Rhogocytes in gastropod larvae: developmental transformation from protonephridial terminal cells

Abstract

AbstractRhogocytes, terminal cells of protonephridia, and podocytes of metanephridial systems share an architectural feature that creates an apparent sieving device. The sieve serves to ultrafilter body fluid during the excretion and osmoregulation process carried out by nephridial systems, but its function in rhogocytes is unclear. Rhogocytes are molluscan hemocoelic cells that appear to have various functions related to metabolism of metal ions, including synthesis of hemocyanin in some gastropods and metal detoxification in pteriomorph bivalves. A hypothesis that proposed developmental and possibly evolutionary conversion between protonephridial terminal cells and rhogocytes has never been further explored; indeed, information on the occurrence of rhogocytes in molluscan developmental stages is meager. We used transmission electron microscopy to show that rhogocytes are present within larvae of eight species of gastropods sampled from the three major gastropod clades with a feeding larval stage in the life history. In larvae of a heterobranch gastropod, a rhogocyte was located next to each terminal cell of a pair of protonephridia that flanked the foregut, whereas all six species of caenogastropod larvae and a neritimorph larva that we examined had rhogocytes, but no protonephridia, in this location. We did not find ring‐shaped profiles of hemocyanin decamers within rhogocytes of larvae or pre‐hatch embryos. Rhogocytes in newly released larvae of Nerita melanotragus contained orderly bundles of cylinders, but the diameter of the cylinders was only 70% of the diameter typical of hemocyanin multidecamers. By examining embryos of the caenogastropod Nassarius mendicus at four successive developmental time points that bracketed the occurrence of larval hatching, we found that terminal cells from non‐functional protonephridia in pre‐hatch embryos transformed into rhogocytes around the time of hatching. This empirical evidence of ontogenetic transformation of protonephridial terminal cells into rhogocytes might be interpreted as developmental recapitulation of an evolutionary transition that occurred early in molluscan history.