Molecular phylogeography and reproductive biology of the freshwater snail Tarebia granifera in Thailand and Timor (Cerithioidea, Thiaridae): morphological disparity versus genetic diversity

The freshwater thiarid gastropod Tarebia granifera (Lamarck, 1816), including taxa considered either congeneric or conspecific by earlier authors, is widespread and abundant in various lentic and lotic water bodies in mainland and insular Southeast Asia, with its range extending onto islands in the Indo-West-Pacific. This snail is, as one of the most frequent and major first intermediate host, an important vector for digenic trematodes causing several human diseases. As a typical thiarid T. granifera is viviparous and parthenogenetic, with various embryonic stages up to larger shelled juveniles developing within the female’s subhemocoelic (i.e non-uterine) brood pouch. Despite the known conchological disparity in other thiarids as well as this taxon, in Thailand Tarebia has been reported with the occurrence of one species only. In light of the polytypic variations found in shell morphology of freshwater snails in general and this taxon in particular, the lack of a modern taxonomic-systematic revision, using molecular genetics, has hampered more detailed insights to date, for example, into the locally varying trematode infection rates found in populations of Tarebia from across its range in Thailand as well as neighboring countries and areas. Here, we integrate evidence from phylogeographical analyses based on phenotypic variation (shell morphology, using biometry and geometric morphometrics) with highly informative and heterogeneous mtDNA sequence data (from the gene fragments cytochrome c oxidase subunit 1 and 16 S rRNA). We evaluate both the morphological and molecular genetic variation (using several phylogenetic analyses, including haplotype networks and a dated molecular tree), in correlation with differences in the reproductive biology among populations of Tarebia from various water bodies in the north, northwest, central, and south of Thailand, supplementing our respective analyses of parasite infections of this thiarid by cercaria of 15 trematode species, reported in a parallel study. Based on the comparison of topotypical material from the island of Timor, with specimens from 12 locations as reference, we found significant, albeit not congruent variation of both phenotype and genotype in Tarebia granifera, based on 1,154 specimens from 95 Thai samples, representing a geographically wide-ranging, river-based cross-section of this country. Our analyses indicate the existence of two genetically distinct clades and hint at possible species differentiation within what has been traditionally considered as T. granifera. These two lineages started to split about 5 mya, possibly related to marine transgressions forming what became known as biogeographical barrier north of the Isthmus of Kra. Grounded on the site-by-site analysis of individual Tarebia populations, our country-wide chorological approach focussing on the conchologically distinct and genetically diverse lineages of Tarebia allows to discuss questions of this either reflecting subspecific forms versus being distinct species within a narrowly delimited species complex. Our results, therefore, provide the ground for new perspectives on the phylogeography, evolution and parasitology of Thai freshwater gastropods, exemplified here by these highly important thiarids

Effects of land cover and protected areas on flying insect diversity

Widespread insect losses are a critical global problem. Mitigating this problem requires identifying the principal drivers across different taxa and determining which insects are covered by protected areas. However, doing so is hindered by missing information on most species owing to extremely high insect diversity and difficulties in morphological identification. To address this knowledge gap, we used one of the most comprehensive insect DNA metabarcoding data sets assembled (encompassing 31,846 flying insect species) in which data were collected from a network of 75 Malaise traps distributed across Germany. Collection sites encompass gradients of land cover, weather, and climate, along with differences in site protection status, which allowed us to gain broader insights into how insects respond to these factors. We examined changes in total insect biomass, species richness, temporal turnover, and shifts in the composition of taxa, key functional groups (pollinators, threatened species, and invasive species), and feeding traits. Lower insect biomass generally equated to lower richness of all insects and higher temporal turnover, suggesting that biomass loss translates to biodiversity loss and less stable communities. Spatial variability in insect biomass and composition was primarily driven by land cover, rather than weather or climate change. As vegetation and land-cover heterogeneity increased, insect biomass increased by 50% in 2019 and 56% in 2020 and total species richness by 58% and 33%, respectively. Similarly, areas with low-vegetation habitats exhibited the highest richness of key taxa, including pollinators and threatened species, and the widest variety of feeding traits. However, these habitats tended to be less protected despite their higher diversity. Our results highlight the value of heterogeneous low vegetation for promoting overall insect biomass and diversity and that better protection of insects requires improved protection and management of unforested areas, where many biodiversity hotspots and key taxa occur

