Evolutionary Dynamics of Parasitic Larval Ecology and Lure Mimicry in North American Freshwater Mussels (Unionidae: Bivalvia: Mollusca)

Abstract

Freshwater mussels in the order Unionoida exhibit two outstanding attributes. Although only one of nine freshwater bivalve lineages, they dominate that group representing over 75% of species. They also have an extraordinary life cycle that includes obligatory parasitic larval development on fish hosts, and gravid females have evolved a spectrum of strategies, including mimicry, to increase the probability of host infection. The primary goal of my thesis was to test the hypothesis that the unique larval ontogeny and ecology of unionid freshwater mussels has contributed to the extraordinary diversification of this group. To do this, I focused on North American unionids using three complimentary levels of investigation: at macro-, meso-, and microevolutionary scales. I used available mussel and fish phylogenies, as well as a database of known mussel-host interactions, to address macroevolutionary and ecological aspects of mussel-fish interaction across North American watersheds. Despite the brief duration of their parasitic larval phase, mussels exhibited a similar, right-skewed distribution of host specialization to most other parasite lineages. I also found that genetic distance, range overlap, and number of citations of mussel taxa were most associated with the degree of fish host sharing. Competition for fish hosts is therefore likely to be a major influence on unionid evolution and diversification. I used a phylogenomic approach to reconstruct the evolution of host infection strategies in the diverse and imperiled Lampsiline clade to put host use in an evolutionary context and to estimate speciation rates. Lampsilines have evolved diverse, elaborate mimetic lures to attract fish hosts and the phylogeny indicates an early evolution of mimetic mantle lures, with the subsequent evolution of brood lures. Additionally, I observed strong clade-specific fidelity of host use, as well as an increase in diversification rates associated with the evolution of a composite host infection strategy involving both mantle and simple brood lures and targeting centrarchid basses. I argue that lampsiline mussels represent a cryptic adaptive radiation, where ecological diversification occurs primarily during the brief parasitic larval stage. That hypothesis is consistent with larval development and ecology being a driver of diversification in the group and may help explain the ecological co-persistence of so many mussel species in North American watersheds without distinct (post-larval) niches.The microevolutionary component was an integrative study of the evolution, behavior, and ecology of diverse mantle lure phenotypes in Lampsilis fasciola. I confirmed that this represents a true polymorphism using a phylogenomic approach and by documenting within-brood polymorphism. I then identified putative model species (darters and a leech) for both main phenotypes in the Raisin River study population. Although differing in both coloration and morphology, this polymorphism does not include a significant behavioral component. The discrete nature of its within-brood inheritance suggests that the polymorphism may be regulated by a single locus, and that this system could serve as a model system for identifying underlying genes controlling mantle lure evolution in lampsilines. Each chapter of my dissertation analyzes the role of larval ontogeny on freshwater mussel biodiversity from a different perspective and this research has obtained considerable supporting evidence for the importance of the larval ontogeny in the diversification of freshwater mussels, although it has also highlighted the need for more data at multiple scales. Accurate, high-resolution data of mussel-host interactions in natural settings is necessary to build useful models of this complex evolutionary system.