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Retinal differentiation in syngnathids: comparison in the developmental rate and acquisition of retinal structures in altricial and precocial fish species

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Abstract

The altricial–precocial spectrum describes the degree of morphological maturation of offspring at the moment of hatching. In fishes, precocial species develop all their structures at early stages of embryogenesis and larvae hatch at an advanced stage of development, while altricial species hatch at a less developed stage. The timing of retinal development also varies significantly between precocial and altricial fish species. Thus, retinal development is completed before hatching in precocial species. In contrast, a relatively simple retina is observed in altricial newborns and the acquisition of the adult retinal features extends until late in larval life. Therefore, retinal maturation at hatching could be considered as a morphological character to describe the developmental mode of fish newborns. Syngnathids fishes hatch with well-developed sensory systems, jaws, and feeding structures and, therefore, they are considered as precocial fish species. Using as a model the retina of two species of syngnathids (Syngnathus typhle and Hippocampus guttulatus), we describe the retinal maturity during different embryological stages and compare the results with previous studies in the retina of other altricial and precocial fish species. This will be done through a review of the pertinent literature, as well as by drawing on our own experience gathered through recent studies on fish retinogenesis. These differences in the maturity of the visual system have implications for the vision-based survival skills during the early life stages after hatching and for the overall ecology and fitness of the species.

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Abbreviations

ac:

Amacrine cells

bc:

Bipolar cells

gc:

Ganglion cells

CMZ:

Ciliary marginal zone

GCL:

Ganglion cell layer

hc:

Horizontal cells

INL:

Inner nuclear layer

IPL:

Inner plexiform layer

L:

Lens

NFL:

Nerve fiber layer

ON:

Optic nerve

ONH:

Optic nerve head

ONL:

Outer nuclear layer

OPL:

Outer plexiform layer

os:

Outer segment of photoreceptors

PE:

Pigmented epithelium

pr:

Photoreceptors

References

  1. Ali MA, Anctil M (1976) Retinas in fish: an atlas. In: Collin SP, Marshall JN (eds) Sensory processing in aquatic environments. Springer, EEUU, New York, pp 139–170

  2. Álvarez-Hernán G, Sánchez-Resino E, Hernández-Nuñez I, Marzal A, Rodríguez-León J, Martín-Partido G, Francisco-Morcillo J (2018) Retinal histogenesis in an altricial avian species, the zebra finch (Taeniopygia guttata, Vieillot 1817). J Anat 233(1):106–120

  3. Arenzana FJ, Arévalo R, Sánchez-González R, Clemente D, Aijón J, Porteros A (2006) Tyrosine hydroxylase immunoreactivity in the developing visual pathway of the zebrafish. Anat Embryol (Berl) 211(4):323–334

  4. Ballard WW, Mellinger J, Lechenault H (1993) A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool 267:318–336

  5. Balon EK (1979) Juvenilization process in phylogeny and the altricial to precocial forms in the ontogeny of fishes. Environ Biol Fish 4(3):193–198

  6. Balon EK (1981) Saltatory processes and altricial to precocial forms in the ontogeny of fishes. Am Zool 21(2):573–596

  7. Balon EK (1984) Reflections on some decisive events in the early life of fishes. Trans Am Fish Soc 113:178–185

  8. Balon EK (1986) Types of feeding in the ontogeny of fishes and the life-history model. Environ Biol Fish 16:11–24

  9. Bejarano-Escobar R, Blasco M, DeGrip WJ, Martín-Partido G, Francisco-Morcillo J (2009) Cell differentiation in the retina of an epibenthonic teleost, the Tench (Tinca tinca, Linneo 1758). Exp Eye Res 89(3):398–415

  10. Bejarano-Escobar R, Blasco M, DeGrip WJ, Oyola-Velasco JA, Martín-Partido G, Francisco-Morcillo J (2010) Eye development and retinal differentiation in an altricial fish species, the Senegalese sole (Solea senegalensis, Kaup 1858). J Exp Zool B Mol Dev Evol 314(7):580–605

  11. Bejarano-Escobar R, Holguín-Arevalo MS, Montero JA, Francisco-Morcillo J, Martín-Partido G (2011) Macrophage and microglia ontogeny in the mouse visual system can be traced by the expression of Cathepsins B and D. Dev Dyn 240(7):1841–1855