Evolutionary systematics and reproductive biology of two Cerithioidea snail families (Thiaridae, Planaxidae)

The current biodiversity crisis and associated mass extinction is undoubtedly the major challenge mankind is facing in the 21st century. To effectively take action against this threat, not only direct action but also fundamental biodiversity research must be undertaken, to assess the ‘true’ biological diversity before it is lost. Thereby, the description of new species is easily as important as the reassessment of known taxa with an ambiguous taxonomic status. To provide a modern assessment of biodiversity in such understudied groups, an evolutionary systematics approach should be conducted, viz. studies integrating several morphological and molecular methods in a framework of evolutionary biology. The thesis at hand compiles several such studies for two families of the understudied gastropod superfamily Cerithioidea. One focus is on the tropical, freshwater Thiaridae, the other on the tropical to warm temperate, marine Planaxidae. Here presented, is the first family-wide molecular study of representative specimens of all genera of Thiaridae. Though several morphological established lineages are not unambiguously resolved within the resulting phylogeny, the study furthers our understanding of the biogeographic history leading to the diversification of this group. Taxonomic assessment of the thiarid Stenomelania-Melanoides complex have been carried out – a taxonomically highly convoluted assemblage of the genera Stenomelania, Melanoides and Neoradina. As major results, the Neoradina lineage is for the first time supported as a distinct lineage of this complex, and Stenomelania is outlined by its differences in developmental mode and shell shape. With the focus on poecilogony (that is the presence of two distinctly different developmental modes within the same animal species) in the planaxid snail species Planaxis sulcatus, for the first time a study encompassing the entire distribution range of the species is compiled, examining its molecular genetics and developmental modes. As a result, the species was found to vary geographically in developmental mode. With the integrative assessment of morphology and molecular biology of Supplanaxis, a so far unrevised planaxid snail genus has been retrieved. Twenty-two nominal species are examined, resulting in an assessment of six valid species, enabled only by the connection between different study methods. Overall, this thesis lays the basis for further evolutionary systematic studies on a complex snail superfamily, that thus far is oftentimes overlooked due to its rough taxonomic history. Thereby this study exemplifies the need to survey all of nature’s parts to be able to assess its full picture. Only then our efforts to protect every part of it will be worthwhile.Die gegenwärtige Biodiversitätskrise und das damit verbundene Massenaussterben ist zweifelsfrei die größte Herausforderung der die Menschheit im 21. Jahrhundert gegenübersteht. Um ein effektives Handeln zu ermöglichen, müssen nicht nur direkte Maßnahmen ergriffen werden, sondern ebenfalls grundlegende Untersuchungen der Biodiversität vorgenommen werden, damit die ‘tatsächliche’ biologische Vielfalt ermittelt werden kann. Hierbei ist die Beschreibung bisher unbekannter Arten ebenso wichtig wie die Neubewertung bekannter Taxa, deren taxonomischer Status unklar ist. Um zeigemäße Studien über die Vielfalt in solch wissenschaftlich vernachlässigten Gruppen durchzuführen, sollten diese im Rahmen eines evolutionssystematischen Ansatzes — also einer Integration morphologischer und molekulargenetischer Methoden vor dem Hintergrund evolutionsbiologischer Fragestellungen — durchgeführt werden. In der vorliegenden Dissertation wurden mehrere solcher Studien über zwei bisher nicht hinreichend untersuchten Schneckenfamilien innerhalb der Überfamilie Cerithioidea zusammengestellt. Hierbei stellten die in tropischen Süßgewässern lebenden Thiaridae sowie die in tropisch bis warm-temperaten Meeresküsten lebenden Planaxidae die untersuchten Fokusgruppen dar. Zuerst wird die erste familienweite molekulargenetische Studie der Thiaridae vorgestellt, die Repräsentanten aller derzeit unterschiedenen Gattungen beinhaltet. Obschon einige morphologisch etablierte Linien in der vorliegenden Phylogenie nicht eindeutig widergespiegelt werden, erweitert die Untersuchung unser Verständnis der historischen Biogeographie, die zur Diversifikation der Gruppen innerhalb dieser Familie führte. Innerhalb der Thiaridae wird der Melanoides-Stenomelania Komplex unterschieden. Dieser stellt eine taxonomisch äußerst unübersichtliche Gruppe von Arten dar, die in den Gattungen Melanoides, Stenomelania und Neoradina geführt werden. Im Ergebnis wird die umstrittene Neoradina Linie für diesen Komplex bestätig und Stenomelania aufgrund ihrer Gehäuseform und ihres differenzierten entwicklungsbiologischem Mechanismus abgegrenzt. Innerhalb der Planaxidae liegt ein Fokus auf der Untersuchung zur Poecilogonie (also dem zeitgleichen Auftreten zweier unterschiedlicher entwicklungsbiologischer Modi innerhalb derselben Art) von Planaxis sulcatus. Erstmalig wurde hier eine Studie über den gesamten Verbreitungsraum der Art durchgeführt, bei der auf die Molekulargenetik und Entwicklungsbiologie der Populationen eingegangen wurde. In der Folge kann eine geographische Poecilogonie festgestellt werden, also eine Varianz der unterschiedlichen Entwicklungsmodi entlang des Verbreitungsgebiets. Weiterhin wird mit einem integrativen Ansatz von morphologischen und molekularen Methoden die Planaxidengattung Supplanaxis revidiert. Unter den zweiundzwanzig Nominalarten dieser Gattung wurden sechs valide Arten festgestellt, die nur durch die Verbindung der angewandten Methoden erkannt werden konnten. Die Ergebnisse aller Teilstudien dieser Dissertation bilden die Basis für eine Vielzahl weiterer evolutionssystematischer Studien an einer oftmals durch ihre unübersichtliche Taxonomie unbearbeiteten Schnecken-Überfamilie. Dabei zeigen diese Arbeiten abermals auf, dass alle noch so kleinen Teilstücke der Natur in Augenschein genommen werden müssen, um ein vollständiges Bild zu erhalten. Nur durch ein solches Vorgehen werden unsere Mühen zum Schutz all dieser Teile sich lohnen

