Wnt signalling underlies the evolution of new phenotypes and craniofacial variability in Lake Malawi cichlids

Abstract

Progress towards understanding adaptive radiations at the mechanistic level is still limited with regard to the proximate molecular factors that both promote and constrain evolution. Here we focus on the craniofacial skeleton and show that expanded Wnt/β-catenin signalling early in ontogeny is associated with the evolution of phenotypic novelty and ecological opportunity in Lake Malawi cichlids. We demonstrate that the mode of action of this molecular change is to effectively lock into place an early larval phenotype, likely through accelerated rates of bone deposition. However, we demonstrate further that this change toward phenotypic novelty may in turn constrain evolutionary potential through the corresponding reduction in craniofacial plasticity at later stages of ontogeny. In all, our data implicate the Wnt pathway as an important mediator of craniofacial form and offer new insights into how developmental systems can evolve to both promote and constrain evolutionary change.

Cichlid fishes as a model to understand normal and clinical craniofacial variation

“…For instance, sex hormones have drastic effects on embryonic facial patterning (Cohen, et al 2014), juvenile development (Fujita, et al 2004; Marquez Hernandez, et al 2011; Verdonck, et al 1998), and bone remodeling at juvenile and adult stages (Frenkel, et al 2010; Nicks, et al 2010). The hardness of diet can also have a significant impact on craniofacial geometry (Genbrugge, et al 2011; Parsons, et al 2014; Swiderski and Zelditch 2013). The role of such sex-specific and GxE interactions represent a long-standing gap in our knowledge of the etiology and pathophysiology of complex diseases that are unlikely to be answered with traditional mutagenesis screens.…”

“…1, (Albertson, et al 2009)). As with human dysmorphologies, craniofacial differences among cichlids can be detected as early as NCC migration (Albertson and Kocher 2006; Powder, et al 2014), with additional shape differences accumulating into larval and juvenile stages (Parsons, et al 2014; Powder, et al 2015). Cichlids are thus an ideal evolutionary system to study the genetic and developmental origins of both subtle and extreme facial variation due to their (1) extensive morphological variation, (2) mimicking of variation found in humans, and (3) similarities to mammals at the molecular and tissue level.…”

“…The choice of whether to examine the mechanism of gene action within cichlids themselves or within traditional model organisms is dependent on the particulars of the candidate gene or pathway. Cichlids are readily susceptible to pharmacological manipulations through addition of small molecules to their water (Bloomquist, et al 2015; Fraser, et al 2008; Fraser, et al 2013; Hu and Albertson 2014; Parsons and Albertson 2013; Parsons, et al 2014; Powder, et al 2015; Roberts, et al 2011; Sylvester, et al 2010; Sylvester, et al 2013). These chemicals have varying degrees of target specificity (i.e.…”

“…Recently work has combined QTL mapping, population genomics, and experimental manipulations in cichlids to associate the Hedgehog and Wnt pathways with subtle, quantitative variation in bone shape (Hu and Albertson 2014; Loh, et al 2008; Parsons, et al 2014; Roberts, et al 2011). In one study, we mapped QTL for the shape of the interopercle bone and length of the retroarticular process of the mandible to the same genetic interval (Hu and Albertson 2014; Roberts, et al 2011).…”

“…Population genomics also identified a highly divergent SNP in β-catenin between cichlids with alternate craniofacial shapes (Loh, et al 2008). This SNP is associated with increased levels of Wnt signaling and accelerated rates of bone deposition in the cichlid face (Parsons, et al 2014). The accelerated bone development prevents outgrowth of the preorbital region, effectively locking into place an early larval phenotype (i.e., paedomorphosis) (Parsons, et al 2014; Powder, et al 2015).…”