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From shallow sands to deep-sea trenches: Towards integrative systematics of Solenogastres (Aplacophora, Mollusca)
From shallow sands to deep-sea trenches: Towards integrative systematics of Solenogastres (Aplacophora, Mollusca)
The marine realm encompasses a plethora of habitats: from light-flooded tropical coral reefs down to chemosynthetic vents and seeps to oceanic trenches several kilometers below the ocean’s surface. Habitat destruction, pollution, and effects of climate change accelerate rates of species extinction and pose a massive threat to marine ecosystems and biodiversity. Lack of baseline knowledge on species diversity is the key shortfall of current biodiversity research and especially prevalent among small-size invertebrates which constitute the larger part of global, metazoan biodiversity. Solenogastres (or Neomeniomorpha), an enigmatic class of molluscs are one of those understudied and neglected marine taxa. Instead of bearing a shell, these worm-shaped molluscs are densely covered in aragonitic spicules (the scleritome). They have been found from the tropics to the poles and occur from shallow waters down to the deep sea, with a peak in diversity along the continental shelfs. Despite their circumglobal occurrence, less than 300 species of Solenogastres have been described during the last 150 years since their first discovery. However, natural history collections alone have been estimated to contain at least ten-times more undescribed species than are currently known. Taxonomy of Solenogastres is bulky, requiring a mosaic of morphological and anatomical characters even for higher classification and is thus considered notoriously complex among zoologists. Novel approaches to characterize solenogaster diversity are urgently needed in order to catch up with discovery rates and modernize the taxonomic process. During my dissertation, I aimed to explore the diversity and evolution of Solenogastres in two understudied marine environments: the shallow-water interstitial habitat (i.e. the pore spaces between sand grains) and the deep oceans beyond the bathyal zone. For this purpose, I developed a novel integrative taxonomic workflow combining morphological characters of traditional taxonomy with DNA barcoding for molecular approaches to species delineation, supplemented with state-of-the-art anatomical 3D reconstructions of selected key lineages. My dissertation research is based on Solenogastres collected by colleagues and myself during sampling trips targeting marine interstitial malacofauna in Bermuda, Hawaii, Azores, Honshu and Okinawa (Japan). I joined two out of a series of four international deep-sea expeditions collecting benthic fauna in the Northwest Pacific, sampling across a depth range from 1,600 m down to almost 10,000 m in the Kuril-Kamchatka Trench. Overall, these expeditions covered different areas in the Northwest Pacific of varying geological age and stages of isolation. Additional material was made available through the natural history collection of the Section Mollusca, Bavarian State Collection of Zoology (SNSB-ZSM München), resulting in a total of 347 Solenogastres investigated during the course of my dissertation. Based on my work we are now able to identify main clades of meiofaunal Solenogastres, in a first step towards elucidating their global diversity of the clade in the interstitial habitat. The discovery of a putative widely distributed mesopsammic lineage of Dondersiidae (order Pholidoskepia) at sampling sites in the Atlantic and Pacific is challenged by the presence of co-occurring morphologically cryptic species revealed through anatomical 3D reconstructions. This highlights 1.) the risk of chimeric species descriptions if several individuals are used to extract all sets of taxonomically relevant characters and 2.) the importance of molecular data to reliably test hypothesis on conspecificity and distribution patterns in this taxonomically challenging group. Northwest Pacific Solenogastres were delineated based on unique morphological characters (i.e. scleritome data) and, if possible, cross-validated via molecular-based phylogenetic analyses. This integrative approach resulted in 60 candidate species across regions and depth zones in the Northwest Pacific (additional 13 candidate species lack molecular data), with the majority constituting species new to science. Their diversity covers all four orders, at least nine families, and 15 genera – therein presenting an immense boost in regional diversity. On a global scale, the number of abyssal Solenogastres has been more than doubled by these studies, and the animals collected from the bottom of the Kuril-Kamchatka Trench provide the first evidence of this molluscan class from the hadal zone and hold its depth record at almost 10,000 meters. The established baseline dataset of alpha-diversity from adjacent areas and depths zones enabled a first glimpse into distribution patterns. While there was overall little faunal overlap between the investigated regions and depths, several unique links were revealed: 1.) across depth by an eurybathic species occurring in the Kuril Basin (3,350 m) and at the bottom of the trench (9,580 m); 2) across the Kuril-Kamchatka Trench: Kruppomenia genslerae Ostermair, Brandt, Haszprunar, Jörger & Bergmeier, 2018 was found in the Sea of Okhotsk and on the open abyssal plain, thereby indicating that a hadal trench does not pose an insurmountable dispersal barrier for benthic invertebrates; and 3) potentially across oceans: anatomical investigations suggest that an abyssal species from the