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First published online April 20, 2007
Journal of Experimental Biology 210, 1641-1652 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.003319

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Historical reconstructions of evolving physiological complexity: O₂ secretion in the eye and swimbladder of fishes

Michael Berenbrink

School of Biological Sciences, The University of Liverpool, Biosciences Building, Crown Street, Liverpool, L69 7ZB, UK

View larger version (19K): [in this window] [in a new window]   Fig. 1. Variability of the Root effect in haemolysates of selected African fishes. The magnitude of the Root effect is measured as the difference in percentage Hb O2 saturation between the two plateaus at high and low pH. Presence and absence of choroid and swimbladder retia mirabilia are indicated for each species. Hb O2 saturation of functional Hb was determined using diluted, air-equilibrated samples (5–15 µmol l–1 [Hb4]) by spectral deconvolution between 500 and 700 nm (Völkel and Berenbrink, 2000). Measurements were performed at 25°C without removal of organic phosphates in 50 mmol l–1 Tris HCl buffer (pH 8.0–6.5) and 50 mmol l–1 citrate buffer (pH 7.0–5.0) in the presence of 0.1 mol l–1 KCl (M. Berenbrink, unpublished). Fish line drawings modified after: Lehrbuch der Speziellen Zoologie. Begruendet von Alfred Kaestner. Band II: Wirbeltiere, 1991©Elsevier GmbH, Spektrum Akademischer Verlag, Heidelberg.

View larger version (65K): [in this window] [in a new window]   Fig. 2. The choroid rete mirabile in the eye of the rainbow trout. (A) Schematic drawing to illustrate the orientation of the vascular corrosion cast from which photomicrographs were taken. (B) View of vascular corrosion cast of left eye from inside the orbit. The opening in the lower centre presents the entry point of the optic nerve. (C) Area indicated by the broken rectangle in B at higher magnification, showing parallel array of intermingled arteries and veins in the choroid rete mirabile. (D) Dorsal view (anterior side is at the bottom) showing the connection between choroid rete mirabile and the dense network of choriocapillaries, which underlies the retina. Abbreviations: a, v, branches of the ophthalmic artery and vein, respectively; crm, choroid rete mirabile; cc, choriocapillaries. Scale bars, 2 mm in B and D, and 500 µm in C. (E) Simplified diagram of the mechanism for specific O2 secretion in the eye and swimbladder of fishes. The three essential components are indicated. See text for further explanation. A–D modified from Berenbrink (Berenbrink, 1995).

View larger version (69K): [in this window] [in a new window]   Fig. 3. Evolution of swimbladder and choroid retia mirabilia in jawed vertebrates. Blue and yellow boxes mark the presence of swimbladder and choroid retia mirabilia in living species, respectively. Open boxes indicate the absence of the respective structure, whereas no box indicates missing information. The status of ancestral species has been reconstructed on a composite branching diagram by maximum parsimony. Yellow and blue branches indicate the presence of the choroid and swimbladder rete mirabile, respectively. White and red branches indicate the absence and presence, respectively, of both structures in an ancestral species. The yellow arrow indicates the branch segment along which the choroid rete mirabile first evolved. The blue arrows indicate the subsequent evolution of a swimbladder rete mirabile in four separate groups. Modified after Berenbrink et al. (Berenbrink et al., 2005).

View larger version (34K): [in this window] [in a new window]   Fig. 4. Evolutionary reconstruction of the Root effect in jawed vertebrates. The underlying phylogenetic tree is based on the species and branching pattern shown in Fig. 3. The Root effect has been colour coded and its magnitude in ancestral species has been reconstructed on the z-plane of the structure by linear parsimony from values measured in living species as shown in Fig. 1. (A) The three-dimensional structure has been rotated to visualise the gradual increase of the Root effect in early ray-finned fishes (nodes c–f) after their ancestors diverged from the lineages of sharks (a) and lobe-finned fishes (including tetrapods, b). The red bar indicates the origin of the choroid rete mirabile in the branch leading to the bowfin and teleosts only after the Root effect had increased. (B) Enlarged part of the structure in A after rotation, showing two examples of secondary reductions of the Root effect in Ostariophysi. The Root effect is only ever reduced when the choroid rete mirabile has been lost. The latter is indicated by red bars. The oriental weather loach still has a swimbladder rete mirabile, whereas the two catfishes lack both types of rete (Fig. 3), consistent with a complete loss of the Root effect in the latter group. Ma, million years. Modified from Berenbrink et al. (Berenbrink et al., 2005).