Development of Convergent Adaptations Reveal Highly Conserved Early Ontogenetic Skull Shape in Fishes with Amphibious Vision

Overview

Journal Sci Rep

Specialty Science

Date 2025 Mar 12

PMID 40069558

Authors

Philipp Thieme

Vivian Fischbach

Ioannis Papadakis

Timo Moritz

Affiliations

Soon will be listed here.

Abstract

The development of skeletal elements in fish is strongly influenced by the functional demands and environmental constraints they face during different life stages but mostly occurs during their larval development. One example of late modifications within the skeletal system is the adaptation of the skull and eye morphology that allows for amphibious vision in the four-eyed fishes Anableps spp. Another species that is equally capable of simultaneous aquatic and aerial vision, Rhinomugil corsula, has been widely neglected in this field of research, although it presents great opportunities for comparative analyses on the evolution of this ability. We studied the development of the skull and eyes of Rhinomugil based on morphological, morphometric, and histological data. While cross sections reveal that the eyes develop required morphological adaptations for simultaneous amphibious vision in larval life stages, the restructuring of the neurocranium which causes the dorsolateral relocation of the eyes occurs only during late juvenile development. In Rhinomugil and Anableps, restructuring of the skull and eye occurs during similar developmental phases suggesting that the development of the skull shape is widely conserved and cannot easily be changed during larval development.

References

Amorim P, Costa W . Multigene phylogeny supports diversification of four-eyed fishes and one-sided livebearers (Cyprinodontiformes: Anablepidae) related to major South American geological events. PLoS One. 2018; 13(6):e0199201. PMC: 6005514. DOI: 10.1371/journal.pone.0199201. View

Cronin T, Shashar N, Caldwell R, Marshall J, Cheroske A, Chiou T . Polarization vision and its role in biological signaling. Integr Comp Biol. 2011; 43(4):549-58. DOI: 10.1093/icb/43.4.549. View

Easter Jr S . Retinal growth in foveated teleosts: nasotemporal asymmetry keeps the fovea in temporal retina. J Neurosci. 1992; 12(6):2381-92. PMC: 6575912. View

Schwab I, Ho V, Roth A, Blankenship T, FitzGerald P . Evolutionary attempts at 4 eyes in vertebrates. Trans Am Ophthalmol Soc. 2002; 99:145-56; discussion 156-7. PMC: 1359005. View

Adriaens D, Verraes W . Ontogeny of the osteocranium in the African catfish, Clarias gariepinus Burchell (1822) (Siluriformes: Clariidae): Ossification sequence as a response to functional demands. J Morphol. 2018; 235(3):183-237. DOI: 10.1002/(SICI)1097-4687(199803)235:3<183::AID-JMOR2>3.0.CO;2-8. View

Langille R, Hall B . Development of the head skeleton of the Japanese medaka, Oryzias latipes (Teleostei). J Morphol. 2018; 193(2):135-158. DOI: 10.1002/jmor.1051930203. View

Baylor E . Air and water vision of the Atlantic flying fish, Cypselurus heterurus. Nature. 1967; 214(5085):307-9. DOI: 10.1038/214307a0. View

Simmich J, Temple S, Collin S . A fish eye out of water: epithelial surface projections on aerial and aquatic corneas of the 'four-eyed fish' Anableps anableps. Clin Exp Optom. 2012; 95(2):140-5. DOI: 10.1111/j.1444-0938.2011.00701.x. View

Owens G, Rennison D, Allison W, Taylor J . In the four-eyed fish (Anableps anableps), the regions of the retina exposed to aquatic and aerial light do not express the same set of opsin genes. Biol Lett. 2011; 8(1):86-9. PMC: 3259961. DOI: 10.1098/rsbl.2011.0582. View

Sivak J . The accommodative significance of the "ramp" retina of the eye of the stingray. Vision Res. 1976; 16(9):945-50. DOI: 10.1016/0042-6989(76)90225-x. View

10.

Easter Jr S, Johns P, Baumann L . Growth of the adult goldfish eye--I: Optics. Vision Res. 1977; 17(3):469-77. DOI: 10.1016/0042-6989(77)90041-4. View

11.

Cronin T, Marshall J . Patterns and properties of polarized light in air and water. Philos Trans R Soc Lond B Biol Sci. 2011; 366(1565):619-26. PMC: 3049010. DOI: 10.1098/rstb.2010.0201. View

12.

Morris S, Gaudin A . Osteocranial development in the viviparous surfperch Amphistichus argenteus (pisces: Embiotocidae). J Morphol. 2018; 174(1):95-120. DOI: 10.1002/jmor.1051740108. View

13.

Higgs , Fuiman . Ontogeny of visual and mechanosensory structure and function in Atlantic menhaden Brevoortia tyrannus. J Exp Biol. 1996; 199(Pt 12):2619-29. DOI: 10.1242/jeb.199.12.2619. View

14.

Aiello B, Bhamla M, Gau J, Morris J, Bomar K, da Cunha S . The origin of blinking in both mudskippers and tetrapods is linked to life on land. Proc Natl Acad Sci U S A. 2023; 120(18):e2220404120. PMC: 10160996. DOI: 10.1073/pnas.2220404120. View

15.

Natchev N, Tzankov N, Werneburg I, Heiss E . Feeding behaviour in a 'basal' tortoise provides insights on the transitional feeding mode at the dawn of modern land turtle evolution. PeerJ. 2015; 3:e1172. PMC: 4558077. DOI: 10.7717/peerj.1172. View

15.

Bennett H, WYRICK A, Lee S, McNEIL J . Science and art in preparing tissues embedded in plastic for light microscopy, with special reference to glycol methacrylate, glass knives and simple stains. Stain Technol. 1976; 51(2):71-97. DOI: 10.3109/10520297609116677. View

16.

Schwassmann H, Kruger L . Experimental analysis of the visual system of the four-eyed fish Anableps microlepis. Vision Res. 1966; 5(5):269-81. DOI: 10.1016/0042-6989(65)90004-0. View

17.

Sivak J . Optics of the eye of the "four-eyed fish" (Anableps anableps). Vision Res. 1976; 16(5):531-4. DOI: 10.1016/0042-6989(76)90035-3. View

18.

Pankhurst P, Pankhurst N, Montgomery J . Comparison of behavioural and morphological measures of visual acuity during ontogeny in a teleost fish, Forsterygion varium, tripterygiidae (Forster, 1801). Brain Behav Evol. 1993; 42(3):178-88. DOI: 10.1159/000114151. View