Atlantic is also present on the Northwest Pacific Plain, albeit molecular data from the putative Atlantic conspecifics to support pan-oceanic distribution is lacking. In order to gain insights into the feeding ecology of deep-sea Solenogastres, we sequenced their gut contents from genomic DNA extracts. This molecular-based approach showed that they are highly specialized micropredators with taxon-specific prey preferences. While anthozoan and hydrozoan cnidarians have been generally assumed as the main food source of Solenogastres, Siphonophora, Nemertea, Annelida and Bivalvia have now been added to their menu. The molecular phylogeny used as a backbone for our integrative approach to characterize their diversity has also several implications for solenogaster systematics. As two fast evolving mitochondrial markers were used in its analyses, without counterbalancing conservative markers the phylogeny cannot reliably resolve deep relationships within a group that has been hypothesized to date back to the early Paleozoic. Nevertheless, as our dataset contains multiple species and genera across several families, we were able to test the validity of existing taxonomic units: several classificatory entities (i.e. the largest order Cavibelonia, families Acanthomeniidae and Pruvotinidae) were retrieved as polyphyletic which will thus necessitate major systematic revisions in the future. The integrative approach developed during my dissertation allows for fast and efficient species delineation. Scleritome characters were chosen as the main morphological trait, as they are comparatively easy to access and provide the necessary link to the existing classificatory system to prevent a parallel system of DNA-based taxonomy. At the same time, reducing the amount of required characters presents an efficient solution when confronted with small-sized animals and high proportions of singletons that hamper the use of single individuals for multiple lines of investigation (e.g. morphology, anatomy, DNA). The set-up of our community-curated online database AplacBase currently serves as an openly accessible repository and initial identification tool, providing supporting information and guiding researchers through the essence of aplacophoran taxonomy. However, in order to overcome the taxonomic deficits prevalent in Solenogastres, novel approaches need to aim beyond the characterization of their diversity and consequently provide efficient solutions to the currently complicated process of species descriptions and diagnosis. Based on a backbone phylogeny stabilized by mitochondrial genomes, a streamlined approach combining “deep taxonomy” with rapid, DNA-based taxonomy is proposed to tackle the emerging wealth of novel Solenogastres species.
Solenogastres, Aplacophora, integrative taxonomy, systematics, biodiversity
Bergmeier, Franziska
2021
English
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Bergmeier, Franziska (2021): From shallow sands to deep-sea trenches: Towards integrative systematics of Solenogastres (Aplacophora, Mollusca). Dissertation, LMU München: Faculty of Biology
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Abstract

The marine realm encompasses a plethora of habitats: from light-flooded tropical coral reefs down to chemosynthetic vents and seeps to oceanic trenches several kilometers below the ocean’s surface. Habitat destruction, pollution, and effects of climate change accelerate rates of species extinction and pose a massive threat to marine ecosystems and biodiversity. Lack of baseline knowledge on species diversity is the key shortfall of current biodiversity research and especially prevalent among small-size invertebrates which constitute the larger part of global, metazoan biodiversity. Solenogastres (or Neomeniomorpha), an enigmatic class of molluscs are one of those understudied and neglected marine taxa. Instead of bearing a shell, these worm-shaped molluscs are densely covered in aragonitic spicules (the scleritome). They have been found from the tropics to the poles and occur from shallow waters down to the deep sea, with a peak in diversity along the continental shelfs. Despite their circumglobal occurrence, less than 300 species of Solenogastres have been described during the last 150 years since their first discovery. However, natural history collections alone have been estimated to contain at least ten-times more undescribed species than are currently known. Taxonomy of Solenogastres is bulky, requiring a mosaic of morphological and anatomical characters even for higher classification and is thus considered notoriously complex among zoologists. Novel approaches to characterize solenogaster diversity are urgently needed in order to catch up with discovery rates and modernize the taxonomic process. During my dissertation, I aimed to explore the diversity and evolution of Solenogastres in two understudied marine environments: the shallow-water interstitial habitat (i.e. the pore spaces between sand grains) and the deep oceans beyond the bathyal zone. For this purpose, I developed a novel integrative taxonomic workflow combining morphological characters of traditional taxonomy with DNA barcoding for molecular approaches to species delineation, supplemented with state-of-the-art anatomical 3D reconstructions of selected key lineages. My dissertation research is based on Solenogastres collected by colleagues and myself during sampling trips targeting marine interstitial malacofauna in Bermuda, Hawaii, Azores, Honshu and Okinawa (Japan). I joined two out of a series of four international deep-sea expeditions collecting benthic fauna in the