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. 2024 May 24:12:e17359.
doi: 10.7717/peerj.17359. eCollection 2024.

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

Trevor L Hewitt  1 , Paul D Johnson  2 , Michael Buntin  2 , Talia Y Moore  1   3 , Diarmaid Ó Foighil  1
Affiliations

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

Trevor L Hewitt et al. PeerJ. .

Abstract

Unionoid freshwater mussels (Bivalvia: Unionidae) are free-living apart from a brief, obligately parasitic, larval stage that infects fish hosts, and gravid female mussels have evolved a spectrum of strategies to infect fish hosts with their larvae. In many North American species, this involves displaying a mantle lure: a pigmented fleshy extension that acts as an aggressive mimic of a host fish prey, thereby eliciting a feeding response that results in host infection. The mantle lure of Lampsilis fasciola is of particular interest because it is apparently polymorphic, with two distinct primary lure phenotypes. One, described as "darter-like", has "eyespots", a mottled body coloration, prominent marginal extensions, and a distinct "tail". The other, described as "worm-like", lacks those features and has an orange and black coloration. We investigated this phenomenon using genomics, captive rearing, biogeographic, and behavioral analyses. Within-brood lure variation and within-population phylogenomic (ddRAD-seq) analyses of individuals bearing different lures confirmed that this phenomenon is a true polymorphism. The relative abundance of the two morphs appears stable over ecological timeframes: the ratio of the two lure phenotypes in a River Raisin (MI) population in 2017 was consistent with that of museum samples collected at the same site six decades earlier. Within the River Raisin, four main "darter-like" lure motifs visually approximated four co-occurring darter species (Etheostoma blennioides, E. exile, E. microperca, and Percina maculata), and the "worm-like" lure resembled a widespread common leech, Macrobdella decora. Darters and leeches are typical prey of Micropterus dolomieui (smallmouth bass), the primary fish host of L. fasciola. In situ field recordings of the L. fasciola "darter" and "leech" lure display behaviors, and the lure display of co-occurring congener L. cardium, were captured. Despite having putative models in distinct phyla, both L. fasciola lure morphs have largely similar display behaviors that differ significantly from that of sympatric L. cardium individuals. Some minor differences in the behavior between the two L. fasciola morphs were observed, but we found no clear evidence for a behavioral component of the polymorphism given the criteria measured. Discovery of discrete within-brood inheritance of the lure polymorphism implies potential control by a single genetic locus and identifies L. fasciola as a promising study system to identify regulatory genes controlling a key adaptive trait of freshwater mussels.

