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The evolution of lamprey (Petromyzontida) life history and the origin of metamorphosis

Abstract

Modern lampreys (Petromyzontiformes) are one of two lineages of surviving jawless fishes (agnathans), and are thus of critical importance to understanding the evolution of the vertebrates. Although their fossil record is meager, it appears they have remained morphologically conserved for at least 360 million years, but the origin of their multi-stage life history is unclear. Unlike hagfishes, the other extant group of jawless fishes, which exhibit direct development, all modern lampreys possess a complex life cycle which includes a long-lived freshwater larval (or ammocoete) period, followed by a true metamorphosis into a sexually-immature juvenile and then mature adult which differ dramatically in their morphology and ecology from the larva. Because of their basal position, it is critical to understand when the extant lamprey life history evolved, and if such a life history was present in the last common ancestor of agnathans and gnathostomes. Recent discoveries in paleontology, genomic analyses, and developmental biology are providing insights into this problem. The current review synthesizes these findings and concludes that the ancestral lamprey life cycle followed a direct development. We suggest that the larval period was short and relatively limited if present at all, but that the juvenile included modern larval traits; over the course of evolution, differential selection pressures throughout the lifetime produced distinct larval and juvenile/adult periods. Each period required the dramatically different morphologies seen in modern lampreys, ultimately requiring a true metamorphosis to accommodate the large changes in the body plan and to maximize the efficiency of each life period. As a result, modern lamprey life histories are a patchwork of ancestral and derived characters.

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Notes

  1. Conodonts are an enigmatic “fish-like” group, which may or may not be vertebrates. They suffered prodigious extinctions at the end of the Permian (250 million years [Ma] ago), but persisted until the end of the Triassic (201 Ma ago) when the whole lineage became extinct. For the purposes of the present paper they are assumed not to belong to the vertebrate family tree (Nelson et al. 2016). However, conodonts may be vertebrates and possibly cyclostomes (Janvier 2015).

  2. While the term “parasitic” is commonly used to describe feeding juvenile lampreys (Potter et al. 2015), juvenile lampreys actually display a range of feeding behaviors (Renaud et al. 2009) from predatory (consumption of multiple prey items) to fully parasitic (removal of a portion of prey item, without necessarily killing the host) which varies between species (Hardisty 2011) and across the juvenile stage (Bence et al. 2003; Madenjian et al. 2003). For instance, small landlocked sea lamprey (Petromyzon marinus) feed on the body fluids of hosts, and probably cause limited host mortality, but as they increase in size their feeding almost always ends in host death (Bence et al. 2003) even though only a portion of the host’s body is consumed (Bergstedt and Schneider 1988). In contrast, Carpathian lamprey (Eudontomyzon danfordi) consume varying portions of the prey, but often eat heart tissue and bones (Talabishka et al. 2012) suggesting a truly predatory relationship. Finally, Arctic lamprey (Lethenteron camtschaticum) stomach contents include fins, scales, vertebral columns, eggs, and internal organs of prey (Shink 2017) showing a range of possible feeding behaviors from parasitic to predatory. Regardless, the literature precedent is to describe lampreys as parasitic or non-parasitic, so the terms are adopted here.

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We thank the editor and two reviewers for helpful comments on an earlier draft which improved the manuscript.

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Correspondence to Thomas M. Evans.

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Evans, T.M., Janvier, P. & Docker, M.F. The evolution of lamprey (Petromyzontida) life history and the origin of metamorphosis. Rev Fish Biol Fisheries 28, 825–838 (2018). https://doi.org/10.1007/s11160-018-9536-z

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  • DOI: https://doi.org/10.1007/s11160-018-9536-z

Keywords

  • Basal vertebrate
  • Heterochrony
  • Life history
  • Metamorphosis