Northwest Pacific, sampling across a depth range from 1,600 m down to almost 10,000 m in the Kuril-Kamchatka Trench. Overall, these expeditions covered different areas in the Northwest Pacific of varying geological age and stages of isolation. Additional material was made available through the natural history collection of the Section Mollusca, Bavarian State Collection of Zoology (SNSB-ZSM München), resulting in a total of 347 Solenogastres investigated during the course of my dissertation. Based on my work we are now able to identify main clades of meiofaunal Solenogastres, in a first step towards elucidating their global diversity of the clade in the interstitial habitat. The discovery of a putative widely distributed mesopsammic lineage of Dondersiidae (order Pholidoskepia) at sampling sites in the Atlantic and Pacific is challenged by the presence of co-occurring morphologically cryptic species revealed through anatomical 3D reconstructions. This highlights 1.) the risk of chimeric species descriptions if several individuals are used to extract all sets of taxonomically relevant characters and 2.) the importance of molecular data to reliably test hypothesis on conspecificity and distribution patterns in this taxonomically challenging group. Northwest Pacific Solenogastres were delineated based on unique morphological characters (i.e. scleritome data) and, if possible, cross-validated via molecular-based phylogenetic analyses. This integrative approach resulted in 60 candidate species across regions and depth zones in the Northwest Pacific (additional 13 candidate species lack molecular data), with the majority constituting species new to science. Their diversity covers all four orders, at least nine families, and 15 genera – therein presenting an immense boost in regional diversity. On a global scale, the number of abyssal Solenogastres has been more than doubled by these studies, and the animals collected from the bottom of the Kuril-Kamchatka Trench provide the first evidence of this molluscan class from the hadal zone and hold its depth record at almost 10,000 meters. The established baseline dataset of alpha-diversity from adjacent areas and depths zones enabled a first glimpse into distribution patterns. While there was overall little faunal overlap between the investigated regions and depths, several unique links were revealed: 1.) across depth by an eurybathic species occurring in the Kuril Basin (3,350 m) and at the bottom of the trench (9,580 m); 2) across the Kuril-Kamchatka Trench: Kruppomenia genslerae Ostermair, Brandt, Haszprunar, Jörger & Bergmeier, 2018 was found in the Sea of Okhotsk and on the open abyssal plain, thereby indicating that a hadal trench does not pose an insurmountable dispersal barrier for benthic invertebrates; and 3) potentially across oceans: anatomical investigations suggest that an abyssal species from the Atlantic is also present on the Northwest Pacific Plain, albeit molecular data from the putative Atlantic conspecifics to support pan-oceanic distribution is lacking. In order to gain insights into the feeding ecology of deep-sea Solenogastres, we sequenced their gut contents from genomic DNA extracts. This molecular-based approach showed that they are highly specialized micropredators with taxon-specific prey preferences. While anthozoan and hydrozoan cnidarians have been generally assumed as the main food source of Solenogastres, Siphonophora, Nemertea, Annelida and Bivalvia have now been added to their menu. The molecular phylogeny used as a backbone for our integrative approach to characterize their diversity has also several implications for solenogaster systematics. As two fast evolving mitochondrial markers were used in its analyses, without counterbalancing conservative markers the phylogeny cannot reliably resolve deep relationships within a group that has been hypothesized to date back to the early Paleozoic. Nevertheless, as our dataset contains multiple species and genera across several families, we were able to test the validity of existing taxonomic units: several classificatory entities (i.e. the largest order Cavibelonia, families Acanthomeniidae and Pruvotinidae) were retrieved as polyphyletic which will thus necessitate major systematic revisions in the future. The integrative approach developed during my dissertation allows for fast and efficient species delineation. Scleritome characters were chosen as the main morphological trait, as they are comparatively easy to access and provide the necessary link to the existing classificatory system to prevent a parallel system of DNA-based taxonomy. At the same time, reducing the amount of required characters presents an efficient solution when confronted with small-sized animals and high proportions of singletons that hamper the use of single individuals for multiple lines of investigation (e.g. morphology, anatomy, DNA). The set-up of our community-curated online database AplacBase currently serves as an openly accessible repository and initial identification tool, providing supporting information and guiding researchers through the essence of aplacophoran taxonomy. However, in order to overcome the taxonomic deficits prevalent in Solenogastres, novel approaches need to aim beyond the characterization of their diversity and consequently provide efficient solutions to the currently complicated process of species descriptions and diagnosis. Based on a backbone phylogeny stabilized by mitochondrial genomes, a streamlined approach combining “deep taxonomy” with rapid, DNA-based taxonomy is proposed to tackle the emerging wealth of novel Solenogastres species.