Molluscan Genomics and Conservation

Abstract

Widespread anthropogenic stress in the southeastern United States, particularly in the Tennessee and Mobile River drainages, has led to a severe decline in aquatic species diversity. This decline coincides with an increased need to conserve remaining diversity and a lack of modern phylogenetic systematic reviews, which often hinders effective conservation planning. This dissertation uses restriction‐site‐associated DNA sequencing approaches and whole-genome sequencing in combination with phylogenomics, population genomics, and comparative genomics to evaluate species diversity and conservation needs within several lineages of freshwater snails and freshwater mussels from the southeastern United States. In chapter 1, we investigated how well previously developed biogeographic models, such as the Theory of Island Biogeography, the Stream Hierarchy Model or the Death Valley Model, can explain freshwater snail diversity in temperate springs in Central Alabama. We generated genome-scale data for two endemic spring-obligate freshwater snails, Elimia bellacrenata and Elimia cochliaris, using a 2b-RAD sequencing approach and found four species-level lineages, including two undescribed species. Each of these lineages had higher genetic diversity than most riverine pleurocerid species, as well as a history of population stability since the Pleistocene. These findings indicate that temperate, spring-endemic gastropods diversity patterns do not conform to previously developed biogeographic models. Furthermore, the use of these models in regional spring ecosystems may be obscuring unique characteristics within a fairly understudied freshwater system. In chapter 2, we conducted a comprehensive taxonomic revision of the highly imperiled freshwater snail genus Lithasia from the Ohio, Mississippi, Cumberland, and Tennessee River drainages. Genome-scale data was generated using a 3RAD-based sequencing approach and we assessed species diversity with maximum likelihood, species tree inference and phylogenetic network approaches. Our results reveal several polyphyletic lineages within Lithasia, which has resulted in the revival of five species from synonymy and seven additional species: Lithasia sanguinea sp. nov., Lithasia conanobrieni sp. nov., Lithasia garneri sp. nov., Lithasia silvestria sp. nov., Lithasia coronata sp. nov., Lithasia johnsoni sp. nov., and Lithasia picea sp. nov. described here. These findings highlight the importance of genomics when conducting modern systematic reviews, which are essential for conservation assessments within highly imperiled groups, such as freshwater mollusks. In chapter 3, we investigated the impacts of sympatric speciation, inter- and intraspecific gene flow, and incomplete lineage sorting for three sympatric species of freshwater snails in the Duck River in central Tennessee. Fine-scale sampling was conducted along the Duck River and genome-scale data was generated using a 3RAD sequencing approach for Lithasia geniculata, Lithasia fuliginosa, and Lithasia duttoniana. We utilized a combination of phylogenomics, population genomics, and morphology to identify species and then performed population genomic analyses to evaluate if any previously developed common riverscape genetic hypotheses could explain the genetic diversity patterns within the Duck River. Our results revealed that the Duck River has likely undergone rapid sympatric diversification due to the recovery of eight to ten ancestral populations and two non-monophyletic lineages. This study was the first to evaluate the population genomics of sympatric freshwater gastropods in the southeastern United States. In chapter 4, we generated the first high-quality genome for Margaritifera hembeli, which is a federally threatened freshwater mussel species in the United States. The genome was assembled from a combination of PacBio HiFi long-reads, Illumina paired-end short-reads, and RNA sequencing. We then scaffolded the assembled genome with Bionano SAPHYR optical mapping and performed whole genome annotation with the Funannotate pipeline. This genome is large and highly contiguous, with low heterozygosity and the highest amount of repeat content among previously published freshwater mussel genome assemblies. We also recovered an unusual homeobox gene arrangement and found two expanded gene families associated with shell matrix proteins involved in the formation of pearls and nacre. This genome contributes to a growing body of genome assemblies and will be a useful tool for future conservation research on freshwater mussels.