Phenotypic Plasticity, Multiple Paternity, and Shell Shape Divergence Across Lake‐Stream Habitats in a Freshwater Mussel Brood (<scp><i>Pyganodon grandis</i></scp>)

ABSTRACT Hydrodynamic forces and their absence appear to exert differential selection pressure on aquatic biodiversity in lake and stream habitats, creating a tight fit between organismal phenotypes and their environments. Ecophenotypic variants may be the result of genetic differentiation or phenotypic plasticity, where a genotype can produce multiple phenotypes dependent on the environment. Freshwater mussels possess a wide degree of morphological variation that frequently covaries with the environment, making them a good system to understand the mechanisms of ecophenotypic variation across hydrological conditions. We designed a two‐year experiment where individuals from the same Pyganodon grandis maternal brood (half and full siblings) were reared at a controlled site and four natural sites involving one lake and three streams. At the end of the experiment, shell shape was quantified for recaptured ( N = 70), wild ( N = 206), and zoo‐reared ( N = 305) mussels. The maternal individual and 46 recaptured mussels were sequenced for genomic single nucleotide polymorphisms to test for multiple paternity and its effect on offspring morphology. Analysis of covariance found significant differences in shell shape between rearing sites, particularly between stream and lake habitats, but no shape differences were detected across the three stream sites. At two of the four sites, the shell shape of recaptured individuals was not significantly different than that of wild populations. Genomic sequencing and parentage analysis identified 11–27 different fathers among recaptured individuals. Yet no genetic differences were present between stream and lake habitats, and there was no paternal effect on shell shape. Taken together, phenotypic plasticity, over genetic differentiation, is identified as the primary mechanism of ecophenotypic variation. Plasticity is likely ubiquitous across freshwater mussels and may be a key adaptation given their high variance in habitat use. Multiple paternity may also play a role in the evolution of phenotypic plasticity, allowing more males from greater distances opportunities for fertilization, thus increasing genetic connectivity. Lastly, phenotypic plasticity and multiple paternity are convenient properties for freshwater mussel conservation and propagation. Multiple fathers increase the genetic variation of propagated broods, while plasticity may provide resilience to the release of stocked individuals across environmental heterogeneity.