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Convergent Evolution of the Cavefish Astyanax (Characidae, Teleostei)

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Convergent Evolution of the Cavefish Astyanax (Characidae, Teleostei) Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066 The Linnean Society of London, 2003? 2003 80? 545554 Original Article CONVERGENCE OF ASTYANAX CAVEFISH EVOLUTION Biological Journal of the Linnean Society, 2003, 80, 545–554. With 6 figures H. WILKENS and U. STRECKER Convergent evolution of the cavefish Astyanax (Characidae, Teleostei): genetic evidence from reduced eye-size and pigmentation HORST WILKENS* and ULRIKE STRECKER Downloaded from https://academic.oup.com/biolinnean/article/80/4/545/2636155 by guest on 29 September 2021 Zoological Institute and Zoological Museum, University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany Received 7 June 2002; accepted for publication 7 March 2003 More than 20 populations of the cave-dwelling characid Astyanax occur within a restricted karst area in Mexico. The fish possess reduced eyes without lenses and visual cells. It is still an open question as to whether this condition evolved convergently after multiple entries of the surface ancestor into the different caves or whether a single cave ancestor, already characterized by reduced eyes, spread secondarily within them. In the crosses between specific pop- ulations, specimens appear that deviate considerably from those of the parents. They possess larger and better-devel- oped eyes with histologically intact lenses and visual cells; they thus have the structural potential for vision. This indicates that in different cave populations, different mutations in the eye gene system have occurred. In cases where these non-functional rudimentary genes are recombined in hybrid specimens, gene expression may be restored. This is the result of separate evolution of several Astyanax cave populations. © 2003 The Linnean Society of London, Bio- logical Journal of the Linnean Society, 2003, 80, 545-554. ADDITIONAL KEYWORDS: Anoptichthys - blindness - crossing experiments - melanophore - mutation pressure - relaxed selection - retina - rudimentation - speciation - troglobite. INTRODUCTION south. These forms (some of which are described as belonging to a separate genus Anoptichthys) are char- Life in continuous darkness, as exhibited by cave liv- acterized by different degrees of rudimentation of ing animals, has stimulated the thinking of biologists eyes and pigmentation. Three populations show an in many ways (Wilkens, Culver & Humphreys, 2000); intermediate stage of reduction, while more than 20 the reduction of biologically functionless traits such as others exhibit an extreme stage (Mitchell, Russell & eyes and pigmentation has been of particular interest. Elliott, 1977). All are closely related to a fully eyed Analysis of the genetic basis of eye and pigment and pigmented fish common in Mexican surface regression provides insight into the process of adapta- waters, and are interfertile with each other as well as tion. Information is obtained as to whether reduction with the surface form (Wilkens, 1988; Culver & Wilk- in eye-size (and regressive evolution in general) is a ens, 2000). constructive process driven by selection or whether it Troglobitic faunas may speciate in two ways. First, a relies on the accumulation of random mutations single, widespread ancestral surface species may (Kosswig, 1960; for a review see Culver & Wilkens, simultaneously invade separate karst or cave systems 2000). by multiple entries. The adaptations to darkness in In north-eastern Mexico, a series of cave popu- this case would be by convergence. Second, a species lations of the characid Astyanax fasciatus already adapted to a subterranean environment may (= A. mexicanus) occurs within a geographically small multiply within it (Holsinger, 2000). The question as karst limestone area, extending about 150 km north– to whether there was a single or multiple invasion by the different Astyanax cave populations is still *Corresponding author. E-mail: disputed (Wilkens, 1971; Avise & Selander, 1972; [email protected] Mitchell et al., 1977; Espinasa & Borowsky, 2001; © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 545–554 545 546 H. WILKENS and U. STRECKER Dowling, Martasian & Jeffery, 2002; Strecker, Ber- RESULTS natchez & Wilkens, 2003). We investigated these issues by crossing fish from JUVENILE EYEBALL SIZE IN THE CAVE FISH AND THEIR populations with extreme eye and pigment reduction CROSSINGS from all over the distribution area: the northernmost Measurement of eyeball size in juveniles (2.5 cm SL) population from Sótano de el Molino (Sierra de Gua- of the various populations revealed differences. It was temala), a more central population from Cueva de El smallest in Piedras, Yerbaniz and