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"Gastropoda - anatomy "
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Phylogenomics reveals deep molluscan relationships
When molluscs got ahead
The Mollusca are one of the most successful animal phyla — ubiquitous, varied in body plan and with a long fossil record. Their interrelationships have been a matter of debate, but phylogenomic methods are beginning to resolve the issue. A new study answers some questions about the base of the molluscan tree, showing that, contrary to the traditional view, bivalves and gastropods are members of sister taxa. This finding also raises the possibility that centralization of neural and sensory organs in the head region, and the development of protective shells, may have occurred on several occasions in the evolutionary history of the molluscs.
Evolutionary relationships among the eight major lineages of Mollusca have remained unresolved despite their diversity and importance. Previous investigations of molluscan phylogeny, based primarily on nuclear ribosomal gene sequences
1
,
2
,
3
or morphological data
4
, have been unsuccessful at elucidating these relationships. Recently, phylogenomic studies using dozens to hundreds of genes have greatly improved our understanding of deep animal relationships
5
. However, limited genomic resources spanning molluscan diversity has prevented use of a phylogenomic approach. Here we use transcriptome and genome data from all major lineages (except Monoplacophora) and recover a well-supported topology for Mollusca. Our results strongly support the Aculifera hypothesis placing Polyplacophora (chitons) in a clade with a monophyletic Aplacophora (worm-like molluscs). Additionally, within Conchifera, a sister-taxon relationship between Gastropoda and Bivalvia is supported. This grouping has received little consideration and contains most (>95%) molluscan species. Thus we propose the node-based name Pleistomollusca. In light of these results, we examined the evolution of morphological characters and found support for advanced cephalization and shells as possibly having multiple origins within Mollusca.
Journal Article
Multilevel fine-scale diversity challenges the ‘cryptic species’ concept
‘Cryptic’ species are an emerging biological problem that is broadly discussed in the present study. Recently, a cryptic species definition was suggested for those species which manifest low morphological, but considerable genetic, disparity. As a case study we present unique material from a charismatic group of nudibranch molluscs of the genus
Trinchesia
from European waters to reveal three new species and demonstrate that they show a dual nature: on one hand, they can be considered a ‘cryptic’ species complex due to their overall similarity, but on the other hand, stable morphological differences as well as molecular differences are demonstrated for every species in that complex. Thus, this species complex can equally be named ‘cryptic’, ‘pseudocryptic’ or ‘non-cryptic’. We also present evidence for an extremely rapid speciation rate in this species complex and link the species problem with epigenetics. Available metazoan-wide data, which are broadly discussed in the present study, show the unsuitability of a ‘cryptic’ species concept because the degree of crypticity represents a continuum when a finer multilevel morphological and molecular scale is applied to uncover more narrowly defined species making the ‘cryptic’ addition to ‘species’ redundant. Morphological and molecular methods should be applied in concordance to form a fine-scale multilevel taxonomic framework, and not necessarily implying only an
a posteriori
transformation of exclusively molecular-based ‘cryptic’ species into morphologically-defined ‘pseudocryptic’ ones. Implications of the present study have importance for many fields, including conservation biology and fine-scale biodiversity assessments.
Journal Article
Body-size evolution in gastropods across the Plio-Pleistocene extinction in the western Atlantic
The Plio-Pleistocene turnover event in the western Atlantic following the closure of the Central American Seaway involved high rates of extinction for both gastropod and bivalve molluscs. This extinction was associated with declining nutrient conditions and has been presumed to be associated with a decrease in molluscan body size. Previous work which has been concordant with this expectation, however, has either focused on bivalves or not considered the effects of the recovery post extinction. In three phylogenetically diverse clades, we found that body-size evolution in gastropods across the turnover event is likely tied to ecology. One clade increased in size, one decreased, and another exhibited no substantial change. Individual species lineages exhibit a mixture of microevolutionary changes from the Pliocene to today. This study indicates that gastropod body-size evolution may be more complex than in bivalves, with ecology and other functional traits playing a significant role. Macroevolutionary processes, especially whether a clade re-radiated post extinction, were found to be important. Indeed, a low portion of extant diversity consists of survivors from clades that increased in size or have similar size distributions among their species relative to the Pliocene.
