New perspective on the haplosporidian parasites of molluscs

Abstract

The protist phylum Haplosporidia comprises over 40 described species with representatives infecting a range of mollusc hosts, including several ecologically and economically significant pathogens. Continuing exploration of haplosporidian diversity has added ten new species in recent years and brought the phylogenetics of the group into somewhat clearer focus, with monophyletic Bonamia and Minchinia lineages continuing to be supported. However, the addition of new sequences to phylogenetic analyses has left the paraphyletic genus Haplosporidium's picture less resolved. It is not clear that even two genera will be enough to accommodate the species presently drawn to the Haplosporidium regions of the haplosporidian tree. In this review, we summarize recent findings in haplosporidian diversity and phylogenetics, and provide a synthesis of our understanding of the life cycles and environmental influences on haplosporidians, with particular emphasis on the important pathogens Haplosporidium nelsoni and Bonamia ostreae. Additionally, we consider the evolution of the "microcell haplosporidian" lifestyle of Bonamia parasites, and suggest that colonization of high-density oyster host populations in relatively stable euhaline marine environments may have been an important development favoring the evolution of the microcell haplosporidian life strategy.

S.O.S. Pinna nobilis: A Mass Mortality Event in Western Mediterranean Sea

“…Regarding the possible origin of the parasite as it has been pointed out by Darriba (2017), it is impossible to asseverate if this parasite is new infecting P. nobilis or if is an old symbiont that has changed leading to a mortality outbreak. Other haplosporidan species, such as Haplosporidium nelsoni and Bonamia spp., have been responsible for bivalve mass mortalities world-wide (Arzul and Carnegie, 2015). Considering the vast geographic spreading, parasite eradication does not seem feasible because historical attempts to eradicate bivalve mollusk parasites from marine open areas have failed; intermediate or reservoir hosts and parasite long-term resistant stages could contribute to parasite staying even if the specimens of the host species are thoroughly removed from affected areas (Grizel et al, 1986;van Banning, 1991).…”

The ecology, evolution, impacts and management of host–parasite interactions of marine molluscs

“…However, the majority of these have either been: (1) inventories of the parasites and diseases influencing particular groups of molluscs (Cheng, 1993;Fryer and Bayne, 1996;AFS-FHS, 2005;Bower, 2006); (2) overviews of specific parasite-host interactions, particular those concerning commercially important species (e.g., Burreson and Ford, 2004;Paillard, 2004;Villalba et al, 2004;Arzul and Carnegie, 2015 this volume); or (3) overviews of molluscan diseases that impact humans (e.g., Rippey, 1994;Wittman and Flick, 1995).…”

“…For example, the physiological inability of the disease-causing parasite, H. nelsoni, to tolerate low salinities (Ford and Haskin, 1988) has resulted in its host, C. virginica, experiencing spatial and temporal refuges from the resultant MSX disease at low salinities (Haskin and Ford, 1982;Andrews, 1983;Ford, 1985;Arzul and Carnegie, 2015 in this volume). Adult bivalves, but not larvae, are able to close their valves to reduce exposure to conditions of unfavorable salinity that extend days to weeks.…”

“…In Delaware Bay, enhanced resistance of Eastern oysters (C. virginica) to MSX disease was initially seen following the 1957-1959 epizootic, but has since plateaued between 1960 and 1987, presumably because most of the surviving oysters were in low-salinity 'refugia' where they were protected from sustained selection and continued to contribute susceptible progeny to the population. In 1984-1986, however, an extended period of drought eliminated these low-salinity disease refuges, resulting in significant mortality across Delaware Bay populations, and leading to a major increase in the level of resistance to MSX disease (e.g., Hofmann et al, 2009;Carnegie and Burreson, 2011;Burge et al, 2014;Arzul and Carnegie, 2015 in this volume). Unlike P. marinus with direct acquisition of the parasite, the transmission of H. nelsoni (disease causing agent of MSX) has not been resolved despite over 50 years of research effort, but most assume that there is an 'intermediate' host involved prior to it infecting oysters (Ford and Tripp, 1996;Lafferty and Harvell, 2014;Arzul and Carnegie, 2015 in this volume).…”

“…Enhanced resistance of Eastern oysters (C. virginica) to MSX disease was seen following the 1957-1959 epizootic, but plateaued between 1960 and 1987, presumably because most of the surviving oysters were in low-salinity 'refugia' where they were protected from sustained selection and continued to contribute susceptible progeny to the population. In 1984-1986, however, an extended period of drought eliminated these lowsalinity disease refuges, resulting in significant mortality across the Bay populations, and leading to a major increase in the level of resistance to MSX disease (e.g., Hofmann et al, 2009;Carnegie and Burreson, 2011;Burge et al, 2014;Arzul and Carnegie, 2015).…”