Curva and largest in Pachón and southern populations from Sótano de Yer- Molino (which has a distribution range separate from baniz, Sótano de las Piedras and Cueva de la Curva, all the other forms). Pachón overlapped with Molino all of which occur in the Sierra de El Abra (Fig. 1). The and Curva (Figs 2, 3). genetic basis of reduced eye-size and pigmentation in Size in the F1 and F2 crosses fell into two groups. The first contained the crosses of Molino with Pachón, the different populations was analysed by studying Downloaded from https://academic.oup.com/biolinnean/article/80/4/545/2636155 by guest on 29 September 2021 eye-size, histology and melanophore density in the Piedras, Yerbaniz and Curva, in which size surpassed hybrid offspring. The results will contribute to the dis- that of the parental generation (Fig. 2). In F2 the vari- cussion as to whether, or to what degree, these evolu- ability was also considerably increased, with smaller tionary processes derive from convergence. eyed parental forms and sizes in offspring which sur- passed even those of Molino. The percentage of large eyes varied: highest in the crosses with Pachón (27% MATERIAL AND METHODS larger than F1), lowest in those with Piedras (8.7%), Curva (8%) and Yerbaniz (10%). The size range was POPULATIONS STUDIED 0.6–1.3 mm in crosses with Piedras and Yerbaniz and The eyed fish were caught in a surface creek draining 0.5–1.5 mm in crosses with Pachón and Curva. into the Micos Cave (Cueva del Río Subtérraneo). The In the second group (the El Abra group) formed by fish from El Sótano de El Molino (1), La Cueva de El crosses between Pachón, Piedras, Yerbaniz and Curva, Pachón (2), El Sótano de Yerbaniz (3), El Sótano de las the size ranges of both F1 and F2 did not surpass those Piedras (4) and La Cueva de la Curva (5) (nomencla- of the parental forms. The values were intermediate ture according to Mitchell et al., 1977) were offspring where the parental eyes were of different sizes; other- of previously caught specimens (2–4 caught in 1971, 1 wise they were similar or even smaller (Fig. 3). and 5 caught in the 1990s by Borowsky (New York Distributions in F1 and F2 crosses of Molino with University)). All were maintained and bred under day- the eyed surface fish corresponded to earlier findings light conditions at 24∞C. in crosses of cave fish with the epigean form (Wilkens, 1988), with mean eye-sizes nearly intermediate between them. The range of the F2 crosses was larger EYES than that of F1 and lay between the parental forms. The horizontal diameter of the enucleated eyeball was The backcross with Molino ranged between F1 and measured in juvenile fish (preservation in 4% formal- Molino. dehyde, 2.5 cm SL, 1 MU = 0.25 mm) with a dissection microscope. For histological analysis, paraffin embed- ded slides of adult specimens were prepared and EYE HISTOLOGY IN ADULT FISH stained in Pasini dye. Adult eye-size was measured in Cave fish these slides. The rudimentary eyes of adult Curva, Piedras and Yerbaniz fish are histologically comparable to those of Pachón and Sabinos (Wilkens, 1970, 1988) and char- MELANOPHORE PATTERN acterized by a variable degree of differentiation. The The total number of melanophores was counted within best developed contain retinal rudiments consisting of an area of 1.77 mm2 from a region in front of the ganglion cell, inner nuclear and inner plexiform layers dorsal fin using a microscope (magnification 35¥). For as well as vitreous bodies, whereas retinal tissue in this purpose the specimens (2.5 cm SL) were narco- the less well developed is not layered and may be tized and adrenalin (L-Noradrenalin, 1 : 1000 in NaCl almost completely reduced. Rudiments of visual cells solution) was distributed in the area with a thin (outer plexiform and nuclear layers, outer segments) pipette. Adrenalin induces a physiological colour never occur in adult specimens. The anterior eye change and the melanophores contract within a few chamber is filled with a derivative of the ligamentum minutes. The fish were kept and bred over black annulare, the spongiosum; the lens and pupil do not underlay to provide equal environmental conditions exist (Wilkens, 1970, 1988). influencing the number of melanophores (morpholog- The Molino fish have similar histological character- ical colour change). istics of eye reduction (Wilkens, 1988). However, © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 545–554 CONVERGENCE OF ASTYANAX CAVEFISH EVOLUTION 547 GUATE SIERRA DE MALA Rio Sa Molino bin as R io F Cabollo Moro r io Downloaded from https://academic.oup.com/biolinnean/article/80/4/545/2636155 by guest on 29 September 2021 Arroyo Lagarto CIUDAD MANTE RioMante Pachon Mexic SIERRA DE EL o R io M e s i LEGEND l l a s ABRA Blind fish cave SIERRA DE Blind fish cave studied Rio River Road Yerbaniz
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