Journal Article
The Central Paratethys Sea—rise and demise of a Miocene European marine biodiversity hotspot
The Miocene Climate Optimum (MCO, ~ 17–14 Ma) was a time of extraordinary marine biodiversity in the Circum-Mediterranean Region. This boom is best recorded in the deposits of the vanished Central Paratethys Sea, which covered large parts of central to southeastern Europe. This sea harbored an extraordinary tropical to subtropical biotic diversity. Here, we present a georeferenced dataset of 859 gastropod species and discuss geodynamics and climate as the main drivers to explain the changes in diversity. The tectonic reorganization around the Early/Middle Miocene boundary resulted in the formation of an archipelago-like landscape and favorable conditions of the MCO allowed the establishment of coral reefs. Both factors increased habitat heterogeneity, which boosted species richness. The subsequent cooling during the Middle Miocene Climate Transition (~ 14–13 Ma) caused a drastic decline in biodiversity of about 67%. Among the most severely hit groups were corallivorous gastropods, reflecting the loss of coral reefs. Deep-water faunas experienced a loss by 57% of the species due to changing patterns in circulation. The low sea level led to a biogeographic fragmentation reflected in higher turnover rates. The largest turnover occurred with the onset of the Sarmatian when bottom water dysoxia eradicated the deep-water fauna whilst surface waters-dwelling planktotrophic species underwent a crisis.
Journal Article
Growth and morphogenesis of the gastropod shell
Gastropod shell morphologies are famously diverse but generally share a common geometry, the logarithmic coil. Variations on this morphology have been modeled mathematically and computationally but the developmental biology of shell morphogenesis remains poorly understood. Here we characterize the organization and growth patterns of the shell-secreting epithelium of the larval shell of the basket whelk Tritia (also known as Ilyanassa). Despite the larval shell’s relative simplicity, we find a surprisingly complex organization of the shell margin in terms of rows and zones of cells. We examined cell division patterns with EdU incorporation assays and found two growth zones within the shell margin. In the more anterior aperture growth zone, we find that inferred division angles are biased to lie parallel to the shell edge, and these divisions occur more on the margin’s left side. In the more posterior mantle epithelium growth zone, inferred divisions are significantly biased to the right, relative to the anterior–posterior axis. These growth zones, and the left–right asymmetries in cleavage patterns they display, can explain the major modes of shell morphogenesis at the level of cellular behavior. In a gastropod with a different coiling geometry, Planorbella sp., we find similar shell margin organization and growth zones as Tritia, but different left–right asymmetries than we observed in the helically coiled shell of Tritia. These results indicate that differential growth patterns in the mantle edge epithelium contribute to shell shape in gastropod shells and identify cellular mechanisms that may vary to generate shell diversity in evolution.
Journal Article
Origin and significance of two pairs of head tentacles in the radiation of euthyneuran sea slugs and land snails
The gastropod infraclass Euthyneura comprises at least 30,000 species of snails and slugs, including nudibranch sea slugs, sea hares and garden snails, that flourish in various environments on earth. A unique morphological feature of Euthyneura is the presence of two pairs of sensory head tentacles with different shapes and functions: the anterior labial tentacles and the posterior rhinophores or eyestalks. Here we combine molecular phylogenetic and microanatomical evidence that suggests the two pairs of head tentacles have originated by splitting of the original single tentacle pair (with two parallel nerve cords in each tentacle) as seen in many other gastropods. Minute deep-sea snails of
Tjaernoeia
and
Parvaplustrum
, which in our phylogeny belonged to the euthyneurans’ sister group (new infraclass Mesoneura), have tentacles that are split along much of their lengths but associated nerves and epidermal sense organs are not as specialized as in Euthyneura. We suggest that further elaboration of cephalic sense organs in Euthyneura closely coincided with their ecological radiation and drastic modification of body plans. The monotypic family Parvaplustridae nov., superfamily Tjaernoeioidea nov. (Tjaernoeiidae + Parvaplustridae), and new major clade Tetratentaculata nov. (Mesoneura nov. + Euthyneura) are also proposed based on their phylogenetic relationships and shared morphological traits.
