Bony Patchwork: Mosaic Patterns of Evolution in the Skull of Electric Fishes (Apteronotidae: Gymnotiformes)

Abstract

Mosaic evolution refers to the pattern whereby different organismal traits exhibit differential rates of evolution typically due to reduced levels of trait covariation through deep time (i.e., modularity). These differences in rates can be attributed to variation in responses to selective pressures between individual traits. Differential responses to selective pressures also have the potential to facilitate functional specialization, allowing certain traits to track environmental stimuli more closely than others. The teleost skull is a multifunctional structure comprising a complex network of bones and thus an excellent system for which to study mosaic evolution. Here we construct an ultrametric phylogeny for a clade of Neotropical electric fishes (Apteronotidae: Gymnotiformes) and use three-dimensional geometric morphometrics to investigate patterns of mosaic evolution in the skull and jaws. We find strong support for a developmental, three-module hypothesis that consists of the face, braincase, and mandible, and we find that the mandible has evolved four times faster than its neighboring modules. We hypothesize that the functional specialization of the mandible in this group of fishes has allowed it to outpace the face and braincase and evolve in a more decoupled manner. We also hypothesize that this pattern of mosaicism may be widespread across other clades of teleost fishes.

Ecomorphological divergence and habitat lability in the context of robust patterns of modularity in the cichlid feeding apparatus

“…This trend is consistent with the adaptive value of these traits with respect to feeding kinematics. Indeed, the trend in functionally relevant components of anatomical structures exhibiting fast rates and high evolvability has been noted in other teleosts groups (i.e., Electric fishes [ 52 , 53 ], cichlids, pomacentrids, centrarchids, and labrids [ 54 ]), and may reflect a general trend across organisms [ 55 , 56 ]. In terms of disparity, it is notable that the tooth-plate module exhibited the highest levels for both the mandible and lower pharyngeal jaw.…”

Ecomorphology of Neotropical Electric Fishes: An Integrative Approach to Testing the Relationships between Form, Function, and Trophic Ecology

“…The shape of mandible in particular has been found to closely track diet and is known to be highly plastic at early developmental stages in fishes ( Hu and Albertson 2017 ). Furthermore, within gymnotiform fishes, the mandible has been shown to evolve nearly four times faster than its neighboring skull regions ( Evans et al. 2019 ).…”

A new species of sexually dimorphic and rheophilic ghost knifefish (Apteronotidae: Gymnotiformes) from the Amazon basin

“…The snout and jaw elongation within Apteronotidae has been the subject of debate in several contributions (Albert, 2001;Albert & Crampton, 2009;Cox Fernandes, 1998;Cox Fernandes et al, 2002;Evans et al, 2017bEvans et al, , 2019aEvans et al, , 2019bHilton & Cox Fernandes, 2006;Keeffe et al, 2019;Py-Daniel & Cox Fernandes, 2004;de Santana & Vari, 2010b). Albert and Crampton (2009) described three patterns for the jaw elongation among apteronotids: snout elongation accompanied by a relatively small, terminal mouth (e.g., Sternarchorhynchus; Sternarchorhamphus + Orthosternarchus), associated with grasp-suction feeding (Marrero & Winemiller, 1993); allometric elongation of the pre-otic region of the neurocranium with a small mouth (e.g., A. cuchillo + A. magalenensis), for benthic probing in deep river channels (Albert & Crampton, 2009); and pre-orbital region elongated with large jaws (e.g., Parapteronotus Albert, 2001 andCompsaraia Albert, 2001) used in social behaviour, such as male-male aggression identified as mouth-gaping behaviour (Evans et al, 2019a: Figure 10;Hagedorn & Heiligenberg, 1985;Kirschbaum, 1992).…”

“…Based on the most recent phylogenetic hypothesis of apteronotids relationships (Bernt et al, 2019), the pattern of the snout elongation present in males of A. quilombola would have evolved independently multiple times within the family (Evans et al, 2019b). Yet despite this, the dimorphic males of these taxa share several osteological similarities related to the elongation of their snouts.…”