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Ontogeny of juvenile freshwater pearl mussels, Margaritifera margaritifera (Bivalvia: Margaritiferidae).

ABSTRACT: The gills of juvenile freshwater bivalves undergo a complex morphogenesis that may correlate with changes in feeding ecology, but ontogenic studies on juvenile mussels are rare. Scanning electron microscopy was used to examine the ultrastructure and ontogeny of 117 juvenile freshwater pearl mussels (Margaritifera margaritifera) ranging in age from 1-44 months and length from 0.49-8.90 mm. Three stages of gill development are described. In Stage 1 (5-9 inner demibranch filaments), only unreflected inner demibranch filaments were present. In Stage 2 (9-17 inner demibranch filaments), inner demibranch filaments began to reflect when shell length exceeded 1.13 mm, at 13-16 months old. Reflection began in medial filaments and then proceeded anterior and posterior. In Stage 3 (28-94 inner demibranch filaments), outer demibranch filaments began developing at shell length > 3.1 mm and about 34 months of age. The oral groove on the inner demibranch was first observed in 34 month old specimens > 2.66 mm but was never observed on the outer demibranch. Shell length (R2 = 0.99) was a better predictor of developmental stage compared to age (R2 = 0.84). The full suite of gill ciliation was present on filaments in all stages. Interfilamentary distance averaged 31.3 μm and did not change with age (4-44 months) or with size (0.75-8.9 mm). Distance between laterofrontal cirri couplets averaged 1.54 μm and did not change significantly with size or age. Labial palp primordia were present in even the youngest individuals but ciliature became more diverse in more developed individuals. Information presented here is valuable to captive rearing programmes as it provides insight in to when juveniles may be particularly vulnerable to stressors due to specific ontogenic changes. The data are compared with two other recent studies of Margaritifera development.

SUBMITTER: Lavictoire L

PROVIDER: S-EPMC5873991 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The Freshwater Pearl Mussel (Margaritifera margaritifera) is an endangered organism across its entire range. It has a complex life cycle and stringent habitat requirements and is therefore an indicator species for the general ecosystem health of host rivers. Whereas historical intensive pearl fishing contributed to population declines, excess nutrient and sediment loss associated with current land use pressures in host river catchments, including modern intensive farming practices, are now highlighted as primary contributory factors. Accordingly, this study investigated the sources and dynamics of fine-grained sediment sampled in the mussel beds of the River Torridge, SW England. Sediment source fingerprinting using a combination of colorimetric and radiometric tracers to construct different composite signatures revealed the importance of roads both as a sediment source and delivery pathway for fine-grained sediment mobilised from fields predominantly supporting lowland livestock farming. Grassland fields with evidence of soil poaching were highlighted as important sediment sources, but equally, riparian woodland was also identified as important, especially during the latter stages of consecutive runoff events when its rainfall buffering capacity was exceeded. Bed sediment storage levels (median up to 393 g m-2) were found to be low (41st percentile) compared to typical values reported by a recent strategic scale survey across England and Wales, whereas elevated turbidity peaks were shown to be long duration (days) in conjunction with consecutive days of rainfall and corresponding runoff events. Hysteresis patterns varied but were generally clockwise during the largest runoff events associated with consecutive rain days; again, suggesting mobilisation of sediment from proximal woodland sources following exceedance of rainfall buffering capacity. In combination, the data assembled by this study provides a basis for planning sediment control measures for protecting the Freshwater Pearl Mussel (FPM) beds from excessive fine-grained sediment inputs associated with the intensive use of primarily grazing land.

Project description:Mitochondrial (mt) function depends critically on optimal interactions between components encoded by mt and nuclear DNAs. mitochondrial DNA (mtDNA) inheritance (SMI) is thought to have evolved in animal species to maintain mito-nuclear complementarity by preventing the spread of selfish mt elements thus typically rendering mtDNA heteroplasmy evolutionarily ephemeral. Here, we show that mtDNA intraorganismal heteroplasmy can have deterministic underpinnings and persist for hundreds of millions of years. We demonstrate that the only exception to SMI in the animal kingdom, that is, the doubly uniparental mtDNA inheritance system in bivalves, with its three-way interactions among egg mt-, sperm mt- and nucleus-encoded gene products, is tightly associated with the maintenance of separate male and female sexes (dioecy) in freshwater mussels. Specifically, this mother-through-daughter and father-through-son mtDNA inheritance system, containing highly differentiated mt genomes, is found in all dioecious freshwater mussel species. Conversely, all hermaphroditic species lack the paternally transmitted mtDNA (=possess SMI) and have heterogeneous macromutations in the recently discovered, novel protein-coding gene (F-orf) in their maternally transmitted mt genomes. Using immunoelectron microscopy, we have localized the F-open reading frame (ORF) protein, likely involved in specifying separate sexes, in mitochondria and in the nucleus. Our results support the hypothesis that proteins coded by the highly divergent maternally and paternally transmitted mt genomes could be directly involved in sex determination in freshwater mussels. Concomitantly, our study demonstrates novel features for animal mt genomes: the existence of additional, lineage-specific, mtDNA-encoded proteins with functional significance and the involvement of mtDNA-encoded proteins in extra-mt functions. Our results open new avenues for the identification, characterization, and functional analyses of ORFs in the intergenic regions, previously defined as "noncoding," found in a large proportion of animal mt genomes.

Dataset Information

Ontogeny of juvenile freshwater pearl mussels, Margaritifera margaritifera (Bivalvia: Margaritiferidae).

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