Journal Article
An Ochered Fossil Marine Shell From the Mousterian of Fumane Cave, Italy
A scanty but varied ensemble of finds challenges the idea that Neandertal material culture was essentially static and did not include symbolic items. In this study we report on a fragmentary Miocene-Pliocene fossil marine shell, Aspamarginata, discovered in a Discoid Mousterian layer of the Fumane Cave, northern Italy, dated to at least 47.6-45.0 Cal ky BP. The shell was collected by Neandertals at a fossil exposure probably located more than 100 kms from the site. Microscopic analysis of the shell surface identifies clusters of striations on the inner lip. A dark red substance, trapped inside micropits produced by bioeroders, is interpreted as pigment that was homogeneously smeared on the outer shell surface. Dispersive X-ray and Raman analysis identify the pigment as pure hematite. Of the four hypotheses we considered to explain the presence of this object at the site, two (tool, pigment container) are discarded because in contradiction with observations. Although the other two (\"manuport\", personal ornament) are both possible, we favor the hypothesis that the object was modified and suspended by a 'thread' for visual display as a pendant. Together with contextual and chronometric data, our results support the hypothesis that deliberate transport and coloring of an exotic object, and perhaps its use as pendant, was a component of Neandertal symbolic culture, well before the earliest appearance of the anatomically modern humans in Europe.
Journal Article
SlugAtlas, a histological and 3D online resource of the land slugs Deroceras laeve and Ambigolimax valentianus
Due to their distinctive anatomical characteristics, land slugs are appealing research subjects from a variety of angles, including stem cell biology, regeneration, embryonic development, allometry, and neurophysiology. Here we present SlugAtlas, an anatomical and histological online resource of the land slugs Deroceras laeve and Ambigolimax valentianus . The atlas is composed of series of histological sections on the horizontal, sagittal, and transversal planes for both species with 3D viewing tools of their major organs. The atlas was used in this work for a comparative analysis of the major organs and tissues of these two species. We provide a comprehensive histological description of them and an explanation of novel findings of unique features of their anatomy. For D . laeve , we additionally studied its ability for degrowth and regrowth, a feature that characterizes animals with high regeneration potential and obtained initial results on the study of the regeneration of its tail. SlugAtlas is a resource that is also built to accommodate future growth and, along with the experimental techniques that we have developed, will provide the foundation for research projects in a variety of biological domains.
Journal Article
Finite element analysis relating shape, material properties, and dimensions of taenioglossan radular teeth with trophic specialisations in Paludomidae (Gastropoda)
The radula, a chitinous membrane with embedded tooth rows, is the molluscan autapomorphy for feeding. The morphologies, arrangements and mechanical properties of teeth can vary between taxa, which is usually interpreted as adaptation to food. In previous studies, we proposed about trophic and other functional specialisations in taenioglossan radulae from species of African paludomid gastropods. These were based on the analysis of shape, material properties, force-resistance, and the mechanical behaviour of teeth, when interacting with an obstacle. The latter was previously simulated for one species (
Spekia zonata
) by the finite-element-analysis (FEA) and, for more species, observed in experiments. In the here presented work we test the previous hypotheses by applying the FEA on 3D modelled radulae, with incorporated material properties, from three additional paludomid species. These species forage either on algae attached to rocks (
Lavigeria grandis
), covering sand (
Cleopatra johnstoni
), or attached to plant surface and covering sand (
Bridouxia grandidieriana
). Since the analysed radulae vary greatly in their general size (e.g. width) and size of teeth between species, we additionally aimed at relating the simulated stress and strain distributions with the tooth sizes by altering the force/volume. For this purpose, we also included
S. zonata
again in the present study. Our FEA results show that smaller radulae are more affected by stress and strain than larger ones, when each tooth is loaded with the same force. However, the results are not fully in congruence with results from the previous breaking stress experiments, indicating that besides the parameter size, more mechanisms leading to reduced stress/strain must be present in radulae.
Journal Article