Evolution of diverse host infection mechanisms delineates an adaptive radiation of lampsiline freshwater mussels centered on their larval ecology

Abstract

North American watersheds contain a high diversity of freshwater mussels (Unionoida). During the long-lived, benthic phase of their life cycle, up to 40 species can co-occur in a single riffle and there is typically little evidence for major differences in their feeding ecology or microhabitat partitioning. In contrast, their brief parasitic larval phase involves the infection of a wide diversity of fish hosts and female mussels have evolved a spectrum of adaptations for infecting host fish with their offspring. Many species use a passive broadcast strategy: placing high numbers of larvae in the water column and relying on chance encounters with potential hosts. Many other species, including most members of the Lampsilini, have a proactive strategy that entails the use of prey-mimetic lures to change the behavior of the hosts, i.e., eliciting a feeding response through which they become infected. Two main lure types are collectively produced: mantle tissue lures (on the female’s body) and brood lures, containing infective larvae, that are released into the external environment. In this study, we used a phylogenomic approach (ddRAD-seq) to place the diversity of infection strategies used by 54 North American lampsiline mussels into an evolutionary context. Ancestral state reconstruction recovered evidence for the early evolution of mantle lures in this clade, with brood lures and broadcast infection strategies both being independently derived twice. The most common infection strategy, occurring in our largest ingroup clade, is a mixed one in which mimetic mantle lures are apparently the predominant infection mechanism, but gravid females also release simple, non-mimetic brood lures at the end of the season. This mixed infection strategy clade shows some evidence of an increase in diversification rate and most members use centrarchids (Micropterus & Lepomis spp.) as their predominant fish hosts. Broad linkage between infection strategies and predominant fish host genera is also seen in other lampsiline clades: worm-like mantle lures of Toxolasma spp. with sunfish (Lepomis spp.); insect larvae-like brood lures (Ptychobranchus spp.), or mantle lures (Medionidus spp., Obovaria spp.), or mantle lures combined with host capture (Epioblasma spp.) with a spectrum of darter (Etheostoma & Percina spp.) and sculpin (Cottus spp.) hosts, and tethered brood lures (Hamiota spp.) with bass (Micropterus spp.). Our phylogenetic results confirm that discrete lampsiline mussel clades exhibit considerable specialization in the primary fish host clades their larvae parasitize, and in the host infection strategies they employ to do so. They are also consistent with the hypothesis that larval resource partitioning of fish hosts is an important factor in maintaining species diversity in mussel assemblages. We conclude that, taking their larval ecology and host-infection mechanisms into account, lampsiline mussels may be legitimately viewed as an adaptive radiation.

Dead‐end hollow fiber ultrafiltration capture of environmental DNA for freshwater mussel (Unionidae) species detection with metabarcoding

“…Previous studies have also shown limited ability of mitochondrial DNA (mtDNA) to distinguish between members of the genus Elliptio (e.g., Inoue et al, 2018), suggesting further investigation is needed to determine whether mtDNA variation is insufficient to separate valid species or if taxonomic revision is warranted. Similarly, available mtDNA sequences show low interspecific divergence between L. cardium and L. satura ; however, a recent phylogenomic study using single‐nucleotide polymorphisms (SNPs) supported recognizing both as distinct, monophyletic taxa (Hewitt et al, 2021). The reliance of eDNA studies on comprehensive DNA libraries and accurate taxonomy amplifies the need for further refinement of unionid systematics and taxonomy; this was identified as the top issue in a national strategy for the conservation of native freshwater mussels by the Freshwater Mollusk Conservation Society (2016).…”

“…Previous studies have also shown limited ability of mitochondrial DNA (mtDNA) to distinguish between members of the genus Elliptio (e.g., Inoue et al, 2018), suggesting further investigation is needed to determine whether mtDNA variation is insufficient to separate valid species or if taxonomic revision is warranted. Similarly, available mtDNA sequences show low interspecific divergence between L. cardium and L. satura; however, a recent phylogenomic study using single-nucleotide polymorphisms (SNPs) supported recognizing both as distinct, monophyletic taxa (Hewitt et al, 2021).…”

Aggressive mimicry lure polymorphisms in the parasitic musselLampsilis fasciolamodel fish or leech host prey and differ in morphology and pigmentation, but not in display behavior

“…Timmermans et al (2020) used SNP data from Papilio dardanus to discover a genomic inversion associated with its mimetic polymorphism, and this approach is likely also tractable for Lampsilis fasciola given the availability of polymorphic broods – we are currently raising an additional polymorphic brood at the AABC. Mantle lures are a key adaptive trait in Lampsiline evolution and diversification (Hewitt, Haponski & Foighil, 2021) and Lampsilis fasciola is a promisinga highly tractable model system to uncover the genetics of lure development and variation in unionoid mussel.…”

Polymorphism in the aggressive mimicry lure of the parasitic freshwater mussel Lampsilis fasciola

“…The variability in lure display behavior among species of unionid is not well understood. Mimetic mantle lures predominate in Lampsilini, a major clade of North American freshwater mussels recently identified as a cryptic adaptive radiation centered on larval ecologies and specialized host-infection behaviors ( Hewitt, Haponski & Ó Foighil, 2021b ). This interaction is referred to as ‘cryptic’ because the specific host-parasite interactions are transient and difficult to determine in-situ .…”

“…Although mimetic mantle lures are a key adaptive trait of freshwater mussel diversification, the genetic regulators underlying their formation ( Kramer, 1970 ), variation ( Haag, Warren & Shillingsford, 1999 ; Zanatta, Fraley & Murphy, 2007 ; Barnhart, Haag & Roston, 2008 ), and evolution ( Zanatta & Murphy, 2006 ; Hewitt, Haponski & Ó Foighil, 2021b ) remain completely unknown. This gap in our knowledge is exacerbated by the stark conservation status of North American freshwater mussels, with two thirds of species classified as threatened or near-threatened ( Lopes-Lima et al, 2018 ).…”