Academic journal article Genetics

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

Academic journal article Genetics

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

Article excerpt

NATURAL model systems, such as Darwin's finches (Abzhanov et al. 2004, 2006; Mallarino et al. 2011) and African cichlid fishes (Albertson et al. 2003; Albertson and Kocher 2006; Streelman and Albertson 2006), provide living proof that the skull is remarkably labile over evolutionary time. Dramatic morphological changes accompany, or perhaps enable, expansion and exploitation of niches through rapid evolution of adaptive feeding modes (Anyonge and Baker 2006; Cooper et al. 2010). While a great deal is known regarding the developmental origin of cranial bones mediating these constructive changes (Smith 2006; Streelman et al. 2007; Jheon and Schneider 2009), little is known of the genetic basis for craniofacial changes that evolve in the absence of obvious selective pressures.

To explore this phenomenon, we examined alterations to the craniofacial skeleton of the freshwater fish Astyanax mexicanus. This species consists of an extant surface-dwelling form and multiple independently derived cave-dwelling forms (Strecker et al. 2003). 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. 2010, 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.

Among the most significant changes affecting the skull in cavefish are alterations to circumorbital bone morphology (Alvaréz 1946, 1947). These modifications demonstrate a spectrum of severity, comprising both bone fragmentation and fusion, much of which is endemic to each independent cavefish population (Mitchell et al. 1977). In surface-dwelling forms, each member of the circumorbital series is present as a single, intact bone (Mitchell et al. 1977). In contrast, fragmentation of the suborbital bones [particularly the first suborbital (SO1) and third suborbital (SO3) bones] has been reported for eight wild cavefish populations, including the Pachón cave (Mitchell et al. 1977). Classic studies, which were essentially descriptive accounts, assumed craniofacial changes in cavefish evolved as a secondary consequence of the loss of the eye.

Yamamoto et al. (2003) tested this hypothesis, using lentectomy and intermorphotype grafting to determine the extent to which craniofacial phenotypes were influenced by experimental removal of the eye. Certain traits were affected, including the distance between the nasal and antorbital bones, the inner sectors of the SO3 and supraorbital bones, and position of the SO3 bone relative to the orbit of the eye (Yamamoto et al. 2003). However, other craniofacial traits were not affected by eye loss, such as number of SO3 bony elements, positioning of SO4-6 bones relative to the opercular bone, and opercular bone shape (Yamamoto et al. 2003). Protas et al. (2008) first investigated the genetic basis for craniofacial defects in Astyanax by evaluating variation in SO3 width on the right side of the face only.

In this study, we searched for additional craniofacial traits demonstrating a genetic basis. We scored 33 phenotypes in a hybrid mapping pedigree derived from blind Pachón cave-dwelling and eyed surface-dwelling forms of A. mexicanus (Supporting Information, Table S1). Prior studies using the same pedigree revealed the genetic basis for a number of cave-associated phenotypes, including eye size reduction, pigmentation loss, and chemical sensitivity (Protas et al. …

Search by... Author
Show... All Results Primary Sources Peer-reviewed

Oops!

An unknown error has occurred. Please click the button below to reload the page. If the problem persists, please try again in a little while.