Non-ammocoete larvae of Palaeozoic stem lampreys

Miyashita, Tetsuto; Gess, Robert W.; Tietjen, Kristen; Coates, Michael I.

doi:10.1038/s41586-021-03305-9

Cited by 48 publications

(95 citation statements)

References 33 publications

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“…Our work thus implies that the adult stage should be used to assess the cell type diversity of lampreys and its comparison with that of other species. This notion is in agreement with the recent discovery that ammocoetes represent an evolutionarily derived and not an ancestral life stage of lampreys 64 .…”

Section: Discussionsupporting

confidence: 92%

Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas

Lamanna

Hervas-Sotomayor

Oel

et al. 2022

Preprint

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The vertebrate brain emerged more than ~500 million years ago in common evolutionary ancestors. To systematically trace its cellular and molecular origins, we established a spatially resolved cell type atlas of the entire brain of the sea lamprey - a jawless species whose phylogenetic position affords the reconstruction of ancestral vertebrate traits - based on extensive single-cell RNA-seq and in situ sequencing data. Comparisons of this atlas to neural data from the mouse and other jawed vertebrates unveiled various shared features that enabled the reconstruction of the core cell type composition, tissue structures, and gene expression programs of the ancestral brain. However, our analyses also revealed key tissues and cell types that arose later in evolution. For example, the ancestral vertebrate brain was likely devoid of cerebellar cell types and oligodendrocytes (myelinating cells); our data suggest that the latter emerged from astrocyte-like evolutionary precursors on the jawed vertebrate lineage. Our work illuminates the cellular and molecular architecture of the ancestral vertebrate brain and provides a foundation for exploring its diversification during evolution.

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Section: Discussionsupporting

confidence: 92%

Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas

Lamanna

Hervas-Sotomayor

Oel

et al. 2022

Preprint

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“…Sea lamprey has a complex anadromous life cycle marked by a dramatic metamorphosis from a benthic filter-feeding larva (termed ‘ammocoete’) into a parasitic juvenile that migrates from FW to SW. After ~ 2 years at sea, the adults migrate upstream to spawn. Although the larval-juvenile metamorphosis has been morphologically conserved from at least the early Cretaceous, ~ 125 mya 45 , recent studies on fossil records suggest that ammocoetes are specializations of modern lampreys rather than a relic of ancient lampreys 46 .…”

Section: Introductionmentioning

confidence: 99%

Tissue and salinity specific Na+/Cl− cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)

Barany

Shaughnessy

Pelis

et al. 2021

Sci Rep

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Two orthologues of the gene encoding the Na+-Cl− cotransporter (NCC), termed ncca and nccb, were found in the sea lamprey genome. No gene encoding the Na+-K+-2Cl− cotransporter 2 (nkcc2) was identified. In a phylogenetic comparison among other vertebrate NCC and NKCC sequences, the sea lamprey NCCs occupied basal positions within the NCC clades. In freshwater, ncca mRNA was found only in the gill and nccb only in the intestine, whereas both were found in the kidney. Intestinal nccb mRNA levels increased during late metamorphosis coincident with salinity tolerance. Acclimation to seawater increased nccb mRNA levels in the intestine and kidney. Electrophysiological analysis of intestinal tissue ex vivo showed this tissue was anion absorptive. After seawater acclimation, the proximal intestine became less anion absorptive, whereas the distal intestine remained unchanged. Luminal application of indapamide (an NCC inhibitor) resulted in 73% and 30% inhibition of short-circuit current (Isc) in the proximal and distal intestine, respectively. Luminal application of bumetanide (an NKCC inhibitor) did not affect intestinal Isc. Indapamide also inhibited intestinal water absorption. Our results indicate that NCCb is likely the key ion cotransport protein for ion uptake by the lamprey intestine that facilitates water absorption in seawater. As such, the preparatory increases in intestinal nccb mRNA levels during metamorphosis of sea lamprey are likely critical to development of whole animal salinity tolerance.

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“…As developmental data on the retina for embryonic hagfish and lamprey is scarce, it is difficult to support this idea using current evidence. Similarly, it is difficult to use fossil data (fossils of juvenile cyclostomes are quite rare although some have recently been found (Miyashita et al, 2021)). Future work comparing retinogenesis in hagfish and lamprey could greatly help to explore this idea.…”

Section: Hagfish Eye Regression Via Paedomorphosismentioning

confidence: 99%

Hagfish to Illuminate the Developmental and Evolutionary Origins of the Vertebrate Retina

Bradshaw

Allison

2022

Front. Cell Dev. Biol.

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The vertebrate eye is a vital sensory organ that has long fascinated scientists, but the details of how this organ evolved are still unclear. The vertebrate eye is distinct from the simple photoreceptive organs of other non-vertebrate chordates and there are no clear transitional forms of the eye in the fossil record. To investigate the evolution of the eye we can examine the eyes of the most ancient extant vertebrates, the hagfish and lamprey. These jawless vertebrates are in an ideal phylogenetic position to study the origin of the vertebrate eye but data on eye/retina development in these organisms is limited. New genomic and gene expression data from hagfish and lamprey suggest they have many of the same genes for eye development and retinal neurogenesis as jawed vertebrates, but functional work to determine if these genes operate in retinogenesis similarly to other vertebrates is missing. In addition, hagfish express a marker of proliferative retinal cells (Pax6) near the margin of the retina, and adult retinal growth is apparent in some species. This finding of eye growth late into hagfish ontogeny is unexpected given the degenerate eye phenotype. Further studies dissecting retinal neurogenesis in jawless vertebrates would allow for comparison of the mechanisms of retinal development between cyclostome and gnathostome eyes and provide insight into the evolutionary origins of the vertebrate eye.

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Non-ammocoete larvae of Palaeozoic stem lampreys

Cited by 48 publications

References 33 publications

Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas

Reconstructing the ancestral vertebrate brain using a lamprey neural cell type atlas

Tissue and salinity specific Na+/Cl− cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)

Hagfish to Illuminate the Developmental and Evolutionary Origins of the Vertebrate Retina

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