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The role of adaptive resistance in a widespread freshwater mussel species

Publication . Santos, Rogério; Sousa, Ronaldo; Lopes-Lima, Manuel; Teixeira, Amílcar

Organism features, such as size, weight, sex and age, among others, can influence the success of parasitism. For species that depend on a host to complete their life cycle, such as freshwater mussels (Bivalvia, Unionida), understanding how these traits influence parasitism can help guide management actions aimed at improving their reproductive success, ultimately benefitting their conservation. In this study, the physiological compatibility between the duck mussel Anodonta anatina and its host fish was investigated in a simultaneous infestation experiment on four (three native and one non-native) fish species using sympatric and allopatric host strains. The success of glochidia metamorphosis in juvenile mussels was evaluated as a function of host species, strain and fish length. Successful metamorphosis was achieved in almost all fish species tested and differences were detected between allopatric and sympatric strains, with higher values found in allopatric hosts. Allopatric strains of primary hosts produce more juveniles than marginal hosts and non-native species. In addition, larger fish have lower rates of metamorphosis. The results confirm recent findings showing high variation in the metamorphosis success of A. anatina glochidia among different native and non-native hosts, both in the natural environment and in artificial laboratory infestations. Allopatric hosts were more suitable for encystment, demonstrating potential adaptive immunity, not yet observed in A. anatina. Nevertheless, A. anatina may temporarily exploit the naivety of smaller fish regardless of strain. Overall, the results suggest that mussel propagation, reproduction and reintroduction efforts should consider the mechanisms that influence adaptive immunity in fish, including differences in compatibility within and between populations of sympatric and allopatric host strains. This situation should be taken into account, as successful metamorphosis is an important factor in the selection of hosts for juvenile development, especially in efforts to propagate endangered mussel species.

2024Journal article

Open access

Integrative phylogenetic, phylogeographic and morphological characterisation of the Unio crassus species complex reveals cryptic diversity with important conservation implications

Publication . Lopes-Lima, Manuel; Geist, Juergen P.; Egg, S.; Beran, Luboš; Bikashvili, Ani; Van Bocxlaer, Bert; Bogan, Arthur E.; Bolotov, Ivan N.; Chelpanovskaya, O.A.; Douda, Karel; Fernandes, Verónica; Gomes-dos-Santos, André; Gonçalves, Duarte Vasconcelos; Gürlek, Mustafa Emre; Johnson, Nathan A.; Karaouzas, Ioannis D.; Kebapçı, Ümit; Kondakov, Duarte Vasconcelos; Kuehn, Ralf; Lajtner, Jasna; Mumladze, Levan; Nagel, Karl Otto; Neubert, Eike; Österling, Martin E.; Pfeiffer, John M.; Prié, Vincent; Riccardi, Nicoletta; Sell, Jerzy; Schneider, Lea D.; Shumka, Spase; Sîrbu, Ioan; Skujienė, Grita; Smith, Chase H.; Sousa, Ronaldo Gomes; Stöckl, K.; Taskinen, Jouni K.; Teixeira, Amílcar; Todorov, Milcho T.; Trichkova, Teodora A.; Urbańska, Maria; Välilä, Santtu; Varandas, Simone Da Graça Pinto; Veríssimo, Joana; Vikhrev, Ilya V.; Woschitz, G.; Zając, Katarzyna; Zając, Tadeusz A.; Zanatta, David Thomas; Zieritz, Alexandra; Zogaris, Stamatis; Froufe, Elsa

The global decline of freshwater mussels and their crucial ecological services highlight the need to understand their phylogeny, phylogeography and patterns of genetic diversity to guide conservation efforts. Such knowledge is urgently needed for Unio crassus, a highly imperilled species originally widespread throughout Europe and southwest Asia. Recent studies have resurrected several species from synonymy based on mitochondrial data, revealing U. crassus to be a complex of cryptic species. To address long-standing taxonomic uncertainties hindering effective conservation, we integrate morphometric, phylogenetic, and phylogeographic analyses to examine species diversity within the U. crassus complex across its entire range. Phylogenetic analyses were performed using cytochrome c oxidase subunit I (815 specimens from 182 populations) and, for selected specimens, whole mitogenome sequences and Anchored Hybrid Enrichment (AHE) data on ∼ 600 nuclear loci. Mito-nuclear discordance was detected, consistent with mitochondrial DNA gene flow between some species during the Pliocene and Pleistocene. Fossil-calibrated phylogenies based on AHE data support a Mediterranean origin for the U. crassus complex in the Early Miocene. The results of our integrative approach support 12 species in the group: the previously recognised Unio bruguierianus, Unio carneus, Unio crassus, Unio damascensis, Unio ionicus, Unio sesirmensis, and Unio tumidiformis, and the reinstatement of five nominal taxa: Unio desectus stat. rev., Unio gontierii stat. rev., Unio mardinensis stat. rev., Unio nanus stat. rev., and Unio vicarius stat. rev. Morphometric analyses of shell contours reveal important morphospace overlaps among these species, highlighting cryptic, but geographically structured, diversity. The distribution, taxonomy, phylogeography, and conservation of each species are succinctly described.

