A Review of the Evolution of Nonparasitism in Lampreys and an Update of the Paired Species Concept
Margaret F. Docker
Abstract.—In most lamprey genera, “paired” species exist in which the larvae (which are microphagous filter feeders) are morphologically similar but the adults differ dramatically, becoming parasitic on teleost fishes or nonparasitic (i.e., do not feed at all) following metamorphosis. Parasitic lampreys feed for several months to several years (either in their natal stream or after migrating to larger fresh or marine water bodies) before embarking on a nontrophic upstream migration, sexual maturation, and spawning (followed by death); nonparasitic lampreys eliminate the parasitic phase, begin sexual maturation toward the end of metamorphosis, and spawn and die within 6–10 months of metamorphosis. In each species pair, the reduction in the length of postlarval life in nonparasitic lampreys is generally accompanied by an increase in the length of the larval period (and size at metamorphosis) so that the evolution of nonparasitism appears to have occurred without a change in the overall life span. Rather, nonparasitism appears to have evolved as a result of a change in the timing of metamorphosis relative to the timing of sexual maturation. Conspicuous morphological (e.g., adult body size, relative eye and oral disk size) and histological (e.g., lack of a functional digestive tract) differences distinguish nonparasitic adults from parasitic forms, and most lamprey taxonomists recognize life history type as a species-specific characteristic. However, plasticity of feeding type (e.g., facultative parasitism) has been observed in some lamprey populations, and molecular data on a number of paired species show no genetic differentiation between sympatric species pairs and suggest a polyphyletic origin for several nonparasitic species. This paper reviews the paired species concept, the repeated and independent evolution of nonparasitism in different genera and even within species, the evidence for facultative parasitism or facultative nonparasitism in some lamprey species, and the potential for hybridization between paired species and attempts to answer the question, are brook lampreys “real” species? The tentative answer is that there likely is not a single answer for all lamprey species pairs; different species pairs represent speciation at different stages. Some pairs appear to be distinct species according to both the biological and phylogenetic species concepts (i.e., they are reproductively isolated and show reciprocal monophyly), although each is not necessarily fixed for feeding type. In contrast, other pairs may represent incipient speciation and others yet may be experiencing ongoing gene flow. Parallels are therefore drawn between different lamprey species pairs and the divergent life history types found in other animal taxa (e.g., echinoderms and amphibians) and other temperate fish species (e.g., anadromous and freshwater-resident salmonids).