  12. Bejarano-Escobar R, Blasco M, Durán AC, Rodríguez C, Martín-Partido G, Francisco-Morcillo J (2012a) Retinal histogenesis and cell differentiation in an elasmobranch species, the small-spotted catshark Scyliorhinus canicula. J Anat 220(4):318–335

  13. Bejarano-Escobar R, Blasco M, Martín-Partido G, Francisco-Morcillo J (2012b) Light-induced degeneration and microglial response in the retina of an epibenthonic pigmented teleost: age-dependent photoreceptor susceptibility to cell death. J Exp Biol 215:3799–3812

  14. Bejarano-Escobar R, Blasco M, Durán AC, Martín-Partido G, Francisco-Morcillo J (2013) Chronotopographical distribution patterns of cell death and of lectin-positive macrophages/microglial cells during the visual system ontogeny of the small-spotted catshark Scyliorhinus canicula. J Anat 223(2):171–184

  15. Bejarano-Escobar R, Blasco M, Martín-Partido G, Francisco-Morcillo J (2014) Molecular characterization of cell types in the developing, mature, and regenerating fish retina. Rev Fish Biol Fish 24:127–158

  16. Bejarano-Escobar R, Álvarez-Hernán G, Morona R, González A, Martín-Partido G, Francisco-Morcillo J (2015) Expression and function of the LIM-homeodomain transcription factor Islet-1 in the developing and mature vertebrate retina. Exp Eye Res 138:22–31

  17. Blaxter J (1986) Development of sense organs and behavior of teleost larvae with special reference to feeding and predator avoidance. Trans Am Fish Soc 115:98–114

  18. Cañavate J, Zerolo R, Fernández-Díaz C (2006) Feeding and development of Senegal sole (Solea senegalensis) larvae reared in different photoperiods. Aquaculture 258(1–4):368–377

  19. Candal E, Anadón R, DeGrip WJ, Rodríguez-Moldes I (2005) Patterns of cell proliferation and cell death in the developing retina and optic tectum of the brown trout. Brain Res Dev Brain Res 154(1):101–119

  20. Candal E, Ferreiro-Galve S, Anadón R, Rodríguez-Moldes I (2008) Morphogenesis in the retina of a slow-developing teleost: emergence of the GABAergic system in relation to cell proliferation and differentiation. Brain Res 1194:21–27

  21. Chai B, Xie C, Wei Q, Chen X, Liu J (2006) The ontogeny of the retina of chinese sturgeon (Acipenser sinensis). J Appl Ichthyol 22(1):196–201

  22. Choo C, Liew H (2006) Morphological development and allometric growth patterns in the juvenile seahorse Hippocampus kuda. J Fish Biol 69:426–445

  23. Collin S, Collin H (1999) The foveal photoreceptor mosaic in the pipefish, Corythoichthyes paxtoni (Syngnathidae, Teleostei). Histol Histopathol 14:369–382

  24. Correia M, Palma J, Koldewey H, Andrade J (2014) The use of a non-invasive tool for capture-recapture studies on a seahorse Hippocampus guttulatus population. J Fish Biol 84:872–884

  25. de Almeida HM, Sousa RP, Bezerra DO, Olivindo RF, das Neves Diniz A, de Oliveira SC et al (2015) Greater rhea (Rhea americana) external morphology at different stages of embryonic and fetal development. Anim Reprod Sci 162:43–51

  26. De Villegas Miguel E, Doldán MJ, Paz-Andrade C, Anadón R (1997) Development of the eye in the turbot Psetta maxima (Teleostei) from hatching through metamorphosis. J Morphol 233:31–42

  27. Dhanya S, Rajagopal S, Ajmal Khan S, Balasubramanian T (2005) Embryonic development in alligator pipefish, Syngnathoides biaculeatus (Bloch, 1785). Curr Sci 88(1):178–181

  28. Doldán MJ, Prego B, de Miguel Villegas E (1999) Immunochemical localization of calretinin in the retina of the turbot (Psetta maxima) during development. J Comp Neurol 406(4):425–432

  29. Elshatory Y, Deng M, Xie X, Gan L (2007) Expression of the LIM-homeodomain protein Isl1 in the developing and mature mouse retina. J Comp Neurol 503:182–197

