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WIREs Dev Biol
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Evolution and development in cave animals: from fish to crustaceans

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Cave animals are excellent models to study the general principles of evolution as well as the mechanisms of adaptation to a novel environment: the perpetual darkness of caves. In this article, two of the major model systems used to study the evolution and development (evo–devo) of cave animals are described: the teleost fish Astyanax mexicanus and the isopod crustacean Asellus aquaticus. The ways in which these animals match the major attributes expected of an evo–devo cave animal model system are described. For both species, we enumerate the regressive and constructive troglomorphic traits that have evolved during their adaptation to cave life, the developmental and genetic basis of these traits, the possible evolutionary forces responsible for them, and potential new areas in which these model systems could be used for further exploration of the evolution of cave animals. Furthermore, we compare the two model cave animals to investigate the mechanisms of troglomorphic evolution. Finally, we propose a few other cave animal systems that would be suitable for development as additional models to obtain a more comprehensive understanding of the developmental and genetic mechanisms involved in troglomorphic evolution. WIREs Dev Biol 2012. doi: 10.1002/wdev.61

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Figure 1.

Requirements of an evo–devo cave system. In red are genetic requirements, in blue developmental requirements, and in green requirements for functional analysis. (a) The cavefish Astyanax mexicanus. (b) The isopod crustacean Asellus aquaticus. Boxes filled with the appropriate color indicate that the above tool is present for the particular species. An empty box indicates that the tool has not yet been generated for the species. (Reprinted with permission from Ref 4. Copyright 2011 National Academy of Sciences)

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Figure 2.

Eye development in Astyanax mexicanus surface fish and cavefish. (a and b) Surface fish (a) and cavefish (b) eye primordia viewed laterally at 1 day post‐fertilization (dpf) showing the small lens (L) and reduced ventral optic cup (OC) in the latter. (Reprinted with permission from Ref 50. Copyright 2004 Nature Publishing Group). (c and d) Section through surface fish (c) and cavefish (d) eye primordia at 1.5 dpf showing apoptotic cells (brown color) detected by the terminal deoxynucleotidyl transferase (TUNEL) assay in the lens and retina in cavefish but not surface fish. (Reprinted with permission from Ref 48. Copyright 2007 Elsevier Limited). (e and f) Sections through surface fish (e) and cavefish (f) eyes at 10 dpf showing dividing cells in the ciliary marginal zone (CMZ) stained with anti‐proliferating cell nuclear antigen (PCNA) (brown color). (Reprinted with permission from Ref 51. Copyright 2002 University of the Basque Country Press). (g–j) Diagram showing OC morphogenesis in surface fish (g and i) and cavefish (h and j). OV, optic vesicle; OS, optic stalk. Black and gray areas represent OC and OS domains, respectively. (Reprinted with permission from Ref 52. Copyright 2003 Oxford University Press). (k) Diagram comparing eye development and growth in surface fish (top) with eye degeneration in cavefish (bottom). (Reprinted with permission from Ref 34. Copyright 2009 Annual Reviews)

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Figure 3.

Role of the lens and shh expression in Astyanax mexicanus eye degeneration. Left columns. Rescue of the cavefish eye by lens transplantation. (a) Diagram showing transplantation of a surface fish embryonic lens to a cavefish embryo (top) and a cavefish embryonic lens to a surface fish embryo (bottom). The host lenses were removed prior to transplantation. (b and c) Dissected eyes from an adult cavefish that received a surface fish lens transplant on one side as an embryo. (b) Transplant side. (c) Control side. (d and e) Dissected eyes from an adult surface fish that received a cavefish lens on one side as an embryo. (d) Transplant side. (e) Control side. Photos (b)–(e) courtesy of Yoshiyuki Yamamoto. Right columns. Role of Shh in cavefish eye degeneration. (f and g). Diagram showing expanded shhA gene expression along the embryonic midline (blue) and inhibitory effects (yellow blocked lines) on pax6 expression (red) in the optic domain of the neural plate in surface fish. (h and i) Four‐gene in situ hybridization showing expanded shhA expression at the cavefish (h) midline (blue) and corresponding reduction of pax6 expression relative to surface fish (i) at the neural plate stage. No changes were seen in pax2a (blue) or dlx3 (red) gene expression. (j and k) In situ hybridization showing expanded shhA expression in the cavefish (j) compared to surface fish (k) rostrum. (l and m) Overexpression of shhA causes lens apoptosis (l, arrow) and eye degeneration (m) in surface fish. (Reprinted with permission from Ref 50. Copyright 2004 Nature Publishing Group)

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Figure 4.

Astyanax mexicanus genetic map showing locations of quantitative trait loci (QTL) and candidate genes. Shown is a linkage map generated from a Pachón F2 cross.28 QTL are shown for eye size, lens size (Lens E, L), melanophore number (Mel A, D, E, L) in four different places on the body, and number of tastebuds (Tbuds). QTL with more precise locations are shown in red. The location of a rib QTL from Ref 28 is also shown. Candidate genes are shown in blue. Candidate genes with red tick marks were mapped in Ref 28. Candidate genes without red tick marks were mapped in a different analysis64 and are shown next to the most closely linked marker in common between the two analyses. (Reprinted with permission from Ref 28. Copyright 2007 Elsevier Limited)

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Figure 5.

