Mosaic Evolution of the Skull in Labrid Fishes Involves Differences in Both Tempo and Mode of Morphological Change

Abstract

Abstract.—Modularity is a ubiquitous feature of organismal design that plays an important role in structuring patterns of morphological diversification. Modularity can facilitate evolutionary changes by allowing subsets of traits to coevolve as integrated units and follow quasi-independent evolutionary trajectories, a pattern that may be particularly consequential in the case of highly complex morphological structures. Here we examine modularity in a complex and highly kinetic structure, the teleost skull, and ask if a modular organization of the skull has influenced the diversification dynamics of the shapes of its osteological components across the labrid phylogeny. We compiled one of the largest 3D morphological data sets of fishes to date and used geometric morphometrics to quantify patterns of cranial shape evolution across 184 species of wrasses (Labridae). We then tested several hypotheses of modularity inspired by functional and developmental relationships between cranial bones and compared phenotypic rates among modules. We also compared the fit of models of trait evolution for the entire skull and the various articulated bones that it comprises. Our analyses indicated strong support for a 2-module hypothesis, one that encompasses the oral and pharyngeal jaws and another module comprised of the neurocranium, hyoid apparatus, and operculum. This functional hypothesis yielded one of the highest significant rate differentials across modules, yet we also found that the best-fitting models of trait evolution differed among skull bones. These results suggest that modularity can influence morphological diversification in complex biological structures via differences in both the tempo and mode of evolutionary change. [3D geometric morphometrics, cranial morphology, evolutionary modularity, Labridae, phenotypic rates, structural complexity.]

Whole-body variational modularity in the zebrafish: an inside-out story of a model species

“…These cranio-vertebral and hyo-pectoral interfaces lead to a more efficient suction mechanism and act as anchors to stabilize the head or to transfer power from the body during feeding [50,51]. The relatively low integration of the skull may also signify that it has a modular organization, which has been previously observed using morphological, developmental and genetic lines of evidence [18,52–56]. Numerous articulated bones and cartilages allow for a high level of cranial kinesis, while functional and biomechanical constraints put a pressure on its variability to preserve functional unity and stability [18,57].…”

How to tuna fish: constraint, convergence and integration in the neurocranium of pelagiarian fishes

“…It is possible that the loose association of jaw, suspensorium, and opercular elements in teleosts is a result of relaxed integration across the entire skull. A recently published study incorporating kinetic skull elements suggested that modularity may influence morphological divergence in complex feeding structures in labrid fishes (wrasses) (Larouche et al, 2022). Wrasses have evolved a diverse range of feeding strategies, which are likely to have been driven by the dietary diversity of their reef and shallow water habitats.…”

“…In contrast to structurally complex biodiverse settings like coral reefs (Roberts et al, 2002; Rabosky et al, 2018), it might seem environmentally homogenous, but the wide range of light levels, temperatures, currents, and food availability creates a surprising diversity of ecological niches that may drive adaptation. Most research on the phenotypic evolution of marine fishes focuses on clades (Larouche et al 2022; Evans et al 2022) or assemblages (Claverie and Wainwright, 2014) principally associated with shallow-water, coastal settings, often in proximity to reefs. However, recent surveys of fishes across marine habitats reveal that some settings are unexpected hotspots of phenotypic evolution (Friedman et al 2019; Martinez et al 2021).…”

“…Similarly, the tetrapod skull has been shown to be highly modular despite the loss or fusion of a number of skull elements through evolutionary history (Goswami et al, 2014; Felice and Goswami, 2017; Bardua et al, 2019; Felice et al, 2019; Fabre et al, 2020). The developmental and evolutionary decoupling of kinetic elements may have allowed teleosts to exploit a wide range of niches by enabling the evolution of diverse feeding strategies (Larouche et al, 2022). Understanding patterns of integration is therefore an important step in understanding the evolution of this complex structure in teleosts in context with better-understood tetrapod groups.…”

Description of the First Species of Polylepion (Teleostei: Labridae) from the Atlantic Ocean with Analysis of Evolutionary Relationships of the New Species

“…In his description of Polylepion , Gomon (1977) noted that, morphologically, the genus closely resembles Decodon , Pimelometopon , Semicossyphus , and Bodianus , the last a historically catch-all wrasse genus to which P. russelli was originally assigned (Gomon and Randall, 1975) and to which Semicossyphus (including Pimelometopon based on Gomon [1997]) was recently provisionally relegated (Santini et al, 2016). Molecular phylogenies of the Labridae revealed a sister-group relationship between Polylepion and Decodon (Aiello et al, 2017; Hughes et al, 2022; Larouche et al, 2022) and a paraphyletic Bodianus without the inclusion of Clepticus , Decodon , Polylepion , and Semicossyphus (Aiello et al, 2017) or without the inclusion of Clepticus and Semicossyphus (Hughes et al, 2022; Larouche et al, 2022). By combining the recently published time-calibrated phylogenomic tree for the Labridae (Hughes et al, 2022) with genetic sequences for over 300 species of wrasses (Aiello et al, 2017), we investigated the evolutionary history and timing of speciation events of the genus Polylepion , incorporating new genetic data for P. cruentum and the new species.…”