One species, two developmental modes: a case of geographic poecilogony in marine gastropods

Abstract Background Poecilogony, the presence of two developmental modes in the same animal species, is a rare phenomenon. Few cases of poecilogony have been suggested for marine invertebrates including molluscs and even less stood extensive testing, mostly revealing a species pair with differing developmental modes. We studied a textbook example of poecilogony in the viviparous snail Planaxis sulcatus (Gastropoda: Planaxidae), for the first time throughout its entire distribution range. Results In the Western Indian Ocean and Red Sea this intertidal species is observed to have large, shelled juveniles, whereas in the Indo-West Pacific planktotrophic veliger larvae are released from a subhaemocoelic brood pouch. We uncovered a shift in developmental modes across its range: from west to east successively earlier developmental stages are released. Furthermore, genetic data based on mitochondrial DNA suggests to recognize P. sulcatus as a single species rather than a group of cryptic species. A reconstruction of the ancestral area of P. sulcatus based on molecular data outlines the Western Indian Ocean and the Indo-West Pacific as area of origin. Conclusion The findings supporting Planaxis sulcatus as a single widespread species and the geographical shift from one reproductive mode to another suggest for this species to truly represent a case of geographic poecilogony, i.e. differing developmental modes between populations of the same species. Furthermore, the results of our ancestral range estimation imply the release of planktotrophic larvae as the ancestral developmental mode

