Abstract
The transition from aquatic to terrestrial life presented tetrapodamorphs with the challenge of maintaining water homeostasis and preventing desiccation on land. The colon evolved in terrestrial vertebrates to help maintain fluid balance. Although marine elasmobranchs lack a colon, their spiral intestine contains a subregion that histologically appears to be colon-like, possibly representing an evolutionary precursor to terrestrial digestive tracts. The distal-most region of the spiral intestine of elasmobranchs has no villi and a large number of acid mucins: hallmarks of water absorption in the colons of terrestrial animals. To determine if histologically distinct regions of the elasmobranch digestive tract correspond to functional differences, we compared water absorption in different subregions of the skate, Leucoraja erinacea digestive tract. Water absorption in stomach and spiral intestinal sacs was linear with time and not hydrostatic pressure-dependent. The histologically distinct distal portion of the spiral intestine had a threefold higher rate of water absorption than the proximal portion of the spiral intestine. In addition, the water-selective, colon-specific aquaporin 4 is expressed strongly in the distal spiral intestine epithelia, correlating with the region of the spiral intestine exhibiting the greatest rate of water absorption. We demonstrate that the distal spiral intestine is histologically and functionally distinct from the rest of the spiral intestine and represents a rudimentary colon within the vertebrate lineage.
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Acknowledgments
We thank D. Evans for manuscript comments and the MDIBL animal core (Salisbury Cove, ME) for L. erinacea animals. NAT received support from a MDIBL New Investigator Award and the Skidmore-Union Network, a project established with a NSF ADVANCE PAID grant. Support for undergraduate research came from the REU Site at MDIBL (NSF DBI-0453391), a Sciortino Cancer Research Fellowship, and a Union College Summer Fellowship Award to A.S. MDIBL is supported by Award Number P20RR016463 from the National Center for Research Resources. The content of this paper is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Research Resources or the National Institutes of Health.
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Theodosiou, N.A., Simeone, A. Evidence of a rudimentary colon in the elasmobranch, Leucoraja erinacea . Dev Genes Evol 222, 237–243 (2012). https://doi.org/10.1007/s00427-012-0406-8
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DOI: https://doi.org/10.1007/s00427-012-0406-8