Glacial vicariance and secondary contact shape demographic histories in a freshwater mussel species complex.

Characterizing the mechanisms influencing the distribution of genetic variation in aquatic species can be difficult due to the dynamic nature of hydrological landscapes. In North America's Central Highlands, a complex history of glacial dynamics, long-term isolation, and secondary contact have shaped genetic variation in aquatic species. Although the effects of glacial history have been demonstrated in many taxa, responses are often lineage- or species-specific and driven by organismal ecology. In this study, we reconstruct the evolutionary history of a freshwater mussel species complex using a suite of mitochondrial and nuclear loci to resolve taxonomic and demographic uncertainties. Our findings do not support Pleurobema rubrum as a valid species, which is proposed for listing as threatened under the U.S. Endangered Species Act. We synonymize P. rubrum under Pleurobema sintoxia-a common and widespread species found throughout the Mississippi River Basin. Further investigation of patterns of genetic variation in P. sintoxia identified a complex demographic history, including ancestral vicariance and secondary contact, within the Eastern Highlands. We hypothesize these patterns were shaped by ancestral vicariance driven by the formation of Lake Green and subsequent secondary contact after the last glacial maximum. Our inference aligns with demographic histories observed in other aquatic taxa in the region and mirrors patterns of genetic variation of a freshwater fish species (Erimystax dissimilis) confirmed to serve as a parasitic larval host for P. sintoxia. Our findings directly link species ecology to observed patterns of genetic variation and may have significant implications for future conservation and recovery actions of freshwater mussels.

Strong, Recent Selective Sweeps Reshape Genetic Diversity in Freshwater Bivalve Megalonaias nervosa.

Freshwater Unionid bivalves have recently faced ecological upheaval through pollution, barriers to dispersal, harvesting, and changes in fish-host prevalence. Currently, over 70% of species in North America are threatened, endangered or extinct. To characterize the genetic response to recent selective pressures, we collected population genetic data for one successful bivalve species, Megalonaias nervosa. We identify megabase-sized regions that are nearly monomorphic across the population, signals of strong, recent selection reshaping diversity across 73 Mb total. These signatures of selection are greater than is commonly seen in population genetic models. We observe 102 duplicate genes with high dN/dS on terminal branches among regions with sweeps, suggesting that gene duplication is a causative mechanism of recent adaptation in M. nervosa. Genes in sweeps reflect functional classes important for Unionid survival, including anticoagulation genes important for fish host parasitization, detox genes, mitochondria management, and shell formation. We identify sweeps in regions with no known functional impacts, suggesting mechanisms of adaptation that deserve greater attention in future work on species survival. In contrast, polymorphic transposable elements (TEs) appear to be detrimental and underrepresented among regions with sweeps. TE site frequency spectra are skewed toward singleton variants, and TEs among regions with sweeps are present at low frequency. Our work suggests that duplicate genes are an essential source of genetic novelty that has helped this species succeed in environments where others have struggled. These results suggest that gene duplications deserve greater attention in non-model population genomics, especially in species that have recently faced sudden environmental challenges.

Assessing Genomic Diversity, Connectivity, and Riverscape Genetics Hypotheses in the Endangered Rough Hornsnail, Pleurocera Foremani, Following Habitat Disruption.

The southeastern United States is home to some of the richest biodiversity in the world. Over the last 200 years, however, rapid industrialization and urbanization have threatened many natural areas, including freshwater habitats. River impoundments have also rapidly altered freshwater habitats, often resulting in species extirpation or extinction. The Coosa River in Alabama experienced one of the largest faunal declines in modern history after impoundment, making it an ideal system for studying how invertebrate species are affected by reservoir creation. One such species, the Rough Hornsnail, Pleurocera foremani, is an endangered freshwater snail in the family Pleuroceridae. We sampled all known localities of P. foremani and used 2bRAD-seq to measure genetic diversity. We assessed riverscape genomic patterns across the current range of P. foremani and measured gene flow within and between impoundments. We also investigated the degree to which P. foremani displays an isolation by distance pattern and conforms to broad hypotheses that have been put forth for population genetics of riverine species like the Mighty Headwater Hypothesis that predicts greater genetic diversity in headwater reaches compared with mainstem populations. Like most other freshwater species, a pattern of isolation by distance was observed in P. foremani. We also found that Coosa River dams are a barrier to gene flow, and genetic fragmentation of P. foremani is likely to increase. However, gene flow appeared common within reservoirs and tributaries. Additionally, we found that spatial genetic structure of P. foremani deviates from what is expected under the Mighty Headwaters Hypothesis, adding to a growing body of research suggesting that the majority of genetic diversity in low-dispersing gastropods is found in mainstem populations.

