Jörg U. Hammel

Deep metazoan phylogeny: When different genes tell different stories

Molecular phylogenetic analyses have produced a plethora of controversial hypotheses regarding the patterns of diversification of non-bilaterian animals. To unravel the causes for the patterns of extreme inconsistencies at the base of the metazoan tree of life, we constructed a novel supermatrix containing 122 genes, enriched with non-bilaterian taxa. Comparative analyses of this supermatrix and its two non-overlapping multi-gene partitions (including ribosomal and non-ribosomal genes) revealed conflicting phylogenetic signals. We show that the levels of saturation and long branch attraction artifacts in the two partitions correlate with gene sampling. The ribosomal gene partition exhibits significantly lower saturation levels than the non-ribosomal one. Additional systematic errors derive from significant variations in amino acid substitution patterns among the metazoan lineages that violate the stationarity assumption of evolutionary models frequently used to reconstruct phylogenies. By modifying gene sampling and the taxonomic composition of the outgroup, we were able to construct three different yet well-supported phylogenies. These results show that the accuracy of phylogenetic inference may be substantially improved by selecting genes that evolve slowly across the Metazoa and applying more realistic substitution models. Additional sequence-independent genomic markers are also necessary to assess the validity of the phylogenetic hypotheses.

Independent evolution of striated muscles in cnidarians and bilaterians

Striated muscles are present in bilaterian animals (for example, vertebrates, insects and annelids) and some non-bilaterian eumetazoans (that is, cnidarians and ctenophores). The considerable ultrastructural similarity of striated muscles between these animal groups is thought to reflect a common evolutionary origin. Here we show that a muscle protein core set, including a type II myosin heavy chain (MyHC) motor protein characteristic of striated muscles in vertebrates, was already present in unicellular organisms before the origin of multicellular animals. Furthermore, ‘striated muscle’ and ‘non-muscle’ myhc orthologues are expressed differentially in two sponges, compatible with a functional diversification before the origin of true muscles and the subsequent use of striated muscle MyHC in fast-contracting smooth and striated muscle. Cnidarians and ctenophores possess striated muscle myhc orthologues but lack crucial components of bilaterian striated muscles, such as genes that code for titin and the troponin complex, suggesting the convergent evolution of striated muscles. Consistently, jellyfish orthologues of a shared set of bilaterian Z-disc proteins are not associated with striated muscles, but are instead expressed elsewhere or ubiquitously. The independent evolution of eumetazoan striated muscles through the addition of new proteins to a pre-existing, ancestral contractile apparatus may serve as a model for the evolution of complex animal cell types.

The contractile sponge epithelium sensu lato – body contraction of the demosponge Tethya wilhelma is mediated by the pinacoderm

SUMMARY Sponges constitute one of the two metazoan phyla that are able to contract their bodies despite a complete lack of muscle cells. Two competing hypotheses on the mechanisms behind this have been postulated to date: (1) mesohyl-mediated contraction originating from fusiform smooth muscle-like actinocytes (‘myocytes’) and (2) epidermal contraction originating in pinacocytes. No direct support exists for either hypothesis. The question of agonist–antagonist interaction in sponge contraction seems to have been completely neglected so far. In the present study we addressed this by studying sponge contraction kinetics. We also tested both hypotheses by carrying out volumetric studies of 3D synchrotron radiation-based x-ray microtomography data obtained from contracted and expanded specimens of Tethya wilhelma. Our results support the pinacoderm contraction hypothesis. Should mesohyl contraction be present, it is likely to be part of the antagonist system. We conclude that epithelial contraction plays a major role in sponges. Contractile epithelia sensu lato may be regarded as part of the ground pattern of the Metazoa.

Climate change and sexual size dimorphism in an Arctic spider

Climate change is advancing the onset of the growing season and this is happening at a particularly fast rate in the High Arctic. However, in most species the relative fitness implications for males and females remain elusive. Here, we present data on 10 successive cohorts of the wolf spider Pardosa glacialis from Zackenberg in High-Arctic, northeast Greenland. We found marked inter-annual variation in adult body size (carapace width) and this variation was greater in females than in males. Earlier snowmelt during both years of its biennial maturation resulted in larger adult body sizes and a skew towards positive sexual size dimorphism (females bigger than males). These results illustrate the pervasive influence of climate on key life-history traits and indicate that male and female responses to climate should be investigated separately whenever possible.

Gains and losses of coral skeletal porosity changes with ocean acidification acclimation

Ocean acidification is predicted to impact ecosystems reliant on calcifying organisms, potentially reducing the socioeconomic benefits these habitats provide. Here we investigate the acclimation potential of stony corals living along a pH gradient caused by a Mediterranean CO2 vent that serves as a natural long-term experimental setting. We show that in response to reduced skeletal mineralization at lower pH, corals increase their skeletal macroporosity (features >10 μm) in order to maintain constant linear extension rate, an important criterion for reproductive output. At the nanoscale, the coral skeletons structural features are not altered. However, higher skeletal porosity, and reduced bulk density and stiffness may contribute to reduce population density and increase damage susceptibility under low pH conditions. Based on these observations, the almost universally employed measure of coral biomineralization, the rate of linear extension, might not be a reliable metric for assessing coral health and resilience in a warming and acidifying ocean.

