Evolution of a soft‐tissue foraging adaptation in African cichlids: Roles for novelty, convergence, and constraint

Abstract

Understanding the origins of biodiversity demands consideration of both extrinsic (e.g., ecological opportunity) and intrinsic (e.g., developmental constraint) factors. Here, we use a combination of phylogenetic and genetic tools to address the origin of novelty in African cichlids. In particular, we focus on an extreme hypertrophied snout that is structurally integrated with the upper jaw. We show that this bizarre trait has evolved independently in at least two distinct and ecologically successful cichlid clades. We find that snout dimensions are decoupled both phenotypically and genetically, which has enabled it to evolve independently in multiple directions. Further, patterns of variation among species and within a genetic mapping pedigree suggest that relative to snout length, depth is under greater genetic and/or developmental constraint. Models of evolution suggest that snout shape is under selection for feeding behavior, with snout depth being important for algae scraping and snout length for sand sifting. Indeed, the deep snout of some algivores is achieved via an expansion of the intermaxillary ligament, which is important for jaw stability and may increase feeding performance. Overall, our data imply that the evolution of exaggerated snout depth required overcoming a genetic/developmental constraint, which led to expanded ecological opportunity via foraging adaptation.

Weak genetic signal for phenotypic integration implicates developmental processes as major regulators of trait covariation

“…Deeper ventricle shapes are typically associated with more active and athletic fish that require greater blood pressure and stroke work (Claireaux et al, 2005). LF therefore appear to develop a more athletic heart, running counter to our initial expectation that LF is a more efficient forager and should therefore expend less overall energy while feeding, compared to TRC (Conith et al, 2019a). Both species are territorial, with males vigorously defending breeding territories (Ribbink et al, 1983), and a recent study examining activity levels across cichlid species found that LF and TRC exhibit high and indistinguishable levels of activity relative to other species (Lloyd et al, 2020).…”

“…Recent studies have also demonstrated that patterns of trait covariation can span tissues with vastly different developmental origins (e.g. Martínez-Vargas et al, 2017;Conith et al, 2019a;Yamamoto et al, 2020). Taken together, it appears that patterns of integration can encompass multiple tissue types, even extending beyond structures in close physical proximity, to act as a global mechanism permitting the skull to operate as a single unit.…”

“…As a result, TRC have a more shallow craniofacial profile, narrower and longer oral jaws, and a more gracile skull shape. While the diet of TRC is similar to LF, TRC plucks filamentous algae using a twisting and jerking method that is presumably more energetically expensive, and means they are often subjected to the turbulent waters surrounding the rocks (Conith et al, 2019a;Konings, 2007).…”

Diversity in rest-activity patterns among Lake Malawi cichlid fishes suggests novel axis of habitat partitioning

“…This species exhibits significant habitat and dietary overlap with L. fuelleborni, another algae foraging species from the rocky shallows. L. fuelleborni is arguably one of the most ecologically successful species in the lake, with numerous anatomical adaptations that enable it to dominate this niche [31,[44][45][46]. How then might another species coexist with such a well-adapted forager?…”

Function of a novel nasal protrusion for oral-shelling within an adaptive radiation of pupfishes

“…Labeotropheus cichlids is used as a fulcrum, allowing fish to more easily crop algae from rocks 111 versus the bite-and-twist method observed in other cichlid species (Konings 2007;Conith et al 112 2018), and specifically that increased snout depth may help create this mechanical advantage 113 (Conith et al 2019). A similar method may be used during oral shelling to amplify force while 114 removing snails from their shells.…”