  30. Evans B, Browman H (2004) Variation in the development of the fish retina. Am Fish Soc Symp 40:145–166

  31. Falk-Peteresen I, Hansen T (2001) Organ differentiation in newly hatched common wolffish. J Fish Biol 59:1465–1482

  32. Ferreiro-Galve S, Candal E, Carrera I, Anadón R, Rodríguez-Moldes I (2008) Early development of GABAergic cells of the retina in sharks: an immunohistochemical study with GABA and GAD antibodies. J Chem Neuroanat 36(1):6–16

  33. Ferreiro-Galve S, Rodríguez-Moldes I, Anadón R, Candal E (2010a) Patterns of cell proliferation and rod photoreceptor differentiation in shark retinas. J Chem Neuroanat 39(1):1–14

  34. Ferreiro-Galve S, Rodríguez-Moldes I, Candal E (2010b) Calretinin immunoreactivity in the developing retina of sharks: comparison with cell proliferation and GABAergic system markers. Exp Eye Res 91(3):378–386

  35. Ferreiro-Galve S, Rodríguez-Moldes I, Candal E (2012) Pax6 expression during retinogenesis in sharks: comparison with markers of cell proliferation and neuronal differentiation. J Exp Zool B 318:91–108. https://doi.org/10.1002/jezb.21448

  36. Fischer AJ, Bosse JL, El-Hodiri HM (2014) Reprint of: the ciliary marginal zone (CMZ) in development and regeneration of the vertebrate eye. Exp Eye Res 123:115–120

  37. Fishelson L, Baranes A (1999) Ocular development in the oman shark, Iago omanensis (Triakidae), Gulf of Aqaba, Red Sea. Anat Rec 256(4):389–402

  38. Fleger-Balon C (1989) Direct and indirect development in fishes- examples of alternative life-history styles. In: Bruton MN (ed) Alternative life-history styles of animals. Persp Vertebrate Sci 6: 71–100

  39. Forsgren K, Lowe C (2006) The life history of weedy seadragons, Phyllopteryx taeniolatus (Teleostei: Syngnathidae). Mar Freshw Res 57:313–322

  40. Foster S, Vincent A (2004) Life history and ecology of seahorses: implications for conservation and management. J Fish Biol 65:1–61

  41. Gwak W, Tsusaki T, Tanaka M (2003) Nutritional condition, as evaluated by RNA/DNA ratios, of hatchery-reared Japanese flounder from hatch to release. Aquaculture 219(1–4):503–514

  42. Harahush B, Fischer A, Collin S (2007) Captive breeding and embryonic development of Chiloscyllium punctatum Muller and Henle, 1838 (Elasmobranchii: Hemiscyllidae). J Fish Biol 71:1007–1022

  43. Harahush BK, Hart NS, Green K, Collin SP (2009) Retinal neurogenesis and ontogenetic changes in the visual system of the brown banded bamboo shark, Chiloscyllium punctatum (Hemiscyllidae, Elasmobranchii). J Comp Neurol 513(1):83–97

  44. Helvik JV, Drivenes O, Harboe T, Seo HC (2001) Topography of different photoreceptor cell types in the larval retina of Atlantic halibut (Hippoglossus hippoglossus). J Exp Biol 204:2553–2559

  45. Hernández S, Lamilla J, Dupré E, Stotz W (2005) Embryonary development of the redspotted catshark Schroederichthys chilensis (Guichenot, 1848) (Chondrichthyes: Scyliorhinidae). Gayana 69(1):191–197

  46. Hora M, Joyeux J (2009) Closing the reproductive cycle: growth of the seahorse Hippocampus reidi (Teleostei, Syngnathidae) from birth to adulthood under experimental conditions. Aquaculture 292:37–41

  47. Hu M, Easter SS (1999) Retinal neurogenesis: the formation of the initial central patch of postmitotic cells. Dev Biol 207(2):309–321

  48. Iwamatsu T (2004) Stages of normal development in the medaka Oryzias latipes. Mech Dev 121(7–8):605–618

  49. Kimmel C, Ballard W, Kimmel S, Ullmann B, Schilling T (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203(3):253–310

  50. Kitambi SS, Malicki JJ (2008) Spatiotemporal features of neurogenesis in the retina of medaka, Oryzias latipes. Dev Dyn 237(12):3870–3881

  51. Köppl C, Futterer E, Nieder B, Sistermann R, Wagner H (2005) Embryonic and posthatching development of the barn owl (Tyto alba): reference data for age determination. Dev Dyn 233(4):1248–1260

