Challenges for Diadromous Fishes in a Dynamic Global Environment

Postglacial Recolonization and the Loss of Anadromy in Rainbow Smelt from Coastal Newfoundland

Ian R. Bradbury, Mark W. Coulson, Steven E. Campana, Eric Baggs, and Paul Bentzen


Abstract.—Postglacial colonization of temperate latitudes by anadromous fishes has frequently resulted in radiation into multiple migration and morphological phenotypes, among which evolutionary relationships are often poorly understood. Freshwater phenotypes may be derived from freshwater forms or independent postglacial colonization by a marine ancestor (i.e., raceme structure). We examined genetic and morphological variation associated with the transition from anadromy to freshwater residency in rainbow smelt Osmerus mordax. Colonization pathways were reconstructed using nine microsatellite loci and mtDNA sequence data, between three pairs of anadromous and adjacent landlocked populations in southeastern Newfoundland. Microsatellite data indicate strong associations between adjacent anadromous and freshwater populations in two of three pairs consistent with independent parallel colonization. In contrast mtDNA sequence analysis suggests little variation and colonization of most of the region by a single glacial race. To explore the independent parallel transition from anadromous to nonanadromous populations, we document a novel estuarine dwarf phenotype inhabiting a partially landlocked fjord (Holyrood Pond) and examine the hypothesis that this estuarine dwarf represents a transitional form between the commonly observed anadromous and freshwater morphs. Habitat reconstructions using LA-ICP-MS and otolith elemental composition from each of the anadromous and freshwater locations as well as Holyrood Pond indicate that Holyrood Pond smelt exist primarily in a stable estuarine environment. Likewise, microsatellite loci show similar levels of diversity and only moderate divergence between nearby anadromous locations and Holyrood Pond. In contrast, morphological and shape variation suggests some similarities between Holyrood Pond and freshwater dwarfs. Comparison of phenotypic and genetic differentiation (i.e., PST and FST) suggest phenotypic convergence among freshwater forms and a greater phenotypic similarity between freshwater and Holyrood Pond dwarfs than between Holyrood Pond and anadromous locations. Estimates of PST were twice those of FST between anadromous and Holyrood Pond smelt consistent with divergence with gene flow. We conclude that postglacial colonization in smelt primarily occurs independently through parallel radiations, and may occur even in the presence of gene flow likely resulting in large variation in migration phenotype and life history.