes. Activation of the MAP kinase pathway is achieved by another, unknown mechanism. Functional MSP genes are required for occasionally emerging males found in some parthenogenetic species. (2) Because of long-term disadvantages, parthenogenesis is of recent origin. MSP genes remained intact during this short intervall although they are useless. As in the first scenario, an unknown mechanism is responsible for MAP kinase activation. (3) The molecular machinery regulating oocyte-to-embryo transition in parthenogenetic nematodes is conserved with respect to C. elegans , thus requiring intact MSP genes. However, MSP expression has been shifted to non-sperm cells and is reduced below the detection limits, but is still sufficient to trigger MAP kinase activation and embryogenesis.

Background The zinc finger (ZF) protein CTCF (CCCTC-binding factor) is highly conserved in Drosophila and vertebrates where it has been shown to mediate chromatin insulation at a genomewide level. A mode of genetic regulation that involves insulators and insulator binding proteins to establish independent transcriptional units is currently not known in nematodes including Caenorhabditis elegans . We therefore searched in nematodes for orthologs of proteins that are involved in chromatin insulation. Results While orthologs for other insulator proteins were absent in all 35 analysed nematode species, we find orthologs of CTCF in a subset of nematodes. As an example for these we cloned the Trichinella spiralis CTCF-like gene and revealed a genomic structure very similar to the Drosophila counterpart. To investigate the pattern of CTCF occurrence in nematodes, we performed phylogenetic analysis with the ZF protein sets of completely sequenced nematodes. We show that three ZF proteins from three basal nematodes cluster together with known CTCF proteins whereas no zinc finger protein of C. elegans and other derived nematodes does so. Conclusion Our findings show that CTCF and possibly chromatin insulation are present in basal nematodes. We suggest that the insulator protein CTCF has been secondarily lost in derived nematodes like C. elegans . We propose a switch in the regulation of gene expression during nematode evolution, from the common vertebrate and insect type involving distantly acting regulatory elements and chromatin insulation to a so far poorly characterised mode present in more derived nematodes. Here, all or some of these components are missing. Instead operons, polycistronic transcriptional units common in derived nematodes, seemingly adopted their function.

The current picture of embryonic development in nematodes is essentially shaped by Caenorhabditis elegans and its close relatives. As their pattern of embryogenesis is rather similar, it is often considered to be representative for the taxon Nematoda as a whole. Here we give for the first time a comprehensive description of embryonic development in an ancestrally diverged nematode. Romanomermis culicivorax differs strikingly from C. elegans with respect to cell division pattern, spatial arrangement of blastomeres and tissue formation. Our study reveals a number of unexpected phenomena. These include (i) unique polar interphase microtubule caps forming in early blastomeres destined to undergo asymmetric cleavages, suggesting the presence of a so far undescribed MTOC; (ii) embryonic cell lineages of reduced complexity with predominantly monoclonal sublineages, generating just a single tissue type; (iii) construction of major parts of the body from duplicating building blocks consisting of rings of cells, a pattern showing some resemblance to segmentation; (iv) prominent differences in cell fate assignment which can be best explained with a global shift affecting all somatic founder cells. In summary, our data indicate that during nematode evolution massive alterations in the developmental program took place of how to generate a juvenile.

In order to evaluate the evolutionary preservation of developmental programs during nematode embryogenesis, we searched for close relatives of the model system Caenorhabditis elegans with deviant patterns.The parthenogenetically reproducing species Diploscapter coronatus shows prominent differences to C. elegans.While in the 2-cell stage of C. elegans a rotation of the nuclear/centrosome complex is found only in the posterior P 1 cell, in D. coronatus cell isolation indicates that rotation takes place in a cell-autonomous manner in both blastomeres, resulting in a linear 4-cell array.In C. elegans, the ABp cell becomes different from its ABa sister via a germlineinduced induction.In D. coronatus, AB daughters do not touch the germline but nevertheless execute different fates, suggesting a cell-autonomous mechanism or signaling over distance.Laser ablation experiments revealed that active migration of the EMS cell is required to transform the linearly ordered blastomeres into a 3-dimensional embryo, and the difference can be most easily explained with a heterochronic shift with respect to cell mobility.In D. coronatus, reversal of cleavage polarity in the germline, typical for C. elegans, is absent.This results in four different transient variants of posterior blastomeres which eventually merge into a single pattern prior to the onset of gastrulation.This merging includes primordial germ cell migrations of variable extent toward the gut precursor cell and suggests a specific cell-cell recognition mechanism.Cell distribution in advanced embryos is essentially indistinguishable between both species.

We have begun to analyze the early embryogenesis of Romanomermis culicivorax, an insect-parasitic nematode phylogenetically distant to Caenorhabditis elegans. Development of R. culicivorax differs from C. elegans in many aspects including establishment of polarity, formation of embryonic axes and the pattern of asymmetric cleavages. Here, a polarity reversal in the germline takes place already in P1 rather than P2, the dorsal–ventral axis appears to be inverted and gut fate is derived from the AB rather than from the EMS blastomere. So far unique for nematodes is the presence of colored cytoplasm and its segregation into one specific founder cell. Normal development observed after experimentally induced abnormal partitioning of pigment indicates that it is not involved in cell specification. Another typical feature is prominent midbodies (MB). We investigated the role of the MB region in the establishment of asymmetry. After its irradiation the potential for unequal cleavage in somatic and germline cells as well as differential distribution of pigment are lost. This indicates a crucial involvement of this region for spindle orientation, positioning, and cytoplasmic segregation. A scenario is sketched suggesting why and how during evolution the observed differences between R. culicivorax and C. elegans may have evolved.

It has been well established that considerable differences exist in the developmental pattern among animal taxa, for instance with respect to how blastomeres perform their early cleavages, how they acquire different fates or how symmetry is formed (Gilbert and Raunio ). Even among relatively closely related species, for instance within sea urchins or tunicates, impressive differences can be found in the pattern of development (Jeffery et al. , Raff ). Nematodes appear to be excellent candidates for a comparative study of early embryogenesis (Schierenberg a). The phylum Nematoda is very old, its origin dating back to the Cambrian (Douzery et al. ), and has many different species (estimates range from tens of thousands to several millions); eggs can develop outside the mother from the first cleavage onward, they are transparent (although to a variable degree), the freshly hatched juveniles appear to have essentially invariant species-specific cell numbers of around  cells (for those species tested so far), many strains can be cultured in the laboratory on simple agar plates, and, last but not least, one of them, Caenorhabditis elegans, has become one of the beststudied model systems. In this chapter, selected aspects of the early embryogenesis of five representatives from different branches of the phylogenetic tree are compared with C. elegans and the impact of the observed differences for evolutionary considerations are discussed. Following a brief reference to phylogeny, basic features of early embryogenesis of C. elegans will be summarised to aid in appreciating the data from other nematodes reported subsequently.