Constraint and diversification of developmental trajectories in cichlid facial morphologies

Abstract

BackgroundA major goal of evolutionary biology is to understand the origins of phenotypic diversity. Changes in development, for instance heterochrony, can be a potent source of phenotypic variation. On the other hand, development can also constrain the spectrum of phenotypes that can be produced. In order to understand these dual roles of development in evolution, we examined the developmental trajectory of a trait central to the extensive adaptive radiation of East African cichlid fishes: craniofacial adaptations that allow optimal exploitation of ecological niches. Specifically, we use geometric morphometric analysis to compare morphological ontogenies among six species of Lake Malawi cichlids (n > 500 individuals) that span a major ecomorphological axis. We further evaluate how modulation of Wnt signaling impacts the long-term developmental trajectory of facial development.ResultsWe find that, despite drastic differences in adult craniofacial morphologies, there are general similarities in the path of craniofacial ontogeny among species, suggesting that natural selection is working within a conserved developmental program. However, we also detect species-specific differences in the timing, direction, and/or duration of particular developmental trajectories, including evidence of heterochrony. Previous work in cichlids and other systems suggests that species-specific differences in adult morphology are due to changes in molecular signaling pathways that regulate early craniofacial development. In support of this, we demonstrate that modulation of Wnt signaling at early stages can shift a developmental trajectory into morphospace normally occupied by another species. However, without sustained modulation, craniofacial shape can recover by juvenile stages. This underscores the idea that craniofacial development is robust and that adult head shapes are the product of many molecular changes acting over extended periods of development.ConclusionsOur results are consistent with the hypothesis that development acts to both constrain and promote morphological diversity. They also illustrate the modular nature of the craniofacial skeleton and hence the ability of selection to act upon distinct anatomical features in an independent manner. We propose that trophic diversity among cichlids has been achieved via shifts in both specific (e.g., stage-specific changes in gene expression) and global (e.g., heterochrony) ontogenetic processes acting within a conserved developmental program.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0020-8) contains supplementary material, which is available to authorized users.

What shapes the oral jaws? Accommodation of complex dentition correlates with premaxillary but not mandibular shape

“…When the same species was fed soft food, the pharyngeal jaws were reduced in size and dentition was less complex (Gunter et al, 2013 and. A recent study by Powder et al (2015) used landmark-based morphometrics to compare the mandibles of several cichlid species throughout development, enabling the authors to relate jaw shape to trophic behaviors. Powder et al (2015) associated benthic feeders with short mandibles and pelagic feeders with longer mandibles.…”

“…A recent study by Powder et al (2015) used landmark-based morphometrics to compare the mandibles of several cichlid species throughout development, enabling the authors to relate jaw shape to trophic behaviors. Powder et al (2015) associated benthic feeders with short mandibles and pelagic feeders with longer mandibles. The relationship between bone and tooth development provides insight into the relationship between phenotypic plasticity and natural selection, and is important to consider when studying evolution and comparative anatomy of related species with different feeding habits.…”

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

“…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.…”

“…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). This ultimately results in a steeper craniofacial slope more resistant to strong bite forces in an animal that eats by shearing algae off of rocks (Cooper, et al 2011; Parsons, et al 2014).…”