Comparative phylogenomics reveal complex evolution of life history strategies in a clade of bivalves with parasitic larvae (Bivalvia: Unionoida: Ambleminae)

Abstract

Freshwater mussels are a species-rich group with biodiversity patterns strongly shaped by a life history strategy that includes an obligate parasitic larval stage. In this study, we set out to reconstruct the life history evolution and systematics in a clade of freshwater mussels adapted to parasitizing a molluscivorous host fish. Anchored hybrid enrichment and ancestral character reconstruction revealed a complex pattern of life history evolution with host switching and multiple instances of convergence, including reduction in size of larvae, increased fecundity, and growth during encapsulation. Our phylogenomic analyses also recovered non-monophyly of taxa exhibiting multiple traits used as the basis for previous taxonomic hypotheses. Taxa with axehead shaped glochidia were resolved as paraphyletic, but our results strongly suggest the complex morphology is an adaptation to reduce larval size, with reduction in size further accentuated in taxa previously assigned to Leptodea. To more accurately reflect the evolutionary history of this group, we make multiple systematic changes, including the description of a new genus, Atlanticoncha gen. nov., and the synonymy of the genus Leptodea under Potamilus. Our findings contribute to the growing body of literature showing that cladistic hypotheses based solely on morphological characters, including larval morphology, can be flawed in freshwater mussels.

A High-Quality Reference Genome for a Parasitic Bivalve with Doubly Uniparental Inheritance (Bivalvia: Unionida)

“…A phylotranscriptomic approach nested P. streckersoni within the family Unionidae and a close relative to Lampsilis and Venustaconcha ellipsiformis ( fig. 1 ), aligning with previous phylogenetic studies ( Smith et al 2019 , 2020 ). The functional annotation returned 52,407 gene models (41,065 protein-coding genes, 11,342 tRNAs).…”

Gene family amplification facilitates adaptation in freshwater unionid bivalve Megalonaias nervosa

“…Phenotypic studies in freshwater bivalves have noted rampant convergence of forms across lineages (Inoue et al, 2013; Johnson et al, 2018; Pfeiffer et al, 2016; Smith et al, 2020; Williams et al, 2008), and phylogenetic analysis has been challenging in the face of variation rather than adherence to strict phenotypes (Campbell et al, 2005). Our preliminary analysis of gene trees based on transcriptome assemblies for six species is consistent with these previous challenges of phylogenetic placement based on both phenotypes and genetic analysis of few loci.…”

Resolving species boundaries in the critically imperiled freshwater mussel species,Fusconaia mitchelli(Bivalvia: Unionidae)

“…An integrative species concept using multiple independent lines of evidence is a powerful approach to species delimitation (De Queiroz, 2007), and this approach has been utilized with success in resolving taxonomic issues for freshwater mussels (Inoue, McQueen, Harris, & Berg, 2014; Johnson et al, 2018; Keogh & Simons, 2019; Lopes‐Lima, Bolotov, et al, 2018; Smith et al, 2018, 2019, 2020). In this study, we utilized multiple data types to re‐evaluate species boundaries in F .…”

“…Molecular genetic studies on freshwater mussels that address phylogenetic placement and species boundaries have been pivotal in inferring important biological characteristics of species (e.g., host use, reproductive traits, habitat preference) and ensuring the taxonomic validity of protected species or those being considered for protection (Johnson et al, 2018; Pfeiffer, Johnson, Randklev, Howells, & Williams, 2016; Smith, Johnson, Pfeiffer, & Gangloff, 2018). Although considerable progress has been made in understanding ecology (Dudding, Hart, Khan, Robertson, Lopez, & Randklev 2019; Hart, Haag, Bringolf, & Stoeckel, 2018; Johnson, McLeod, Holcomb, Rowe, & Williams, 2016; Sietman, Hove, & Davis, 2018) and evolution (Inoue, Harris, Robertson, Johnson, & Randklev, 2020; Lopes‐Lima et al, 2017; Pfeiffer, Atkinson, et al, 2019; Pfeiffer, Breinholt, & Page, 2019; Smith, Johnson, Inoue, Doyle, & Randklev, 2019; Smith, Pfeiffer, & Johnson 2020) of freshwater mussels in recent years, many species still remain poorly understood and species validity has not been confirmed using robust molecular genetic analyses (Haag, 2012; Lopes‐Lima, Burlakova, et al, 2018). This is certainly the case in the southwestern United States, where diversity, distribution, and ecology of many mussel species are still poorly understood (Haag, 2012; Howells, Neck, & Murray, 1996).…”