2024Journal article

Open access

Interspecific differences in the physiological condition of native freshwater mussels in response to the invasive Asian clam Corbicula fluminea

Publication . Modesto, Vanessa; Ilarri, Martina; Castro, Paulo S.; Carvalho, Francisco; Cavalheri, Thais; Lopes-Lima, Manuel; Teixeira, Amílcar; Ozório, Rodrigo O.A.; Antunes, Carlos; Sousa, Ronaldo

The Asian clam Corbicula fluminea has been widely introduced into aquatic ecosystems and may impact the physiological condition and survival of native freshwater mussels. However, very few studies have evaluated this issue quantitatively. To fill this gap, manipulative field experiments were performed to assess two possible mechanisms of impact on native mussels: (i) interspecific interactions, and (ii) C. fluminea die-offs. We assessed these effects by measuring the physiological condition through the analysis of glycogen content in the foot tissue of the native freshwater mussel species Anodonta anatina, Potomida littoralis, and Unio delphinus. Although with interspecific differences, our results suggest that C. fluminea can impact the physiological condition of native freshwater mussels. Anodonta anatina showed positive significant variations on glycogen content when subjected to high densities of live C. fluminea in contrast to the other native species studied, P. littoralis and U. delphinus, where no significances were observed. On the other hand, these native species do not seem be significantly impacted by the decomposition of C. fluminea resulting from a die-off. Overall, and contrary to our expectations, both experiments showed a positive (or no) effect of C. fluminea on the physiological condition of the three freshwater mussel species.

2023Journal article

Restricted access

The crown pearl V2: an improved genome assembly of the European freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758)

Publication . Gomes-dos-Santos, André; Lopes-Lima, Manuel; Machado, André M.; Forest, Thomas; Achaz, Guillaume; Teixeira, Amílcar; Prié, Vincent; Castro, L. Filipe C.; Froufe, Elsa

Contiguous assemblies are fundamental to deciphering the composition of extant genomes. In molluscs, this is considerably challenging owing to the large size of their genomes, heterozygosity, and widespread repetitive content. Consequently, long-read sequencing technologies are fundamental for high contiguity and quality. The first genome assembly of Margaritifera margaritifera (Linnaeus, 1758) (Mollusca: Bivalvia: Unionida), a culturally relevant, widespread, and highly threatened species of freshwater mussels, was recently generated. However, the resulting genome is highly fragmented since the assembly relied on short-read approaches. Here, an improved reference genome assembly was generated using a combination of PacBio CLR long reads and Illumina paired-end short reads. This genome assembly is 2.4 Gb long, organized into 1,700 scaffolds with a contig N50 length of 3.4 Mbp. The ab initio gene prediction resulted in 48,314 protein-coding genes. Our new assembly is a substantial improvement and an essential resource for studying this species’ unique biological and evolutionary features, helping promote its conservation.

2023Journal article

Open access

The complete mitochondrial genome of Potomida acarnanica (Kobelt, 1879)

Publication . Matos, Ana; Gomes-dos-Santos, André; Teixeira, Amílcar; Varandas, Simone; Sousa, Ronaldo; Karaouzas, Ioannis; Zogaris, Stamatis; Froufe, Elsa; Lopes-Lima, Manuel

Freshwater mussels (Bivalvia, Unionida) play essential roles in the well-functioning of ecosystems, even providing essential services to humans. However, these bivalves face numerous threats (e.g. habitat loss and fragmentation, pollution, introduction of invasive species, and climate change) which have already led to the extinction of many populations. This underscores the need to fully characterize the biology of these species, particularly those, such as Potomida acarnanica, that are still poorly studied. This study presents the first mitogenome of P. acarnanica (Kobelt, 1879), an endemic species of Greece with a distribution limited to only two river basins. The mitochondrial genome of a P. acarnanica specimen, collected at Pamisos River (Peloponnese, Greece), was sequenced by Illumina high-throughput sequencing. This mitogenome (16,101 bp) is characterized by 13 protein-coding genes, 22 transfer RNA and 2 ribosomal RNA genes. The size of this mitogenome is within the range of another Potomida mitogenome already published for the species Potomida littoralis. In the phylogenetic inference, P. acarnanica was recovered as monophyletic with P. littoralis mitogenome in the Lamprotulini tribe, as expected. This genomic resource will assist in genetically characterizing the species, potentially benefiting future evolutionary studies and conservation efforts.

2024Journal article

Open access