Pigmentation in Astyanax mexicanus. (a) Tyrosinase positive cells in a Pachón cavefish embryo at 72 hpf. (b–e′) F2 animals from a cross between a surface and a Pachón cave individual. (b–e) Side views of each fish head. (b′–e′) Higher magnification of (b–e). Genotypes of each individual are written in (b′–e′) for both mc1r and oca2. (f) Table describing certain cave populations of A. mexicanus: whether the albino and/or brown phenotypes are present, what genes are responsible, and what mutations are responsible. nt, nucleotide. ‘Mc1r?’ or ‘Oca2?’ shows that complementation tests indicate that the particular gene is involved but no coding mutation has been observed. (b–e′) from Gross et al.64 (f) Summarizing results in Gross et al.64 Protas et al.30 and Wilkens and Strecker.80

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Figure 6.

Constructive traits in Astyanax mexicanus cavefish. (a and b) Superficial neuromast number and diameter (insets) is increased in cavefish relative to surface fish (a). (Reprinted with permission from Ref 88. Copyright 2010 Elsevier Limited). (c) Differences in feeding posture behavior in surface fish and cavefish. (Reprinted with permission from Ref 90. Copyright 2005 Oxford University Press). (d–g) Cavefish embryos (e) have a larger mouth (o) than surface fish (d). The mouth is encircled by shhA expression (d and e). Later in development (f and g), shhA expression is attenuated to tooth germs (downward arrowheads) and developing taste buds (upward arrowheads). (h–k) Cavefish larvae (i) show increased jaw span (double headed arrows) and anti‐calretinin‐stained taste buds (arrowheads) on their lips (k) relative to surface fish (h and j). (l and m) Overexpression of shhA by mRNA injection into cavefish embryos causes the formation of a large gaping mouth with excessive taste bud development. (l) Surface fish control and (m) shhA‐injected cavefish. (n and o) Conditional heat shock shhA overexpression at the tailbud stage (n) but not at 1 dpf (o) induces eye degeneration, forebrain enlargement, and a larger mouth with more taste buds (not shown) in surface fish larvae. (Reprinted with permission from Ref 91. Copyright 2009 Elsevier Limited)

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Figure 7.

Cave arthropods. (a) The crustacean, Monolistra monstruosa, photo courtesy of Helena Bilandžija. (b) The spider, Travunia jandai and the isopod crustacean, Aegonethes cervinus, photo courtesy of Helena Bilandžija. (c) The beetle, Ptomaphagus hirtus, photo courtesy of Markus Friedrich. (d) The crustacean, Gammarus minus, photo courtesy of Dan Fong. (e) The beetle, Leptodirus hochenwartii, photo courtesy of Helena Bilandžija. (f) The collembolan, Verhoeffiella longicornis, photo courtesy of Marko Lukić. (g) The spider, Sulcia nocturna, photo courtesy of Martina Pavlek. (h) The millipede, Brachidesmus sp., photo courtesy of Helena Bilandžija.

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Figure 8.

Different cave and surface populations of Asellus aquaticus. (a) Map of cave and surface populations of A. aquaticus. (Reprinted with permission from Ref 17. Copyright 2010 John Wiley and Sons). (b) Drawings of eye rudiments from individuals from the Planina cave population. Pairs of eye rudiments depict right and left sides from the same individual. (Reprinted with permission from Ref 105. Copyright 1965 Guy Demortier). (c–f) Drawings of individuals from (c) Planina cave in Slovenia, (d) Planina polje (surface water) in Slovenia, (e) Mangalia well in Romania, and (f) Bucharest, Romania surface waters. Note differences in length of appendages and numbers of setae. P, pereopod (thoracic leg) and A, antennae. (Reprinted with permission from Ref 104. Copyright 1996 Springer)

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Figure 9.

Quantitative trait loci (QTL) map, phenotypes, and mapped loci in a backcross of cave and surface Asellus aquaticus. (a) Surface head, arrows pointing to the eyes. Scale bar = 0.25 mm. (b) Cave head, arrows pointing to the eyes. (c–f) Four different eye colors present in the backcross offspring. (g) Surface eye. Scale bar = 0.125 mm. (h–j) Representative eye phenotypes in the backcross offspring. (k) Linkage map with eight linkage groups. Distance in centimorgans is on the left side of the linkage group and marker name is on the right side of the linkage group. Mapped locations of various QTL and loci for eye and pigment traits. The length of the black bar represents the 1.5 logarithm (base 10) of odds (LOD) interval of the QTL or locus. (Reprinted with permission from Ref 4. Copyright 2011 National Academy of Sciences)

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Figure 10.

Embryonic development in the surface form of Asellus aquaticus. (a) Lateral view of an embryo at 40% of development. h, head; y, yolk. The dotted line shows the separation between the head and the posterior. (b) Lateral view of an embryo at 60% of development. (b′). Dorsal view of the same embryo. lo, lateral organs; at, antenna. (c) Lateral view of an embryo at 70% of development. (d) Dorsal view of an embryo at 90% of development, just before hatching. e, eye. (Reprinted with permission from Ref 111. Copyright 2010 Staatliches Museum für Naturkunde Stuttgart)

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Figure 11.

Differences in albinism between Astyanax mexicanus and Asellus aquaticus. (a) Three different cavefish populations: Molino, Pachón, and Japones have an albino phenotype and the causative gene appears to be oca2. (In Japonés, the actual mutation has not been mapped—the evidence for oca2 as the responsible gene is by complementation test).30 (b) In A. aquaticus, only one cave population has been examined but there are two different methods observed to cause albinism; either a single locus or mutations at two different loci.4

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