Keywords: Behavior; Captive brood; Freshwater mussels; Mimicry; Parasitism; Polymorphism; ddRAD.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Illustration of Lampsilis fasciola life cycle.
(A) The life cycle of the freshwater mussel Lampsilis fasciola. A gravid female mussel displays a mantle lure, here a darter mimic, to the primary fish host, Micropterus dolomieu. This elicits an attack through which the host is infected by mussel parasitic larvae (glochidia). After a short infective period (~2 weeks), the parasitic larvae metamorphose into juvenile mussels that detach from the host and fall to the substrate. (B) (“darter-like”) and (C) (“worm-like”) depict the two primary phenotypes of lure observed in L. fasciola. The former (B) has “eyespots”, a mottled “main body” pigmentation composed of lateral and dorsal spots that can vary substantially in color, numerous and prominent marginal extensions, and a distinct “tail” region, whereas the latter lacks those features and has instead a uniform bright orange coloration underlain with a black basal stripe. Illustration by John Megahan.
Figure 2
Figure 2. Map displaying geographic range of Lampsilis fasciola and its primary host, Micropterus dolomieu, as well as sampling locations.
Map of eastern North America showing the estimated ranges of Lampsilis fasciola (orange) and of its primary host fish Micropterus dolomieu (green). Red dots indicate sampling sites: Raisin River at Sharon Mils County Park (A), Huron River at Hudson Mills Park (B), Paint Rock River (C) and Little Tennessee River (D). Base map layer is from U.S. Geological Survey (2022).
Figure 3
Figure 3. Photographs of Lampsilis fasciola brood raised at the Alabama Aquatic Biodiversity Center, as well as photographs of preserved lure rudiments.
The Lampsilis fasciola brood raised at the Alabama Aquatic Biodiversity Center from a wild, gravid female, with a “worm-like” mantle lure, sampled from the Paint Rock River in June 2009. (A) shows juvenile members of the brood after ~16 months in culture. (B and C) show single, sexually maturing females after ~2 years of culture. The young female in (B) displayed a developing “darter-like” mantle lure (with “eyespots”, mottled lateral coloration, marginal extensions, and a “tail”) whereas her full- or half-sibling in (C) displayed a “worm-like” mantle lure (lacking the “darter” characteristics and having orange pigmentation with a black underlay). (D and E) Respectively show photomicrographs, taken with a dissecting microscope, of 95% ethanol-preserved rudimentary “darter-like” and “worm-like” lures from two additional brood members, part of a 50-individual subsample preserved in 2011.
Figure 4
Figure 4. Phylogenomic tree displaying Lampsilis fasciola from two MI populations, one NC population, and the Paint Rock River brood raised at the Alabama Aquatic Biodiversity Center.
Phylogenomic tree of 96 Lampsilis fasciola individuals created in RAxML using 28,735 concatenated ddRAD-seq loci. Gravid, lure-displaying females sampled from two Michigan drainages, River Raisin and Huron River, are respectively highlighted in peach and pink. Specimens sampled from the Paint Rock River, Alabama are highlighted in blue and consisted of three gravid, lure-displaying females, in addition to 50 larval brood members raised at the Alabama Aquatic Biodiversity Center in the zoomed-in tip clade. Gravid, lure-displaying females sampled from the Little Tennessee River in North Carolina are highlighted in yellow. Boxes indicate primary mantle lure phenotypes—“darter-like” (gray) or “worm-like” (orange)—of all L. fasciola individuals.
Figure 5
Figure 5. The ratio of “worm-like” and “darter-like” Lampsilis fasciola lures over time in the River Raisin, MI, using historical and contemporary samples.
The observed frequency of River Raisin Lampsilis fasciola primary mantle lure phenotypes (“darter-like”; gray vs. “worm-like”; orange) at the Sharon Mills County Park study site during two different time periods. The 1954–1962 data were obtained from the University of Michigan Museum of Zoology (UMMZ) collection specimens, both female and male. The 2017 data were based on field observations of displaying females. (B) A jar of preserved UMMZ Sharon Mills specimens showing a “darter-like” and a “worm-like” mantle lure. (C) A “eyespot”, lateral pigmented blotches, and marginal extensions in a “darter-like” lure of a preserved specimen.
Figure 6
Figure 6. Panel displaying variability in the two primary lure phenotypes of Lampsilis fasciola.
Variability in lure phenotype, both within a population and across the range of Lampsilis fasciola. (A–D) are “darter-like” Raisin River (MI) lures photographed in the field at Sharon Mills County Park. (E) Depicts a “darter-like” lure displayed by a Paint Rock River (AL) female. (F–H) show field photographs of “worm-like” lures displayed by three Sharon Mills females, with specimen H being a younger adult. (I and J) are photographs of two captive AABC specimens, with “worm-like” lures, sourced from the Paint Rock River. The former photo (I), taken in 2011, shows a young (2-year old) female, a member of the captive brood, displaying her lure, and the latter photo (J) is of a female field-sampled in 2022, and showing a partially retracted mantle lure.
Figure 7
Figure 7. Illustration of hypothetical benthic assemblage of main Lampsilis fasciola lure groups, and proposed models.
A hypothetical Raisin River (Michigan) benthic assemblage showing displaying exemplars of the putative five main Lampsilis fasciola mimetic mantle lure groups (Figs. 6A–6D and 6F) present at the Sharon Mills County Park study site, together with their respective model species, and their primary receiver/fish host, Micropterus dolomieu. Also shown is a displaying Lampsilis cardium with a “small minnow” mimetic mantle lure (Patterson et al., 2018) and its putative model, Pimephales notatus, the most common fish species in the River Raisin (Smith, Taylor & Grimshaw, 1981). Illustration by John Megahan.
Figure 8
Figure 8. Estimated range maps for proposed models of Lampsilis fasciola lures.
Estimated range maps for five proposed models for Lampsilis fasciola lures compared to the estimated geographic range of Lampsilis fasciola (orange). (A) Etheostoma blennoides (red), (B) Etheostoma exile (mauve), (C) Percina maculata (yellow), (D) Etheostoma microperca (blue), and (E) Macrobdella decora (gray). Note the differences in spatial scales in the panels. Model Illustrations by John Megahan. Base map layers are from U.S. Geological Survey (2022).
Figure 9
Figure 9. Gait diagrams for three exemplar mussel displays; a “darter-like” L. fasciola, a “leech-like” L. fasciola, and a Lampsilis cardium.
Mantle lure gait diagrams for three representative individuals sampled. (A) shows a Lampsilis fasciola “darter” lure sample (https://figshare.com/articles/media/GH010077_cropped_mp4Polymorphism_in_the_aggressive_mimicry_lure_of_the_parasitic_freshwater_mussel_Lampsilis_fasciola/24850899), (B) displays a Lampsilis fasciola “leech” lure sample (https://figshare.com/articles/media/GH010579_cropped_mp4Polymorphism_in_the_aggressive_mimicry_lure_of_the_parasitic_freshwater_mussel_Lampsilis_fasciola/24850902), and (C) shows a Lampsilis cardium sample (https://figshare.com/articles/media/GH010060_cropped_mp4Polymorphism_in_the_aggressive_mimicry_lure_of_the_parasitic_freshwater_mussel_Lampsilis_fasciola/24847932). Red center lines indicate synchronized lure movement for both left and right mantle flaps, and black lines above and below the center line indicate independent left and right movements, respectively. The x-axis denotes time in seconds and frame number (120 fps).
Figure 10
Figure 10. Summary plots for behavioral analysis of the two primary Lampsilis fasciola lure phenotypes and Lampsilis cardium.
Boxplots from behavioral analyses of the two primary Lampsilis fasciola mantle lure phenotypes (“darter” vs. “leech”, N = 15,12 respectively) and of Lampsilis cardium (N = 4). The middle line in the represents the median, the gray rectangle represents the interquartile range, the whiskers represent the minimum and maximum, excluding outliers, which are defined by 1.5* the interquartile range. (A) Comparison of the mean interval between movements of left mantle flap (s). (B) The standard deviation of lure movement interval (s) as a proxy for variability. (C) The average duration of each mantle lure movement. (D) The proportion of movements that are left-right synchronized. Note that the value for L. cardium is 1.0 (all lure movements for all individuals were synchronized) and indicated with *. (A–C) Show means for left mantle flap movements only.
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Grants and funding

This work was financially supported through block grant funding through Rackham School of Graduate Studies, the Dr. Nancy Williams Walls award for field research, and the State Wildlife Grant Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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