Evolution of Different Migratory and Feeding Types in Lampreys

Of the 41 extant lamprey species that have been described, 18 are parasitic (on actinopterygian fishes) and 23 are nonparasitic (i.e., do not feed at all) following metamorphosis.  The nonparasitic “brook” lampreys all spend their entire life in fresh water, whereas parasitic lampreys may be either “typical” or “praecox” anadromous forms (the praecox forms are smaller, presumably due to a shorter time feeding at sea) or may feed entirely within freshwater.  In most lamprey genera, species with different migratory and feeding types have been grouped together into so-called “paired” or “satellite” species based on similarities in morphology and distribution.  Life history transitions therefore appear to have occurred repeatedly in lamprey evolution, with wide-ranging anadromous parasitic ancestors giving rise to more localized freshwater-resident forms and nonparasitic species evolving from a parasitic ancestor.  In this talk, we discuss which characteristics of parasitic species are fundamental to the evolution of nonparasitism by comparing those species for which there are no nonparasitic forms (i.e., sea and pouched lampreys) with those species for which one or more nonparasitic derivatives have been identified.  We conclude that the anadromous sea and pouched lampreys are distinguished from all other parasitic species by consistently attaining a large body size.  Those species that have given rise to nonparasitic derivatives are consistently smaller or at least produce small praecox forms in addition to the large anadromous forms.  We therefore suggest that the anadromous sea and pouched lamprey, as the result of wide-ranging offshore feeding (with an abundance of prey), have not been under selection to reduce the duration of their feeding phase.  In contrast, a reduction in the length of the parasitic phase would be expected in freshwater-resident lampreys and anadromous species feeding in more coastal waters; in these lampreys, a further reduction (i.e., elimination) of the feeding phase would produce nonparasitic lampreys.  Our observations led to the prediction that the Caspian lamprey (which is confined to the Caspian Sea, and in which a praecox form has been reported) is capable of giving rise to a nonparasitic form.  Although no such species has been identified, recent molecular data suggest that two Eudontomyzon brook lampreys may be distantly “paired” with this species.  We end by asking the question: Is the landlocked sea lamprey in the Laurentian Great Lakes (which is smaller and feeds for one year less than the anadromous form) now a “jumping off point” for the evolution of nonparasitism?