  52. Kvenseth AM, Pittman K, Helvik JV (1996) Eye development in Atlantic halibut (Hippoglossus hippoglossus): Differentiation and development of the retina from yolk sac stages through metamorphosis. Can J Fish Aquat Sci 53:2524–2532

  53. Lee H, O’Brien K (2011) Morphological and behavioral limit of visual resolution in temperate (Hippocampus abdominalis) and tropical (Hippocampus taeniopterus) seahorses. Vis Neurosci 28:351–360

  54. Lipton A, Thangaraj M (2014) Courtship behaviour, brood characteristics and embryo development in three spotted seahorse, Hippocampus trimaculatus (Leach, 1814). Int Res J Biol Sci 3(1):6–10

  55. Matsuura R, Sawada Y, Ishibashi Y (2010) Development of visual cells in the Pacific bluefin tuna Thunnus orientalis. Fish Physiol Biochem 36:391–402

  56. Morrison C, Miyake T, Wright J (2001) Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces: Cichlidae). J Morphol 247:172–195

  57. Mosk V, Thomas N, Hart N, Partridge J, Beazley L, Shand J (2007) Spectral sensitivities of the seahorses Hippocampus subelongatus and Hippocampus barbouri and the pipefish Stigmatopora argus. Vis Neurosci 24:345–354

  58. Mukai Y, Tuzan A, Lim L, Wahid N, Sitti-Raehanah M, Senoo S (2008) Development of the sensory organs in larvae of African catfish Clarias gariepinus. J Fish Biol 73:1648–1661

  59. Mukai Y, Tuzan A, Shaleh S, Manjaji-Matsumoto B (2010) Development of sensory organs and changes of behavior in larvae of the sutchi catfish, Pangasianodon hypophthalmus. Fish Sci 76:921–930

  60. Murray JR, Varian-Ramos CW, Welch ZS, Saha MS (2013) Embryological staging of the Zebra Finch, Taeniopygia guttata. J Morphol 274(10):1090–1110

  61. Neave DA (1985) The dorsal light reactions of larval and metamorphosing flatfish. J Fish Biol 26:629–640

  62. Negishi K, Wagner HJ (1995) Differentiation of photoreceptors, glia, and neurons in the retina of the cichlid fish Aequidens pulcher; an immunocytochemical study. Brain Res Dev Brain Res 89(1):87–102

  63. Novelli B, Socorro J, Caballero M, Otero-Ferrer F, Segade-Botella A, Molina-Domínguez L (2015) Development of seahorse (Hippocampus reidi, Gisnburg 1933): histological and histochemical study. Fish Physiol Biochem 41:1233–1251

  64. Novelli B, Otero-Ferrer F, Socorro J, Caballero M, Segade-Botella A, Molina-Domínguez L (2017) Development of short-snouted seahorse (Hippocampus hippocampus L. 1758): osteological and morphological aspects. Fish Physiol Biochem 43(3):833–848

  65. Olea GB, Sandoval MT (2012) Embryonic development of Columba livia (Aves: Columbiformes) from an altricial-precocial perspective. Revista Colombiana de Ciencias Pecuarias 25:3–13

  66. Olea GB, Hernando AB, Lombardo DM (2016) Heterochronic events in the ontogeny of Columba livia, Coturnix coturnix, and Gallus gallus domesticus. Revista Colombiana de Ciencias Pecuarias 29:274–282

  67. Palma J, Stockdale J, Correia M, Andrade J (2008) Growth and survival of adult long snout seahorse (Hippocampus guttulatus) using frozen diets. Aquaculture 278:55–59

  68. Pavón-Muñoz T, Bejarano-Escobar R, Blasco M, Martín-Partido G, Francisco-Morcillo J (2016) Retinal development in the gilthead seabream Sparus aurata. J Fish Biol 88(2):492–507

  69. Rapaport DH, Wong LL, Wood ED, Yasumura D, LaVail MM (2004) Timing and topography of cell genesis in the rat retina. J Comp Neurol 474(2):304–324

  70. Sánchez-Farías N, Candal E (2015) Doublecortin is widely expressed in the developing and adult retina of sharks. Exp Eye Res 134:90–100

  71. Sánchez-Farías N, Candal E (2016) Identification of radial glia progenitors in the developing and adult retina of sharks. Front Neuroanat 10:65

