Adaptations to host infection and larval parasitism in Unionoida

Abstract

Freshwater mussel larval parasitism of fish is unique among bivalves. The relationship is primarily phoretic rather than nutritive; only the smallest glochidia and the haustorial larva grow substantially while on the host. Growth of the smallest larvae suggests a lower functional size limit of ;150 lm for the juvenile stage. Most Ambleminae, the most diverse North American clade, infect host gills by attracting feeding fish. Many species of Pleurobemini and some Lampsilini release conglutinates of eggs and larvae that resemble host food items. Many Lampsilini and a few Quadrulini use mantle modifications to attract host fish to the female. The mantle of some Quadrulini forms a posterior chamber that holds glochidia for immediate release in response to host fish. In many Lampsilini, mantle flap lures and a protrusible marsupium promote attack by the host fish and direct extraction of glochidia from the marsupium by the host. Host extraction of glochidia from the brooding female might have favored the evolution of long-term brooding in Lampsilini because glochidia need not be released by the female to encounter the host. A remarkable derivative of the host extraction strategy evolved in Epioblasma, which catch fish between the valves and release glochidia directly to the trapped host before releasing it. Host specificity is a critical feature of the evolutionary diversification and conservation biology of Unionoida. As temporary parasites, mussels must primarily evade the innate immune responses of the host, rather than the adaptive (acquired) responses. Evolution of host specificity is associated with selective encounter of host taxa, either because of host attraction strategies or because of dominance of particular host species in the habitat. The intricate relationships between mussels and fish are easily disrupted and, thus, contribute to the imperilment of many mussel species, yet they also fascinate us and compel conservation efforts.

Molecular phylogeny of the Nearctic and Mesoamerican freshwater mussel genus Megalonaias

“…The Unionidae is Earth's most diverse freshwater bivalve family and is well-known for its imperiled conservation status and remarkable parasitic life history (Barnhart et al, 2008;Graf, 2013;Haag & Williams, 2013). Although the higher-level classification of the Unionidae is unstable (Whelan et al, 2011;Pfeiffer & Graf, 2015;Lopes-Lima et al, 2016;Bolotov et al, 2017), it remains clear that the subfamily Ambleminae has experienced the most dramatic evolutionary radiation, representing over half of the species-level diversity of the family.…”

“…Understanding the evolution and ecology of the Ambleminae and its tribes is an important focus of freshwater biodiversity research in North America and has positively influenced many aspects of applied freshwater science (e.g., Serb et al, 2003;Zanatta & Murphy, 2006;Barnhart et al, 2008;Haag & Rypel, 2011;Campbell & Lydeard, 2012;Haag, 2012); however, the current theory of amblemine phylogeny, biogeography, and ecology is strongly geographically biased due to the near complete exclusion of Mesoamerican taxa from recent research. Comprehensive understanding of the Ambleminae, its tribes, and several of its genera, necessitates inclusion of Mesoamerican representatives, and their consideration is likely to have major implications in various disciplines of freshwater mussel research (e.g., evolutionary biology, ecology, and conservation).…”

Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): Defining modern subfamilies and tribes

“…Gln was divided into three size classes: small (60.020), medium (>0.020 and 60.070) and large (>0.070). These classes were determined using all glochidia measurements collected for this study (Table C1) and those included in Barnhart et al (2008) and Hoggarth (1999); the smaller size range of Quadrulini was used to define the class 'small'; the larger size range of Anodontini was used to define the class 'large'; and the 'medium' class size was defined with intermediate Gln values between the two other classes.…”

“…Due to their ecological and economic importance, interesting biological traits (e.g., a parasitic life with the reproductive dependence on a host fish and a particular form of mitochondrial inheritance called double uniparental inheritance; Barnhart et al, 2008;Breton et al, 2007;Hoeh et al, 1996Hoeh et al, , 2002a, scientific research on Unionida has grown in recent years (Haag, 2012;Lopes-Lima et al, 2014). However, taxon-based conservation efforts focused on the Unionidae are hindered by various phylogenetic and taxonomic uncertainties (e.g., Inoue et al, 2014;, and many species, especially those outside of North America and Western Europe, have been assigned a Data Deficient status by the IUCN (Bogan and Roe, 2008;IUCN, 2015;Kohler et al, 2012).…”

Continuous reproduction of Sinanodonta woodiana (Lea, 1824) females: an invasive mussel species in a female-biased population

“…Glochidia attached to the fish body migrate to certain distances, undergo metamorphosis, and begin a relatively sedentary lifestyle in a new habitat (Kat, 1984;Rogers-Lowery & Dimock, Rogers-Lowery et al, 2006). Most unionid species are also generalists with respect to the choice of host, including cases of encystation on the body of fish species with which they do not coexist in the areas of their natural range of distribution (Barnhart et al, 2008;Łabęcka, 2009;Douda et al, 2012). In addition to the natural tendency of organisms for expansion, many spectacular examples of extension in the distribution range of different aquatic species have been observed in connection with the development of the transport and construction of channels linking river and marine catchment basins (Hebert et al, 1989).…”