Evolution of Holdfast Diversity and Attachment Strategies of Ediacaran Benthic Macroalgae

Holdfast morphologies and attachment strategies of benthic macroalgae are somewhat flexible and controlled by both the substrate condition and species. Six forms (tapered base, globose holdfast, composite globose holdfast, discoidal holdfast, rhizoids and horizontal rhizomes) of attachment structures of Ediacaran benthic macroalgae are recognized from the early Ediacaran Lantian biota and late Ediacaran Miaohe biota in South China based on functional morphology. Each form is considered either adapted to firm substrates that dominate the Precambrian seafloor, or soft substrates that are more common in the Phanerozoic. The results show a diversification in both holdfast morphology and attachment strategies of macroalgae during the Ediacaran Period. In the early Ediacaran Lantian biota, none of the benthic macroalgae is adapted to soft substrates, while in the late Ediacaran Miaohe biota, a considerable number (41%) of species are adapted to relatively soft substrates. This shift might be an adaptive response to the diversification of macroalgae and a changing substrate condition during the Ediacaran Period: the decline of microbial mats and increase of water content in the sediments in the Ediacaran.

Getting a Grip on the Adhesion Mechanism of Epiphytic Orchids – Evidence From Histology and Cryo-Scanning Electron Microscopy

Plants and animals evolve different attachment structures and strategies for reversible or permanent adhesion to different substrate types. For vascular epiphytes, having the ability to permanently attach to their host plants is essential for establishment and survival. Unlike mistletoe roots, roots of vascular epiphytes do not penetrate the host tissues but instead achieve attachment by growing in close contact to the surface of the substrate. However, the fundamental understanding of the attachment functions of epiphytic roots remains scarce, where majority of studies focused on the general root morphology, their functional properties and the descriptions of associated microbial endophytes. To date, research on attachment strategies in plants is almost entirely limited to climbers. Therefore, this study aims to fill the knowledge gap and elucidate the attachment functions of roots of epiphytic orchids. With the use of histology and high-resolution cryo-scanning electron microscopy (cryo-SEM) technique with freeze fracturing, the intimate root-bark substrate interface of epiphytic orchid Epidendrum nocturnum Jacq was investigated. Results showed a flattened underside of the root upon contact with the substrate surface, and the velamen layer appeared to behave like a soft foam, closely following the contours of the substrate. Root hairs emerged from the outermost velamen layer and entered into the crevices in the substrate, whenever possible. A layer of amorphous substance (glue-like substance) was observed on the surface of the root hairs. Combining the observations from this study and knowledge from previous studies, we hypothesised that epiphytic orchid roots produced a layer of glue-like substance to adhere the root to the substrate. Then root hairs are produced and enter into the voids and crevices of the substrate. This further generates a mechanical interlocking mechanism between root and substrate, thus reinforcing the attachment of the root (and hence the whole plant) to its substrate.

Cells at the Edge: The Dentin–Bone Interface in Zebrafish Teeth

Bone-producing osteoblasts and dentin-producing odontoblasts are closely related cell types, a result from their shared evolutionary history in the ancient dermal skeleton. In mammals, the two cell types can be distinguished based on histological characters and the cells’ position in the pulp cavity or in the tripartite periodontal complex. Different from mammals, teleost fish feature a broad diversity in tooth attachment modes, ranging from fibrous attachment to firm ankylosis to the underlying bone. The connection between dentin and jaw bone is often mediated by a collar of mineralized tissue, a part of the dental unit that has been termed “bone of attachment”. Its nature (bone, dentin, or an intermediate tissue type) is still debated. Likewise, there is a debate about the nature of the cells secreting this tissue: osteoblasts, odontoblasts, or yet another (intermediate) type of scleroblast. Here, we use expression of the P/Q rich secretory calcium-binding phosphoprotein 5 (scpp5) to characterize the cells lining the so-called bone of attachment in the zebrafish dentition. scpp5 is expressed in late cytodifferentiation stage odontoblasts but not in the cells depositing the “bone of attachment”. nor in bona fide osteoblasts lining the supporting pharyngeal jaw bone. Together with the presence of the osteoblast marker Zns-5, and the absence of covering epithelium, this links the cells depositing the “bone of attachment” to osteoblasts rather than to odontoblasts. The presence of dentinal tubule-like cell extensions and the near absence of osteocytes, nevertheless distinguishes the “bone of attachment” from true bone. These results suggest that the “bone of attachment” in zebrafish has characters intermediate between bone and dentin, and, as a tissue, is better termed “dentinous bone”. In other teleosts, the tissue may adopt different properties. The data furthermore support the view that these two tissues are part of a continuum of mineralized tissues. Expression of scpp5 can be a valuable tool to investigate how differentiation pathways diverge between osteoblasts and odontoblasts in teleost models and help resolving the evolutionary history of tooth attachment structures in actinopterygians.

