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Enhanced Prey Capture Skills in Astyanax Cavefish Larvae Are Independent from Eye Loss Luis Espinasa1, Jonathan Bibliowicz2, William R Jeffery3 and Sylvie Rétaux2*

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Enhanced Prey Capture Skills in Astyanax Cavefish Larvae Are Independent from Eye Loss Luis Espinasa1, Jonathan Bibliowicz2, William R Jeffery3 and Sylvie Rétaux2* Espinasa et al. EvoDevo 2014, 5:35 http://www.evodevojournal.com/content/5/1/35 RESEARCH Open Access Enhanced prey capture skills in Astyanax cavefish larvae are independent from eye loss Luis Espinasa1, Jonathan Bibliowicz2, William R Jeffery3 and Sylvie Rétaux2* Abstract Background: Enhanced food-finding efficiency is an obvious adaptive response to cave environments. Here, we have compared the food-finding abilities of Astyanax surface fish and blind cavefish young larvae in their first month of life, in the dark. Results: Our results show that enhanced prey capture skills of cavefish are already in effect in fry soon after the yolk is depleted and the young larvae must find food for themselves. Moreover, using prey capture competition assays on surface fish fry with lensectomies, we showed that eye-dependent developmental processes are not the main determinant for enhanced prey capture skills. Finally, using F2 hybrid larvae resulting from crosses between surface fish and cavefish, we found that reduced eyes do not confer a selective advantage for prey capture by fry in the dark. Conclusion: We discuss these data with regards to our current developmental and genetic understanding of cavefish morphological and behavioral evolution. Keywords: Astyanax, Lensectomy, Prey capture, Cavefish, Troglomorphy Background well fitted for laboratory research as surface fish and cavefish A significant modification in feeding skills could be an are inter-fertile as well as suitable for experimental manipu- evolutionary key to adapt to a new environment. Food lations [7,8]. In the literature it is often stated that the adult scarcity and/or the lack of visual cues in caves can act as cave morph is more efficient in finding food in darkness. strong selective agents. An enhanced food-finding effi- Specific modifications have been described to support this ciency is an obvious adaptive response to environments statement, such as a higher number of taste buds [9,10], that lack light and are often poor in food. For example, the higher chemosensory capabilities [11,12], an enhanced num- cave crayfish Orconectes inermis [1], the cave salamander ber of cranial neuromasts [13], modulation in early develop- Proteus anguineus [2], and the spring cavefish Chologaster mental signaling pathways influencing brain development Agassizi [3]haveahigherperformanceinpreydetection and organization [14,15], and a behaviorally more efficient and/or feeding success in the darkness when compared to posture with respect to the substrate when bottom feeding closely related surface species (discussed in [4]). [16]. However, increased food finding efficiency is to our The blind Mexican tetra Astyanax mexicanus is a knowledge supported by only three controlled observations model system in evolutionary developmental biology, or experiments in which cavefish directly outcompeted which has provided an unprecedented understanding of surface fish for a limited amount of food. the genetic and developmental controls of troglomorphic features. There are 30 known caves harboring Astyanax a) In the Hüppop [4] food-finding ability experiment, cavefish populations in México [5,6] and their closely six surface and six Pachón cavefish aged at least related surface-dwelling morph abound in nearby surface 1.5 years (adults) were put in the dark to compete streams and throughout most of Mexico. Astyanax is for single 10 mm3 pieces of beef-heart muscle, provided one at a time. About 80% of all food * Correspondence: [email protected] particles were found and eaten by cavefish. 2 Equipe Développement Evolution du Cerveau Antérieur, UPR3294 N&D, b) In the Yoshizawa et al. [17] prey capture CNRS, Institut Alfred Fessard, 91198 Gif-sur-Yvette, France Full list of author information is available at the end of the article competition assay, a pair of 2.5 to 4.0 cm long © 2014 Espinasa et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Espinasa et al. EvoDevo 2014, 5:35 Page 2 of 7 http://www.evodevojournal.com/content/5/1/35 surface fish and Pachón cavefish were put in the degenerate eyes. Likewise surface embryos on which len- dark and were provided with three drops of living sectomy had been performed also resulted in adults with Artemia larvae. Strikes at prey were recorded for degenerated eyes. The physical presence of an eye has an 1 min with an infrared camcorder. About 70% of all effect on the developmental structure of the skull and the strikes were performed by cavefish. position of the suborbital bones [22], and the number of c) In Wilkens and Hüppop [18], measurements of the the small mandibular teeth [23]. But the most intriguing population’s condition factor, that is, the relationship eye-dependent developmental effect is that the distance of body weight and body length as a measure of the between the nasal and antorbital bones is enlarged when nutritional state of a fish, were reported. In a few an eye is absent during development. Direct measure- caves the cavefish live associated with surface fish, ments of the size of the olfactory pits confirmed that a which sometimes are washed into the cave by wider olfactory pit is present on eyeless cave fish and sur- flooding or by swimming upstream from springs. In face fish with a degenerate eye, and a narrower olfactory caves where food is abundant, such as in the Chica pit in eyed surface fish and cavefish with a restored eye. cave where the guano of a large bat colony is The width of the olfactory pit is modified by an average available, surface fish have a comparable condition 12.9% due to the eye-dependent developmental processes factor to the cavefish. On the contrary, in caves [22]. An enlarged olfactory pit could result in an enhanced where food is scarce, such as the Río Subterráneo sense of smell, which could directly correlate with feeding cave in the Micos area, surface fish washed into the skills of eyeless fish [12]. cave look undernourished, have very low condition In recent years, much of the evolutionary developmental factor, and seem to be unable to compete with the studies in Astyanax have been conducted in young fish. local cave fish. The authors of the current paper Results show that drastic changes with significant mor- have personally corroborated this observation and phological and physiological outcomes occur within the witnessed in multiple trips to this cave that in the first days after fertilization. The first objective of this paper first pool of the Río Subterráneo cave, surface fish is to describe a technique for assessing feeding skills after are thin, and often appear to be dying or are already the yolk has just disappeared and the young larvae must dead. In contrast, troglomorphic fish swimming in find food for themselves. The second objective is to estab- the same pool are well nourished. lish if the eye-dependent developmental processes by themselves are enough to account for the improved feed- A related feeding competition experiment was carried ing skills in Astyanax cavefish larvae. The final objective is out by Sadoglu [19], but in this case the possibility of to replicate Sadoglu’s experiment of decoupling the select- coupling between the selective value of the eye loss and ive value of the eye loss from other troglomorphic features other troglomorphic features was studied using the F2 by using F2 progeny, but under reduced food conditions progeny of a Pachón cavefish and surface fish cross to seg- that would foster high selective competition for prey regate the eyeless phenotype from other characters. For capture skills. this experiment, 208 F2 larvae were put in dark or in light conditions and were given large amounts of Artemia lar- Methods vae during the first month, complemented with dried food Specimens starting on week 2. After 3 months and 33% mortality, the Astyanax mexicanus surface and Pachón cavefish were surviving fish were classified according to eye morph- obtained from the Jeffery lab (University of Maryland, ology. Results showed that eye phenotypes (eye size) were College Park, MD, USA) in 2004. Since then they have statistically the same in both environments. Sadoglu con- been maintained at the CNRS facility at Gif sur Yvette, cluded that ‘in mixed populations where interactions of France. Surface fish had initially been collected in San phenotypes exist and where there is abundant food, eye Solomon Spring, Balmorhea State Park, Texas, and the type seems not to be selected: Survival value of each type cavefish from Pachón cave, in Mexico. Spawning was in- is the same… we do not know what would be the result if duced as in [24]. The spawn of cave and surface fish was the experiments were repeated under reduced food kept in 90 mm Petri dishes in an incubator at 23°C in ‘blue -1 -1 -1 conditions’. water’ (1 g.L NaCl, 30 mg.L KCl, 40 mg.L CaCl2, -1 Eye degeneration in Astyanax is triggered by lens apop- 160 mg.L MgSO4, and trace of methylene blue as anti- tosis [20,21]. Using tissue transplantation, Yamamoto and infectious agent) changed daily [8]. They were divided into Jeffery [21] reversed the loss of eyes in Astyanax cavefish. four groups: cavefish in a 14:10 hour light/dark cycle, sur- Surface fish lens vesicles were transplanted into cavefish face fish in a 14:10 hour light/dark cycle, surface fish embryonic optic cups, inducing the development of large under constant darkness, and surface fish which had eyes.
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