Aggressive mimicry lure polymorphisms in the parasitic mussel Lampsilis fasciola model fish or leech host prey and differ in morphology and pigmentation, but not in display behavior.

Abstract

Unionoid freshwater mussels (Bivalvia: Unionidae) are free-living apart from a brief, obligately parasitic, larval stage that infects fish hosts and gravid female mussels have evolved a spectrum of strategies to infect fish hosts with their larvae. In many North American species, this involves displaying a mantle lure: a pigmented fleshy extension that acts as an aggressive mimic of a host fish prey, thereby eliciting a feeding response that results in host infection. The mantle lure of Lampsilis fasciola is of particular interest because it is apparently polymorphic, with two distinct primary lure phenotypes. One, described as "darter-like", has "eyespots", a mottled body coloration, prominent marginal extensions, and a distinct "tail". The other, described as "worm-like", lacks those features and has an orange and black coloration. We investigated this phenomenon to 1) confirm that it is a true polymorphism; 2) investigate its ecological persistence; 3) identify the range of putative model species targeted by this mimicry system within a river drainage; 4) determine whether the mantle lure polymorphism includes a behavioral component. Detection of within-brood lure variation and within-population phylogenomic (ddRAD-seq) analyses of individuals bearing different lures confirmed that this phenomenon is a true polymorphism. It appears stable over ecological timeframes: the ratio of the two lure phenotypes in a River Raisin (MI) population in 2017 was consistent with that of museum samples collected at the same site 6 decades earlier. Within the River Raisin, four main "darter-like" lure motifs visually approximated four co-occurring darter species (Etheostoma blennioides, E. exile, E. microperca, and Percina maculata) and the "worm-like" lure resembled a widespread common leech, Macrobdella decora. Darters and leeches are typical prey of Micropterus dolomieui (smallmouth bass), the primary fish host of L. fasciola. In situ field recordings were made of the L. fasciola "darter" and "leech" lure display behaviors, in addition to the non-polymorphic lure display of co-occurring L. cardium. Despite having putative models in distinct phyla, both L. fasciola lure morphs have similar display behaviors that differ significantly from that of sympatric L. cardium individuals. We conclude that the L. fasciola mantle lure polymorphism does not include a behavioral component. Discovery of discrete within-brood inheritance of the lure polymorphism implies potential control by a single genetic locus and identifies L. fasciola as a promising study system to identify regulatory genes controlling a key adaptive trait of freshwater mussels.