Synchrotron imagery of phosphatized eggs in Waptia cf. W. fieldensis from the middle Cambrian (Miaolingian, Wuliuan) Spence Shale of Utah

Exceptionally preserved fossil eggs and embryos provide critical information regarding paleoembryogenesis, reproductive strategies, and the early ontogeny of early arthropods, but the rarity of preservation of both eggs and egg-bearing organisms in situ limits their use in detailed evolutionary developmental (evo-devo) studies. Burgess Shale-type deposits preserve rare instances of egg-bearing arthropods as carbonaceous compressions; however, the eggs are usually poorly preserved with no compelling evidence of embryos. We describe the first record of a brooding specimen of Waptia cf. W. fieldensis from the Spence Shale, a Cambrian (Wuliuan Stage) Burgess Shale-type deposit in northeastern Utah and southeastern Idaho. This is the first record of an egg-bearing arthropod from the Spence Shale and it exhibits two distinct modes of preservation among eggs within the single clutch: carbonization and phosphatization. Unlike the egg-bearing Burgess Shale specimens, many eggs of this Utah specimen are also preserved three-dimensionally. In addition, synchrotron radiation X-ray tomographic microscopy reveals internal distributions of mineral phases, along with potential remnants of the egg membrane and attachment structures, but, as in the Burgess Shale, no explicit traces of developing embryos. The distinct modes of preservation highlight the existence of diagenetic microenvironments within some eggs, but not in others during fossilization.

Crinoid encrustation of holocystitid diploporitan echinoderms: strongly asymmetrical Silurian dendritic attachment structures with palaeobiological implications

Articulated thecae of the holocystitid diploporitan echinoderm Holocystites scutellatus from the middle Silurian (Wenlock: Sheinwoodian) Massie Formation of southeastern Indiana, USA, are encrusted by distinctive structures belonging to another echinoderm. A dendritic attachment structure consisting of multiple slender, branching radices, attributable to the camerate crinoid Eucalyptocrinites, is present on one side of each of the diploporitan thecae. However, the development of radices is remarkably asymmetrical, with all radices—including one more than 25 mm in length—being present exclusively on one side of the attachment structure. This reflects initial settlement by the encrusting crinoids near the oral or marginal regions rather than the central portion of the diploporitan thecae, which were on their sides; this essentially prohibited further outward growth of radices toward the oral area or edges, but allowed radices oriented in the opposite direction to extend over nearly the entire length of the lateral surface of the theca. Although crinoid encrustation of holocystitid diploporitan thecae is moderately common in the Massie Formation, no previously described specimens display such pronounced asymmetry with respect to radice development. More importantly, these specimens convincingly illustrate the degree to which Eucalyptocrinites attachment structure morphologies could be modified in response to local substrate variations; such skeletal modules were, indeed, highly dynamic, probably contributing to the success of taxa bearing such adaptable attachment structures.

