Emerging model systems in evo-devo: cavefish and microevolution of development

Abstract

Cavefish and their conspecific surface-dwelling ancestors (Astyanax mexicanus) are emerging as a model system to study the microevolution of development. Here we describe attributes that make this system highly promising for such studies. We review how the Astyanax system is being used to understand evolutionary forces underlying loss of eyes and pigmentation in cavefish. Pigment regression is probably explained by neutral mutations, whereas natural selection is a likely mechanism for loss of eyes. Finally, we discuss several research frontiers in which Astyanax is poised to make significant contributions in the future: evolution of constructive traits, the craniofacial skeleton, the central nervous system, and behavior.

Fig. 1

(A) Astyanax surface fish and some of the different cavefish populations (letters in orange indicate the location of caves harboring these populations; see (B)). (B) Sketch map of the Sierra de El Abra region showing approximate location of caves harboring cavefish populations (orange- or pink-filled circles). Orange-filled circles with letters indicate cavefish populations maintained in the Jeffery laboratory cavefish colony (see (A)). The inset in (B) is an outline of Mexico showing the region of the large map in black and Guerrero in the orange rectangle. (C) Albinitic Pachó n cavefish embryo with melanin positive melanoblasts after L-DOPA supplementation. (D, E) Surface fish embryo with eye primordium (D), and adult with eye (E). (F, G) Pachó n cavefish embryo with small eye primordium showing a reduced ventral sector (F), and eyeless adult (G). (H–K) Cavefish embryos show expanded shhA expression along the midline and contracted pax6 expression in the eye fields. (H, I) Surface fish. (J, K) Pachó n cavefish. (H, J). Neural plate stage viewed dorsally. (I, K) Ten somite stage viewed rostrally. Markers (dlx3) indicate the border of the neural plate and (pax2) boundary of the future midbrain and hindbrain region in the neural plate. (L, M) Overexpression of shh induces lens apoptosis (L) and a blind cavefish phenocopy (M) in surface fish. (N) Transplantation of a lens from an embryonic surface fish into the optic cup of a Los Sabinos cavefish rescues eye development. (O, P) Sections through embryonic surface fish and Pachó n cavefish eye primordia showing apoptosis in the cavefish (P) but not the surface fish (O) lens. Arrows in (P) indicate the lens (L) and retina (R). (Q) Diagram showing effects of expanded Hh signaling in cavefish. (R) Comparison of brain morphology in surface fish and cavefish. Dorsal views with anterior on the left. (S) Differences in bottom feeding posture in surface fish and cavefish. (A) is reproduced from Jeffery et al. (2003) and Protas et al. (2007), (C) from McCauley et al. (2004), (D, F) from Yamamoto and Jeffery (2000), (H–M) from Yamamoto et al. (2004), N from Jeffery et al. (2003), (O, P) from Strickler et al. (2007a), (R) from Soares et al. (2004), and (S) from Jeffery (2005).

Fig. 2

Astyanax surface fish and cavefish craniofacial skeletons. Features that are changed are shown in black. N, nasal bones; MT, maxillary teeth. SO3: Fractured third suborbital bone. Op, operculum. Modified from Yamamoto et al. (2003).