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WIREs Dev Biol
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Annual fish: developmental adaptations for an extreme environment

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Annual fish are freshwater teleosts found in South America and Africa that are exposed to an extremely variable environment. They develop and reproduce in seasonal ponds that dry during the summer eliminating the entire adult population. Remarkably, desiccation‐resistant embryos survive in these dry ponds that hatch during the next rainy season when the ponds are recreated. Among vertebrates, they represent one of the most remarkable extremophiles. They share several features with other fish models; however, they exhibit unique traits related to their peculiar life cycle. Epiboly is temporally and spatially uncoupled from organogenesis, and the embryos can undergo reversible developmental arrests (diapauses). These attributes make them a useful model to study diverse topics in developmental biology using a comparative and evolutionary approach. In this article, different aspects related to annual fish biology, taxonomy and phylogenetic considerations, reproductive strategy, and developmental characteristics with special focus on arrests, are summarized. The current challenge is to document and determine the factors that generate such high diversity and unique adaptations of annual fish. To understand this complexity, interdisciplinary approaches are being employed taking into consideration evolutionary biology, ethology, reproductive strategies, regulation of developmental mechanisms, and senescence. WIREs Dev Biol 2012, 1:595–602. doi: 10.1002/wdev.39

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  • Comparative Development and Evolution > Model Systems

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Figure 1.

Habitat (temporary pond) and biological cycle of annual fish. (a) From fall to the end of spring, the ponds are flooded and the adults reproduce. Austrolebias charrua male and female are shown. (b) During summer, the ponds are dry, the adults have died, and the embryos remain in the substrate in a pre‐hatching state of developmental arrest (diapause III). An embryo of the same species is shown.

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Figure 2.

Egg envelope ultrastructure (SEM) of two species of Austrolebias: (a) A. nigripinnis (b) A. charrua. The eggs show differences in envelope surface, filament shape, and pattern of distribution.

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Figure 3.

Early Austrolebias development. (a) One‐cell stage embryo. (b) Thirty‐two‐ to sixty‐four‐cell stage. (c) Blastula. Special stages during early annual fish development: (d) early dispersion stage geometric‐shaped blastomeres (white arrows) are observed over the lipid drop, progressively separating each other; (e) reaggregation stage the round blastomeres, smaller than at the previous stage, are joining in the middle of the picture (black arrows). (f) Early somite embryo. B, blastomere; DB, deep blastomere; Op, optic vesicle; Ot: otic vesicle; PB, peripheral blastomere; Pn, pronucleus; Pv, perivitelline space; S, somites; Sc, segmentation cavity; Sl, syncytial layer; Y, yolk. (Images (a), (b), (c), and (f) were reprinted with permission from Ref 18 . Copyright 2005 John Wiley & Sons, Inc.)

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Figure 4.

Schematic representation of main developmental stages in annual fish. (a) One‐cell stage. (b) Thirty‐two‐ to sixty‐four‐cell stage. (c) Blastula. Arrow indicates movement direction. (d) Dispersed phase. (e) Early reaggregate (highlighted by square). DB, deep blastomere; ECL, enveloping cell layer; PB, peripheral blastomere; Pn, pronucleus; R, reaggregate; Sc, segmentation cavity; Sl, syncytial layer; Y, yolk. (Reprinted with permission from Ref 18 . Copyright 2005 John Wiley & Sons, Inc.)

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Figure 5.

Comparison between two teleost species: Austrolebias viarius (Ref 18) and Danio rerio (Ref 30). Stage duration indicates the end of each presented stage.

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