Pleiotropic functions of embryonic sonic hedgehog expression link jaw and taste bud amplification with eye loss during cavefish evolution

Abstract

This study addresses the role of sonic hedgehog (shh) in increasing oral pharyngeal constructive traits (jaws and taste buds) at the expense of eyes in the blind cavefish Astyanax mexicanus. In cavefish embryos, eye primordia degenerate under the influence of hyperactive Shh signaling. In concert, cavefish show amplified jaw size and taste bud numbers as part of an adaptive change in feeding behavior. To determine whether pleiotropic effects of hyperactive Shh signaling link these regressive and constructive traits, sonic hedgehog (shh) expression was compared during late development of the surface- (surface fish) and cave-dwelling forms of Astyanax. After an initial expansion along the midline of early embryos, shh was elevated in the oral pharyngeal region in cavefish and later was confined to taste buds. The results of shh inhibition and overexpression experiments indicate that Shh signaling has an important role in oral and taste bud development. Heat shock mediated activation of an injected shh transgene at specific times in development showed that taste bud amplification and eye degeneration are sensitive to shh overexpression during the same early developmental period, although taste buds are not formed until much later. Genetic crosses between cavefish and surface fish revealed an inverse relationship between eye size and jaw size/taste bud number, supporing the linkage between oral pharyngeal constructive traits and eye degeneration. The results suggest that hyperactive Shh signaling increases oral and taste bud amplification in cavefish and suggest that selection for constructive oral pharyngeal traits may be responsible for eye loss via pleiotropic function of the Shh signaling pathway.

Contrasting feeding habits of post-larval and adult Astyanax cavefish

“…Multiple morphological and behavioural attributes have been described to support this statement, such as a higher number of taste buds (Yamamoto et al 2009;Varatharasan et al 2009), higher chemosensory capabilities (Protas et al 2008;Bibliowicz et al 2013;Hinaux et al 2016), an enhanced number of cranial neuromasts (Yoshizawa et al 2012), modulation in early developmental signalling pathways influencing brain development and organization (Yamamoto et al 2004;Pottin et al 2011), and a behaviourally more efficient posture with respect to the substrate when bottom feeding (Schemmel 1980).…”

Complex Craniofacial Changes in Blind Cave-Dwelling Fish Are Mediated by Genetically Symmetric and Asymmetric Loci

“…As a consequence of invading the subterranean environment millions of years ago (Bradic et al 2012), cave-dwelling morphs have evolved a series of regressive (e.g., eye loss) and constructive (e.g., increased lateral line sensitivity) phenotypes (Wilkens 1971;Montgomery et al 2001;Jeffery 2009;Yoshizawa et al 2010Yoshizawa et al , 2012. Phenotypic loss is believed to arise through genetic drift (Wilkens 1988), direct selection (Klaus et al 2013), or indirect selection via linkage or pleiotropy (Yamamoto et al 2009); however, the evolutionary mechanism that drives regressive loss remains unclear (Gross 2012). Our natural model system enables us to investigate the extent to which evolutionary modifications of the craniofacial complex evolve as an indirect consequence of pleiotropy or close physical linkage between causative gene(s) mediating craniofacial traits and other regressive traits, such as eye loss.…”

Coevolutionary patterning of teeth and taste buds

“…There is tremendous variation in tooth and taste bud numbers among vertebrates. Among closely related species, this variation likely has ecological relevance (13). For example, in Lake Malawi cichlids, planktivores typically possess a small number of widely spaced teeth (14) with reduced taste bud counts on the oral jaws.…”