Sponge budding is a spatiotemporal morphological patterning process: Insights from synchrotron radiation-based x-ray microtomography into the asexual reproduction of Tethya wilhelma

BackgroundPrimary agametic-asexual reproduction mechanisms such as budding and fission are present in all non-bilaterian and many bilaterian animal taxa and are likely to be metazoan ground pattern characters. Cnidarians display highly organized and regulated budding processes. In contrast, budding in poriferans was thought to be less specific and related to the general ability of this group to reorganize their tissues. Here we test the hypothesis of morphological pattern formation during sponge budding.ResultsWe investigated the budding process in Tethya wilhelma (Demospongiae) by applying 3D morphometrics to high resolution synchrotron radiation-based x-ray microtomography (SR-μCT) image data. We followed the morphogenesis of characteristic body structures and identified distinct morphological states which indeed reveal characteristic spatiotemporal morphological patterns in sponge bud development. We discovered the distribution of skeletal elements, canal system and sponge tissue to be based on a sequential series of distinct morphological states. Based on morphometric data we defined four typical bud stages. Once they have reached the final stage buds are released as fully functional juvenile sponges which are morphologically and functionally equivalent to adult specimens.ConclusionOur results demonstrate that budding in demosponges is considerably more highly organized and regulated than previously assumed. Morphological pattern formation in asexual reproduction with underlying genetic regulation seems to have evolved early in metazoans and was likely part of the developmental program of the last common ancestor of all Metazoa (LCAM).

Micro-CT at the imaging beamline P05 at PETRA III

The Imaging Beamline (IBL) P05 is operated by the Helmholtz-Zentrum Geesthacht and located at the DESY storage ring PETRA III. IBL is dedicated to X-ray full field imaging and consists of two experimental end stations. A micro tomography end station equipped for spatial resolutions down to 1 µm and a nano tomography end station for spatial resolutions down to 100 nm. The micro tomography end station is in user operation since 2013 and offers imaging with absorption contrast, phase enhanced absorption contrast and phase contrast methods. We report here on the current status and developments of the micro tomography end station including technical descriptions and show examples of research performed at P05.

P05 imaging beamline at PETRA III: first results

The imaging beamline (IBL/P05) operated by Helmholtz Zentrum Geesthacht (HZG) at the DESY PETRA III storage ring consists of two experimental stations: A micro tomography and a nano tomography end station. Here an overview of the experimental setups and the data acquisition will be given. In addition some first results out of the wide range of applications using the micro tomography station at P05 will be shown. Furthermore, we present first results of the nano tomography end station. These were obtained with an x–ray microscopy setup, which currently operates at energies of 17.4 and 30 keV using polymer compound refractive lenses (CRLs) and rolled prism lenses. Taken together these results clearly show the high potential of the newly built imaging beamline IBL.

Myoanatomy of the velvet worm leg revealed by laboratory-based nanofocus X-ray source tomography

Significance X-ray computed tomography (CT) imaging has become popular for investigating, nondestructively and three-dimensionally, both external and internal structures of various specimens. However, the limited resolution of conventional laboratory-based CT systems (≥500 nm) still hampers the detailed visualization of features on the low nanometer level. We present a laboratory CT device and data processing pipeline to routinely and efficiently generate high-resolution 3D data (≈100 nm) without requiring synchrotron radiation facilities. Our setup is especially relevant for conducting detailed analysis of very small biological samples, as demonstrated for a walking appendage of a velvet worm. Comparative analyses of our CT data with those obtained from other popular imaging methods highlight the advantages and future applicability of the nanoCT setup. X-ray computed tomography (CT) is a powerful noninvasive technique for investigating the inner structure of objects and organisms. However, the resolution of laboratory CT systems is typically limited to the micrometer range. In this paper, we present a table-top nanoCT system in conjunction with standard processing tools that is able to routinely reach resolutions down to 100 nm without using X-ray optics. We demonstrate its potential for biological investigations by imaging a walking appendage of Euperipatoides rowelli, a representative of Onychophora—an invertebrate group pivotal for understanding animal evolution. Comparative analyses proved that the nanoCT can depict the external morphology of the limb with an image quality similar to scanning electron microscopy, while simultaneously visualizing internal muscular structures at higher resolutions than confocal laser scanning microscopy. The obtained nanoCT data revealed hitherto unknown aspects of the onychophoran limb musculature, enabling the 3D reconstruction of individual muscle fibers, which was previously impossible using any laboratory-based imaging technique.

Capture of Prey, Feeding, and Functional Anatomy of the Jaws in Velvet Worms (Onychophora)

Onychophorans are carnivorous, terrestrial invertebrates that occur in tropical and temperate forests of the Southern Hemisphere and around the Equator. Together with tardigrades, onychophorans are regarded as one of the closest relatives of arthropods. One of the most peculiar features of onychophorans is their hunting and feeding behavior. These animals secrete a sticky slime, which is ejected via a pair of slime-papillae, to entangle the prey. After the prey has been immobilized, its cuticle is punctured using a pair of jaws located within the mouth. These jaws constitute internalized appendages of the second body segment and are innervated by the deutocerebrum; thus, they are homologous to the chelicerae of chelicerates, and to the (first) antennae of myriapods, crustaceans, and insects. The jaws are also serial homologs of the paired claws associated with each walking limb of the trunk. The structure of the jaws is similar in representatives of the two major onychophoran subgroups, the Peripatidae and Peripatopsidae. Each jaw is characterized by an outer and an inner blade; while the outer blade consists only of a large principal tooth and up to three accessory teeth, the inner blade bears numerous additional denticles. These denticles are separated from the remaining part of the inner jaw by a diastema and a soft membrane only in peripatids. The onychophoran jaws are associated with large apodemes and specialized muscles that enable their movement. In contrast to the mandibles of arthropods, the onychophoran jaws are moved along, rather than perpendicular to, the main axis of the body. Our elemental analysis reveals an increased incorporation of calcium at the tip of each blade, which might provide rigidity, whereas there is no evidence for incorporation of metal or prominent mineralization. Stability of the jaw might be further facilitated by the cone-in-cone organization of its cuticle, as each blade consists of several stacked, cuticular elements. In this work, we summarize current knowledge on the jaws of onychophorans, which are a characteristic feature of these animals.