Gene family amplification facilitates adaptation in freshwater unionid bivalve Megalonaias nervosa.

Freshwater unionid bivalves currently face severe anthropogenic challenges. Over 70% of species in the United States are threatened, endangered or extinct due to pollution, damming of waterways and overfishing. These species are notable for their unusual life history strategy, parasite-host co-evolution and biparental mitochondrial inheritance. Among this clade, the washboard mussel Megalonaias nervosa is one species that remains prevalent across the Southeastern United States, with robust population sizes. We have created a reference genome for M. nervosa to determine how genome content has evolved in the face of these widespread environmental challenges. We observe dynamic changes in genome content, with a burst of recent transposable element proliferation causing a 382 Mb expansion in genome content. Birth-death models suggest rapid expansions among gene families, with a mutation rate of 1.16 × 10-8 duplications per gene per generation. Cytochrome P450 gene families have experienced exceptional recent amplification beyond expectations based on genome-wide birth-death processes. These genes are associated with increased rates of amino acid changes, a signature of selection driving evolution of detox genes. Fitting evolutionary models of adaptation from standing genetic variation, we can compare adaptive potential across species and mutation types. The large population size in M. nervosa suggests a 4.7-fold advantage in the ability to adapt from standing genetic variation compared with a low diversity endemic E. hopetonensis. Estimates suggest that gene family evolution may offer an exceptional substrate of genetic variation in M. nervosa, with Psgv  = 0.185 compared with Psgv  = 0.067 for single nucleotide changes. Hence, we suggest that gene family evolution is a source of 'hopeful monsters' within the genome that may facilitate adaptation when selective pressures shift. These results suggest that gene family expansion is a key driver of adaptive evolution in this key species of freshwater Unionidae that is currently facing widespread environmental challenges. This work has clear implications for conservation genomics on freshwater bivalves as well as evolutionary theory. This genome represents a first step to facilitate reverse ecological genomics in Unionidae and identify the genetic underpinnings of phenotypic diversity.

The effect of bivalve filtration on eDNA-based detection of aquatic organisms.

As the use of environmental-DNA (eDNA) expands as a method to detect the presence and quantity of aquatic taxa, factors potentially impacting the efficacy of this technique must be investigated. Many studies have examined the effects of abiotic parameters on the degradation of environmental-DNA (e.g. UV radiation, pH, temperature, etc.), however, few have focused on biotic effectors. Through high-filtering rates coupled with dense colonization, Asian clams (Corbicula fluminea) are able to drastically alter the quantity of particulate matter through translocation into the sediment, potentially including sources of eDNA in lotic and lentic systems. Using a longitudinal, laboratory experiment, we tested the effect of varying densities of Asian clams on the translocation rate of common goldfish (Carassius auratus) DNA. Target DNA in testing tanks was quantified through quantitative PCR (qPCR) at regular intervals and compared. Tanks housing the highest density of Asian clams produced significantly lower DNA concentrations over time compared to tanks of lower densities. These results show, for the first time, a density-dependent reduction of local eDNA sources by bivalve filtration that may lead to the obstructed detection of target species through the sampling of eDNA. Based on these findings, we recommend highly concentrated bivalve populations be taken into consideration when choosing the time and locality of eDNA sampling efforts.

On the identity of Leptoxis taeniata - a misapplied name for the threatened Painted Rocksnail (Cerithioidea, Pleuroceridae).

The Painted Rocksnail, currently known as Leptoxis taeniata, is a federally threatened species native to the Mobile River basin in Alabama, USA. Presently restricted to four disjunct populations, the species is at considerable risk of extinction after a range decline of over 95% in the 20th century because of habitat alteration following impoundment of the Coosa River. Here, we reassess the identity and historical range of the Painted Rocksnail to improve communication and conservation efforts for the species. We determined that L. taeniata is a synonym of L. picta and that the name L. taeniata has been misapplied to the current concept of the Painted Rocksnail for which L. coosaensis is the oldest available name. Leptoxis coosaensis and L. picta are herein redescribed. After examination of historical material, we determined that records of the Painted Rocksnail outside the Coosa River drainage were misidentifications. Thus, we redefine the historical range of the Painted Rocksnail as restricted to the Coosa River and select tributaries above the Fall Line at Wetumpka, Alabama, rather than extending into the Alabama River as previously thought. Leptoxis coosaensis is in dire need of conservation, and management plans should take into consideration the revised historical range of the species.