  72. Scheiber IBR, Weiss BM, Kingma SA, Komdeur J (2017) The importance of the altricial-precocial spectrum for social complexity in mammals and birds—a review. Front Zool 14:3

  73. Schmitt EA, Dowling JE (1996) Comparison of topographical patterns of ganglion and photoreceptor cell differentiation in the retina of the zebrafish, Danio rerio. J Comp Neurol 371(2):222–234

  74. Senoo S, Ang K, Kawamura G (1994) Development of sense organs and mouth and feeding of reared marble goby Oxyeleotris marmoratus larvae. Fish Sci 60(4):361–368

  75. Silva K, Monteiro NM, Almada VC, Vieira MN (2005) Early life history of Syngnathus abaster. J Fish Biol 67:1–7

  76. Sommer S, Whittington CM, Wilson AB (2012) Standardised classification of pre-release development in male-brooding pipefish, seahorses, and seadragons (Family Syngnathidae). BMC Dev Biol 12:39

  77. Starck J, Ricklefs R (1998) Patterns of development: the altricial-precocial spectrum. In S. a. R. (eds) Avian growth and development. Oxford University Press, New York, pp 3–30

  78. Tanaka M, Kawai S, Seikai T, Burke JS (1996) Development of the digestive organ system in Japanese flounder in relation to metamorphosis and settlement. Mar Freshw Behav Physiol 28:19–31

  79. Tsai H, Chang M, Liu S, Abe G, Ota K (2013) Embryonic development of goldfish (Carassius auratus): a model for the study of evolutionary change in developmental mechanisms by artificial selection. Dev Dyn 242:1262–1283

  80. Van Wassenbergh S, Roos G, Genbrugge A, Leysen H, Aerts P, Adriaens D et al (2009) Suction is kid´s play: extremely fast suction in newborn seahorses. Biol Lett 5(2):1–4

  81. Vecino E, García-Briñón J, Velasco A, Caminos E, Lara J (1993) Calbindin D-28 K distribution in the retina of the developing trout (Salmo fario L.). Neurosci Lett 152:291–295

  82. Weruaga E, Velasco A, Briñón JG, Arévalo R, Aijón J, Alonso JR (2000) Distribution of the calcium-binding proteins parvalbumin, calbindin D-28 k and calretinin in the retina of two teleosts. J Chem Neuroanat 19:1–15

  83. Wetzel JT, Wourns JP (2004) Embryogenesis in the dwarf seahorse, Hippocampus zosterae (Syngnathidae). Gulf Caribb Res 16:27–35

  84. Yeo JY, Lee ES, Jeon CJ (2009) Parvalbumin-immunoreactive neurons in the inner nuclear layer of zebrafish retina. Exp Eye Res 88(3):553–560

  85. Young RW (1985a) Cell differentiation in the retina of the mouse. Anat Rec 212(2):199–205

  86. Young RW (1985b) Cell proliferation during postnatal development of the retina in the mouse. Brain Res 353(2):229–239

  87. Yúfera M, Parra G, Santiago R (1999) Growth, carbon, nitrogen and caloric content of Solea senegalensis (Pisces: Soleidae) from egg fertilization to metamorphosis. Mar Biol 134(1):43–49

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Acknowledgements

The authors express their gratitude to M.S. Holguín-Arévalo for her excellent technical assistance. Samples for this study were obtained under the frame of the research Projecto Hipposafe, funded by the Fundaçao para a Ciencia e a Tecnologia, Portugal (PTDC/MAR/122616/2010). This work was also supported by grants from the Spanish Ministerio de Ciencia y Tecnología (BFU2007-67540) and Junta de Extremadura (PRI06A195, GR15158).

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Correspondence to Javier Francisco-Morcillo.

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Animals included in the present study were treated according to the regulations and laws of the European Union (EU Directive 2010/63/EU) and Spain (Royal Decree 1386/2018). This article does not contain any studies with human participants performed by any of the authors.

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Álvarez-Hernán, G., Andrade, J.P., Escarabajal-Blázquez, L. et al. Retinal differentiation in syngnathids: comparison in the developmental rate and acquisition of retinal structures in altricial and precocial fish species. Zoomorphology 138, 371–385 (2019). https://doi.org/10.1007/s00435-019-00447-3

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Keywords

  • Altricial
  • Development
  • Fish
  • Hippocampus guttulatus
  • Precocial
  • Retina
  • Syngnathus typhle
  • Visual system