Trophic Specialisation Reflected by Radular Tooth Material Properties in An

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Trophic Specialisation Reflected by Radular Tooth Material Properties in An Krings et al. BMC Ecol Evo (2021) 21:35 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01754-4 RESEARCH ARTICLE Open Access Trophic specialisation refected by radular tooth material properties in an “ancient” Lake Tanganyikan gastropod species fock Wencke Krings1,2* , Marco T. Neiber1, Alexander Kovalev2, Stanislav N. Gorb2 and Matthias Glaubrecht1 Abstract Background: Lake Tanganyika belongs to the East African Great Lakes and is well known for harbouring a high pro- portion of endemic and morphologically distinct genera, in cichlids but also in paludomid gastropods. With about 50 species these snails form a fock of high interest because of its diversity, the question of its origin and the evolutionary processes that might have resulted in its elevated amount of taxa. While earlier debates centred on these paludomids to be a result of an intralacustrine adaptive radiation, there are strong indications for the existence of several lineages before the lake formation. To evaluate hypotheses on the evolution and radiation the detection of actual adaptations is however crucial. Since the Tanganyikan gastropods show distinct radular tooth morphologies hypotheses about potential trophic specializations are at hand. Results: Here, based on a phylogenetic tree of the paludomid species from Lake Tanganyika and adjacent river systems, the mechanical properties of their teeth were evaluated by nanoindentation, a method measuring the hard- ness and elasticity of a structure, and related with the gastropods’ specifc feeding substrate (soft, solid, mixed). Results identify mechanical adaptations in the tooth cusps to the substrate and, with reference to the tooth morphology, assign distinct functions (scratching or gathering) to tooth types. Analysing pure tooth morphology does not consist- ently refect ecological specializations, but the mechanical properties allow the determination of eco-morphotypes. Conclusion: In almost every lineage we discovered adaptations to diferent substrates, leading to the hypothesis that one main engine of the fock’s evolution is trophic specialization, establishing distinct ecological niches and allowing the coexistence of taxa. Keywords: Functional morphology, Nanoindentation, Mechanical properties, Gastropoda, Trophic specialisation, Adaptive radiation Background geographical and ecological conditions [1–3]. Addressing Hypotheses on how biodiversity relates with the tempo- this topic has seen various approaches based on verte- ral and spatial “flling” of available habitats and annida- brates, such as the studies on Darwin fnches [4–9], the tion itself, i.e. the actual formation of ecological niches cichlid fshes in the East African lakes [10–13] and Nic- as a combined process of internal and external factors, is aragua [14–16] or Anolis lizards [17–19]. Tese species paramount for understanding how species evolve under focks [cf. 20] are usually regarded as examples of adap- tive radiations, the evolution of ecological and pheno- typic diversity within a rapidly multiplying lineage, thus *Correspondence: [email protected] linking speciation and ecology [21–26]. 1 Center of Natural History (CeNak), Universität Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany However, even though the majority of all known ani- Full list of author information is available at the end of the article mals are invertebrates [27, 28], fewer model systems were © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Krings et al. BMC Ecol Evo (2021) 21:35 Page 2 of 25 on focus (with exceptions, e.g. [29, 30] on crickets). Tere processing ingesta and directly linking the organism with are however spectacular examples of invertebrate species its food. Various muscles control the motion of this feed- focks exhibiting a great diversity, especially among mol- ing organ, pulling the chitinous radular membrane with luscs [see also 31, 32], the lacustrine and riverine fresh- rows of small embedded radular teeth [100] across an water gastropods on Sulawesi [33–38], Madagascar [39], odontophoral cartilage (Fig. 2a). As teeth are in direct in the Tai rivers [40, 41], or “ancient” Lake Tanganyika contact with the ingesta, their morphology can often be [42–44]. Te latter is well known for its unique assem- directly linked with the animal’s ecology and can refect blage of endemic species and has been a natural labora- various transitions from zoovorous to herbivorous traits tory for research on the drivers of evolution for decades. [101–106]. Form together with the tooth’s position and It harbours paludomid gastropods (Fig. 1) which trig- chemical composition are widely considered adaptive to gered many expeditions and subsequently malacological food and are hence closely associated with feeding strat- descriptions [e.g. 45–60] and a long-lasting controversy egies, competitor avoidance and thus trophic specializa- about the origin and evolution of the lake and its fauna. tion [107–118]. Due to their marine-like appearance (termed “thalassoid” Strong indications for trophic specialization in the con- by [45] and “halolimnic” by [61]) many earlier authors text of gastropod adaptive radiations have been described addressed the possibility of a marine origin of the Lake for the radular tooth morphologies of lacustrine Tylo- Tanganyika fauna and discussed the causes of the thalas- melania from Sulawesi [33, 35, 38], the riverine gastro- soid appearance of its endemic molluscs. However, this pods from Kaek River [40], and marine Dendronotus eventually led to the refutation of Moore’s controversial [119]. For the Lake Tanganyikan paludomids hypotheses hypothesis [61–63] of the lake being once directly con- on the potential infuence of trophic specialization on the nected to the ocean [see e.g. in 64–68]. evolution of this fock are consequential, since these spe- For a long time the idea that this largest and deepest cies show an extraordinarily high interspecifc diversity in of the African lakes has supplied its gastropod diversity tooth morphologies [e.g. 44, 120]. Tese shapes can often with a stable inland environment and ofered unique be related with the gastropods’ specifc feeding substrates opportunities for within-lake diversifcation (“ancient (soft, mixed or solid) since teeth as highly functionate endemic radiation” see [65, 69]) resulting in a truly “adap- interfaces do not only interact with the food but also with tive” radiation [cf. 70, 71] was common [e.g. 72–86]. the substrate the food is attached to [121, 122]. In addi- However, strong evidence for an ancient origin of dispar- tion, recent studies on the paludomid tooth anchorages ity and diversity in this fock has been presented, indicat- in the radular membrane, which are also diverse between ing the existence of major gastropod lineages before the taxa, relate this connecting area with the gastropod’s spe- formation of the lake itself or its proto-lakes. Te oldest cifc feeding substrate [123]. formation estimates are 9–12 Mya [87–89], while more In addition to morphology, the structural composi- recent studies date the pre-rift formation to 4–11 Mya tion also infuences functionality. For reconstructing the and the earliest onset of a true rifting activity to 5.5 Mya evolutionary history of the African Paludomidae and to [90–93]. With a molecular clock approach in support develop hypotheses on the role of trophic specialisation [42], this alternative hypothesis of the former existence of in their evolution, we here identifed the hardness and several originally riverine paludomid lineages later inhab- elasticity of taenioglossan radular teeth from 24 species iting the lake and bringing possible adaptations to former belonging to this fock utilising nanoindentation, a tech- river environments with them was suggested by [43, 44]. nique previously employed to identify local mechanical To allocate hypotheses about paludomid evolution and properties of various biological materials [e.g. 124–130]. radiations—especially in the context of adaptive radia- Results, with reference to morphology, allow the assign- tions—the identifcation of actual adaptation is crucial. ment of distinct functions to certain tooth types. Te Morphological structures associated with feeding, such identifcation of mechanical adaptations in their cusps to as e.g. bills or skulls in birds, vomer bones in cichlid the preferred feeding substrate allowed the establishment fshes or teeth in mammals, can exhibit adaptations and of eco-morphotypes. Our results strongly
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