A Multi-Species Comparison and Evolutionary Perspectives on Ion Regulation in the Antennal Gland of Brachyurans

Abstract

Brachyurans inhabit a variety of habitats and have evolved diverse osmoregulatory patterns. Gills, antennal glands and a lung-like structure are important organs of crabs that maintain their homeostasis in different habitats. Species use different processes to regulate ions in the antennal gland, especially those with high terrestriality such as Grapsoidea and Ocypodoidea. Our phylogenetic generalized least square (PGLS) result also suggested that there is a correlation between antennal gland NKA activity and urine-hemolymph ratio for Na⁺ concentration in hypo-osmotic environments among crabs. Species with higher antennal gland NKA activity showed a lower urine-hemolymph ratio for Na⁺ concentration under hypo-osmotic stress. These phenomenon may correlate to the structural and functional differences in gills and lung-like structure among crabs. However, a limited number of studies have focused on the structural and functional differences in the antennal gland among brachyurans. Integrative and systemic methods like next generation sequencing and proteomics method can be useful for investigating the differences in multi-gene expression and sequences among species. These perspectives can be combined to further elucidate the phylogenetic history of crab antennal glands.

Keywords: NKA activity; antennal gland; brachyurans; evolutionary physiology; ion regulation.

FIGURE 1

The cell types and presumed urine production and re-absorption process in antennal gland of Ocypode stimpsoni. (A) Three types of cell in antennal gland of O. stimpsoni. Coelomic cells with different size of vesicle (open arrow and triangle) and endosome (V), (a). Labyrinthine cells have a great of mitochondria (m) in basal folding, vesicles (open triangle) in sub-apical region and aposomes (black triangle) around apical microvilli, (b). End-labyrinthine cells, another type of labyrinthine cells, showed a different shape of apical membrane compared to labyrinthine cells. In addition, mitochondria not only distributed in basal folding, but also in other regions of end-labyrinthine cells, (c). (B) Hemolymph will be filtrated through coelomic cells (dash arrow), and the ions and other substances will be re-absorbed into hemolymph by labyrinthine cells (grey arrow). COE, coelomic cell. hs, haemolymph sinus. LBR, labyrinthine cell. The figure comes from Tsai and Lin, (2014).

FIGURE 2

The NKA activity and urine and hemolymph ratio (U/H) for Na⁺ in the antennal glands of different crab species. The phylogenetic tree was generated by Bayesian inference with COI and 16S rDNA. The antennal gland NKA activity of crabs in 5 ppt was mapped on the phylogenetic tree and the ancestor status was predicted by the phylogenetic structure. Labels in blue boxes were the superfamilies of brachyuran. Labels in green boxes were the groups separated by the clades in phylogenetic trees. (A) Antennal gland NKA activity in the ocypodid group was higher than that in the grapsid group. (B) Ocypodidae species had a lower U/H for Na⁺ than did species in other families. The figure comes from Tseng et al. (2020).

FIGURE 3

The relationship between antennal gland NKA activity and U/H for Na⁺ concentration in the antennal gland of different crab species in hypo- and hyper-osmotic environments. The phylogenetic tree was generated by Bayesian inference with COI, 12S and 16S rDNA. The antennal gland NKA activity and U/H for Na⁺ concentration of crabs in 5 or 35 ppt were mapped on the phylogenetic tree and the ancestor status was predicted by the phylogenetic structure. The correlation between antennal gland NKA activity and U/H for Na⁺ concentration was analyzed by PGLS. Left pictures were the results of antennal gland NKA activity, and right sides were U/H for Na⁺ concentration. (A) The antennal gland NKA activity was correlated with the U/H for Na⁺ concentration in the antennal gland when species were transferred into hypo-osmotic environments (t value = −5.7963, df = 8, p = 0.0012, R² = 0.88). (B) There was no correlation between antennal gland NKA activity and the U/H for Na⁺ concentration in the antennal gland when species were transferred into hyper-osmotic mediums (t value = −0.1627, df = 6, p = 0.8786, R² < 0.001). Data of Ocypode quadrata are from DeVries et al. (1994). Data of Gecarcinus lateralis are from Gross (1964) and DeVries et al. (1994). Data of Candidiopotamon rathbunae are from Wang and Lin (2011).