Physical constraints lead to parallel evolution of micro- and nanostructures of animal adhesive pads: a review

Adhesive pads are functional systems with specific micro- and nanostructures which evolved as a response to specific environmental conditions and therefore exhibit convergent traits. The functional constraints that shape systems for the attachment to a surface are general requirements. Different strategies to solve similar problems often follow similar physical principles, hence, the morphology of attachment devices is affected by physical constraints. This resulted in two main types of attachment devices in animals: hairy and smooth. They differ in morphology and ultrastructure but achieve mechanical adaptation to substrates with different roughness and maximise the actual contact area with them. Species-specific environmental surface conditions resulted in different solutions for the specific ecological surroundings of different animals. As the conditions are similar in discrete environments unrelated to the group of animals, the micro- and nanostructural adaptations of the attachment systems of different animal groups reveal similar mechanisms. Consequently, similar attachment organs evolved in a convergent manner and different attachment solutions can occur within closely related lineages. In this review, we present a summary of the literature on structural and functional principles of attachment pads with a special focus on insects, describe micro- and nanostructures, surface patterns, origin of different pads and their evolution, discuss the material properties (elasticity, viscoelasticity, adhesion, friction) and basic physical forces contributing to adhesion, show the influence of different factors, such as substrate roughness and pad stiffness, on contact forces, and review the chemical composition of pad fluids, which is an important component of an adhesive function. Attachment systems are omnipresent in animals. We show parallel evolution of attachment structures on micro- and nanoscales at different phylogenetic levels, focus on insects as the largest animal group on earth, and subsequently zoom into the attachment pads of the stick and leaf insects (Phasmatodea) to explore convergent evolution of attachment pads at even smaller scales. Since convergent events might be potentially interesting for engineers as a kind of optimal solution by nature, the biomimetic implications of the discussed results are briefly presented.

First description ofLotmaria passimandCrithidia mellificaehaptomonad stage in the honeybee hindgut

The remodelling of flagella into attachment structures is a common and important event in the insect stages of the trypanosomatid life cycle. Among their hymenopteran hosts,Lotmaria passimandCrithidia mellificaecan parasitizeApis mellifera, and as a result they might have a significant impact on honeybee health. However, there are details of their life cycle and the mechanisms underlying their pathogenicity in this host that remain unclear. Here we show that bothL. passimpromastigotes andC. mellificaechoanomastigotes differentiate into haptomonad stage covering the ileum and rectum of honeybees. These haptomonad cells remain attached to the host surface via zonular hemidesmosome-like structures, as revealed by Transmission Electron Microscopy. Hence, for the first time this work describes the haptomonad morphotype of these species and their hemidesmosome-like attachment inApis mellifera, a key trait exploited by other trypanosomatid species to proliferate in the insect host hindgut.Author summaryIn recent years, the mortality of European Honeybees (Apis mellifera) has risen worldwide due to a variety of factors, including their infection by parasites. Former studies have linked the presence of several trypanosomatids species, beingLotmaria passimandCrithidia mellificaethe most prevalent ones, with this increase in mortality. Although previous studies have shown that trypanosomatid infection reduces the lifespan of bees, there is little information regarding their development in the gut when honeybees become infected. Here, for the first time we describe the haptomonad morphotype of these two trypanosomatid species inA. mellifera. The most characteristic feature of haptomonads is the extensive remodelling of the flagellum and the formation of junctional complexes at the host gut wall. The presence of this morphotype in the honeybee hindgut increases our understanding of the life cycle of these species and their possible pathogenic mechanisms. We found that they can multiply while attached and that their disposition, covering the hindgut walls, could hinder host nutrient uptake and consequently, represent a pathogenic mechanism itself. This attachment could also be a key stage in the life-cycle to prevent the trypanosomatids leaving the host prematurely, ensuring transmission through infective morphotypes.

Role of legs and foot adhesion in salticid spiders jumping from smooth surfaces

Many spiders and insects can perform rapid jumps from smooth plant surfaces. Here, we investigate how jumping spiders (Pseudeuophrys lanigera and Sitticus pubescens) avoid slipping when accelerating. Both species differed in the relative contribution of leg pairs to the jump. P. lanigera accelerated mainly with their long third legs, whereas their short fourth legs detached earlier. In contrast, S. pubescens accelerated mainly with their long fourth legs, and their short third legs detached earlier. Because of the different orientation (fourth-leg tip pointing backward, third-leg tip pointing forward), the fourth-leg tarsus pushed, whereas the third-leg tarsus pulled. High-speed video recordings showed that pushing and pulling was achieved by different attachment structures. In P. lanigera, third-leg feet made surface contact with setae on their distal or lateral claw tuft, whereas fourth-leg feet engaged the proximal claw tuft, and the distal tuft was raised off the ground. S. pubescens showed the same division of labour between proximal and distal claw tuft for pushing and pulling, but the claw tuft contact lasted longer and was more visible in the fourth than in the third legs. Experimental ablation of claw tufts caused accelerating spiders to slip, confirming that adhesion is essential for jumps from smooth substrates.