One species, two developmental modes: a case of geographic poecilogony in marine gastropods

Abstract Background Poecilogony, the presence of two developmental modes in the same animal species, is a rare phenomenon. Few cases of poecilogony have been suggested for marine invertebrates including molluscs and even less stood extensive testing, mostly revealing a species pair with differing developmental modes. We studied a textbook example of poecilogony in the viviparous snail Planaxis sulcatus (Gastropoda: Planaxidae), for the first time throughout its entire distribution range. Results In the Western Indian Ocean and Red Sea this intertidal species is observed to have large, shelled juveniles, whereas in the Indo-West Pacific planktotrophic veliger larvae are released from a subhaemocoelic brood pouch. We uncovered a shift in developmental modes across its range: from west to east successively earlier developmental stages are released. Furthermore, genetic data based on mitochondrial DNA suggests to recognize P. sulcatus as a single species rather than a group of cryptic species. A reconstruction of the ancestral area of P. sulcatus based on molecular data outlines the Western Indian Ocean and the Indo-West Pacific as area of origin. Conclusion The findings supporting Planaxis sulcatus as a single widespread species and the geographical shift from one reproductive mode to another suggest for this species to truly represent a case of geographic poecilogony, i.e. differing developmental modes between populations of the same species. Furthermore, the results of our ancestral range estimation imply the release of planktotrophic larvae as the ancestral developmental mode. </jats:sec

Adding the West-African riverine component: Revision of the Recent freshwater snails belonging to Pseudocleopatra Thiele, 1928 (Caenogastropoda, Cerithioidea, Paludomidae)

Neiber, Marco T., Kahl, Sandra M., Wiggering, Benedikt, Glaubrecht, Matthias (2019): Adding the West-African riverine component: Revision of the Recent freshwater snails belonging to Pseudocleopatra Thiele, 1928 (Caenogastropoda, Cerithioidea, Paludomidae). Zootaxa 4674 (3): 301-328, DOI: https://doi.org/10.11646/zootaxa.4674.3.

&lt;p&gt;&lt;strong&gt;Adding the West-African riverine component: Revision of the Recent freshwater snails belonging to &lt;em&gt;Pseudocleopatra&lt;/em&gt; Thiele, 1928 (Caenogastropoda, Cerithioidea, Paludomidae)&lt;/strong&gt;&lt;/p&gt;

While Africa’s lacustrine gastropod fauna, in particular of Lake Tanganyika, has received much attention, the continent’s riverine malacofauna has long been neglected. Pseudocleopatra is a relatively poorly known paludomid gastropod genus with species found throughout the lower reaches of the West African Volta and Congo rivers. In the course of ongoing systematic revisions of African paludomids, we present here a morphometric analysis and revision of the recent species assigned to the genus, i.e., P. togoensis, P. voltana, P. dartevellei and P. bennikei, to improve taxonomic acuity for this group. We use available museum material for geometric morphometrics, multivariate ratio analysis and comparisons of radular and opercular characters. Our results demonstrate that the four recent species of Pseudocleopatra are clearly distinguishable on the basis of ratios of shell measurements as well as radular and opercular characters. Pseudocleopatra has generic-level synapomorphies including: concentric opercula with relatively large paucispiral nuclei, and rachidian radular teeth with usually 13–20 cusps. On the basis of this characterisation, the nominal species Cleopatra broecki is transferred to Pseudocleopatra. Additionally, the nominal taxon P. bennikei is synonymized with P. broecki n. comb. The phylogenetic relationships of Pseudocleopatra are currently unknown, but the observed tendency of some fossil taxa assigned to Pseudocleopatra towards thalassoidism, i.e., the resemblance to marine gastropods, has led to the hypothesis that some of the thalassoid endemics in Lake Tanganyika may have originated from or be related to Pseudocleopatra. Should this hypothesis be correct, which is in need of testing by molecular genetic methods when suitable samples become available, Pseudocleopatra may play a crucial role in understanding of the evolution of thalassoidism in African Paludomidae. </jats:p