Computer-based three-dimensional reconstruction of the anatomy ofMicrohedyle remanei (Marcus, 1953), an interstitial acochlidian gastropod from Bermuda

Abstract

Phylogenetic analysis of the highly enigmatic and aberrant acochlidian opisthobranch gastropods is mainly hindered by the lack of reliable anatomical data. Due to their small size, marine interstitial acochlidian species are not suitable for anatomical investigations by dissecting. The tinyness and complexity of, e.g., opisthobranch central nervous and reproductive systems make data derived from older paraffin-based histology and interpretation by hand-based graphical reconstruction questionable. In a former study, a hermaphroditic member of the basal acochlidian genus Hedylopsis ("Hedylopsacea") has been examined in detail. The present study uses the gonochoric Microhedyle remanei (Microhedylidae) as a model organism of the other traditional major acochlidian subgroup, the "Microhedylacea." More than 20 specimens with up to 2 mm body length were extracted from coarse subtidal sand near Castle Roads, Bermuda Islands. Their central nervous, digestive, circulatory, excretory, and genital systems were reconstructed three-dimensionally from serial semithin histological sections using AMIRA software. The radula was analyzed by SEM. Our specimens closely resemble the original description of M. remanei (Marcus, 1953; as Unela) from Brazil; apparent differences regarding the number of visceral loop ganglia or details of male genitalia are assumed to be due to oversights by the former author or because of different ontogenetic stages. Microhedyle remanei differs from all congeners due to the lack (vs. presence) of eyes; further distinguishing features are discussed. In contrast to members of the hedylopsacean Hedylopsidae, Acochlidiidae, and Tantulidae, M. remanei shows a nervous system with numerous precerebral accessory "ganglia" that are not differentiated into cortex and medulla. While all Microhedylidae previously were thought to lack a heart, M. remanei shows a two-chambered heart, as is usual for opisthobranchs. The oocytes of M. remanei are yolky and large in relation to body size and suggest intracapsular larval development. A comparative microanatomical discussion and the distribution of characters within acochlidian taxa indicate that the current classification of the Acochlidia does not reflect phylogenetic relationships. Detailed structural investigations on further poorly known species are required; the computer-based 3D reconstruction of semithin serial sections with AMIRA is shown to be an ideal tool for efficient analysis and presentation of the microanatomy of small specimens.

Flashback and foreshadowing—a review of the taxon Opisthobranchia

“…Wägele and Cervera 2001;Göbbeler and Klussmann-Kolb 2010b), ideally combined with full, software-aided 3D microanatomical reconstructions (e.g. Neusser et al 2006), paved the way for comparative studies across euthyneurans (e.g., Rückert et al 2008;Neusser et al 2009bNeusser et al , 2011aGolding 2010;Wägele et al 2010;Brenzinger et al 2011a, b;Eder et al 2011;Haszprunar et al 2011;Kohnert et al 2013). For example, Brenzinger et al (2013a) could show that the close affinities of Rhodopemorpha with "lower heterobranchs" related to Murchisonellidae, and morphological features similar to Doridoidea, are due to convergences.…”

Embedding 3D models of biological specimens in PDF publications

“…) and automated procedures (prealignment, generation of final geometric models, etc.) mostly surface (rendering) models of specimens or specimen components are generated (see e.g., Haas et al, 2006;Mashanov et al, 2007;Neusser et al, 2006;Ruthensteiner, 2006;Taguchi and Kohsuke, 2003). These are particularly appropriate as interactive PDF models, since with the aid of the Adobe software 3D Toolkit (included in Acrobat 3D software package) these models can easily be converted to a format suitable for PDF files.…”

Serotonin-like Immunoreactivity in the Central and Peripheral Nervous Systems of the Interstitial AcochlideanAsperspinasp. (Opisthobranchia)

“…Recent investigations of interstitial opisthobranchs have shown the importance of providing a detailed three-dimensional representation of anatomical structure, which allows for a better assessment of organ system homology and function (Sommerfeldt and Schrödl, 2005;Neusser et al, 2006). As stated in both studies, previous investigations of opisthobranch anatomy have relied almost exclusively on traditional histological techniques and in some cases missed or misrepresented important details because of the miniscule size of the organ systems and the lack of fine structural information obtainable from paraffin sections.…”

“…As stated in both studies, previous investigations of opisthobranch anatomy have relied almost exclusively on traditional histological techniques and in some cases missed or misrepresented important details because of the miniscule size of the organ systems and the lack of fine structural information obtainable from paraffin sections. For these reasons, modern studies have relied on a combination of semithin and ultrathin resin sections, electron microscopy, and/or computer-based reconstruction of the major organ systems (Fahrner and Haszprunar, 2002;Sommerfeldt and Schrödl, 2005;Neusser et al, 2006). To date, two species of the order Acochlidia, Hedylopsis ballantinei Sommerfeldt and Schrödl, 2005, and Microhedyle remanei (Marcus, 1953), have been examined using some combination of these techniques, revealing a wealth of new information on the structure of the digestive tract, reproductive system, and central nervous system.…”

“…To date, two species of the order Acochlidia, Hedylopsis ballantinei Sommerfeldt and Schrödl, 2005, and Microhedyle remanei (Marcus, 1953), have been examined using some combination of these techniques, revealing a wealth of new information on the structure of the digestive tract, reproductive system, and central nervous system. The structure of the nervous system is especially important because of its conservative nature in higher molluscan taxa (e.g., Bargmann, 1930;Bishop, 1978;Haszprunar and Huber, 1990), and among acochlidean opisthobranchs may provide clues to their origins and phylogenetic status (Neusser et al, 2006). To date, there is little evidence to suggest monophyly of the Acochlidea, as many of the hypothesized synapomorphies, such as the absence of a shell and the production of spicules, may be viewed as convergent adaptations to an interstitial lifestyle (reviewed by Swedmark, 1968).…”