Evolution of Silk Anchor Structure as the Joint Effect of Spinning Behavior and Spinneret Morphology

Synopsis Spider web anchors are attachment structures composed of the bi-phasic glue-fiber secretion from the piriform silk glands. The mechanical performance of the anchors strongly correlates with the structural assembly of the silk lines, which makes spider silk anchors an ideal system to study the biomechanical function of extended phenotypes and its evolution. It was proposed that silk anchor function guided the evolution of spider web architectures, but its fine-structural variation and whether its evolution was rather determined by changes of the shape of the spinneret tip or in the innate spinning choreography remained unresolved. Here, we comparatively studied the micro-structure of silk anchors across the spider tree of life, and set it in relation to spinneret morphology, spinning behavior and the ecology of the spider. We identified a number of apomorphies in the structure of silk anchors that may positively affect anchor function: (1) bundled dragline, (2) dragline envelope, and (3) dragline suspension (“bridge”). All these characters were apomorphic and evolved repeatedly in multiple lineages, supporting the notion that they are adaptive. The occurrence of these structural features can be explained with changes in the shape and mobility of the spinneret tip, the spinning behavior, or both. Spinneret shapes generally varied less than their fine-tuned movements, indicating that changes in construction behavior play a more important role in the evolution of silk anchor assembly. However, the morphology of the spinning apparatus is also a major constraint to the evolution of the spinning choreography. These results highlight the changes in behavior as the proximate and in morphology as the ultimate causes of extended phenotype evolution. Further, this research provides a roadmap for future bioprospecting research to design high-performance instant line anchors.

Forces at the Anterior Meniscus Attachments Strongly Increase Under Dynamic Knee Joint Loading

Background: The anatomic appearance and biomechanical and clinical importance of the anterior meniscus roots are well described. However, little is known about the loads that act on these attachment structures under physiological joint loads and movements. Hypotheses: As compared with uniaxial loading conditions under static knee flexion angles or at very low flexion-extension speeds, more realistic continuous movement simulations in combination with physiological muscle force simulations lead to significantly higher anterior meniscus attachment forces. This increase is even more pronounced in combination with a longitudinal meniscal tear or after total medial meniscectomy. Study Design: Controlled laboratory study. Methods: A validated Oxford Rig–like knee simulator was used to perform a slow squat, a fast squat, and jump landing maneuvers on 9 cadaveric human knee joints, with and without muscle force simulation. The strains in the anterior medial and lateral meniscal periphery and the respective attachments were determined in 3 states: intact meniscus, medial longitudinal tear, and total medial meniscectomy. To determine the attachment forces, a subsequent in situ tensile test was performed. Results: Muscle force simulation resulted in a significant strain increase at the anterior meniscus attachments of up to 308% ( P < .038) and the anterior meniscal periphery of up to 276%. This corresponded to significantly increased forces ( P < .038) acting in the anteromedial attachment with a maximum force of 140 N, as determined during the jump landing simulation. Meniscus attachment strains and forces were significantly influenced ( P = .008) by the longitudinal tear and meniscectomy during the drop jump simulation. Conclusion: Medial and lateral anterior meniscus attachment strains and forces were significantly increased with physiological muscle force simulation, corroborating our hypothesis. Therefore, in vitro tests applying uniaxial loads combined with static knee flexion angles or very low flexion-extension speeds appear to underestimate meniscus attachment forces. Clinical Relevance: The data of the present study might help to optimize the anchoring of meniscal allografts and artificial meniscal substitutes to the tibial plateau. Furthermore, this is the first in vitro study to indicate reasonable minimum stability requirements regarding the reattachment of torn anterior meniscus roots.