Extreme Morphology, Functional Trade-offs, and Evolutionary Dynamics in a Clade of Open-Ocean Fishes (Perciformes: Bramidae)

Abstract

When novel or extreme morphologies arise, they are oft met with the burden of functional trade-offs in other aspects of anatomy, which may limit phenotypic diversification and make particular adaptive peaks inaccessible. Bramids (Perciformes: Bramidae) comprise a small family of 20 extant species of fishes, which are distributed throughout pelagic waters worldwide. Within the Bramidae, the fanfishes (Pteraclis and Pterycombus) differ morphologically from the generally stout, laterally compressed species that typify the family. Instead, Pteraclis and Pterycombus exhibit extreme anterior positioning of the dorsal fin onto the craniofacial skeleton. Consequently, they possess fin and skull anatomies that are radically different from other bramid species. Here, we investigate the anatomy, development, and evolution of the Bramidae to test the hypothesis that morphological innovations come at functional (proximate) and evolutionary (ultimate) costs. Addressing proximate effects, we find that the development of an exaggerated dorsal fin is associated with neurocrania modified to accommodate an anterior expansion of the dorsal fin. This occurs via reduced development of the supraoccipital crest (SOC), providing a broad surface area on the skull for insertion of the dorsal fin musculature. While these anatomical shifts are presumably associated with enhanced maneuverability in fanfishes, they are also predicted to result in compromised suction feeding, possibly limiting the mechanisms of feeding in this group. Phylogenetic analyses suggest craniofacial and fin morphologies of fanfishes evolved rapidly and are evolutionarily correlated across bramids. Furthermore, fanfishes exhibit a similar rate of lineage diversification as the rest of the Bramidae, lending little support for the prediction that exaggerated medial fins are associated with phylogenetic constraint. Our phylogeny places fanfishes at the base of the Bramidae and suggests that non-fanfish bramids have reduced medial fins and re-evolved SOCs. These observations suggest that the evolution of novel fin morphologies in basal species has led to the phylogenetic coupling of head and fin shape, possibly predisposing the entire family to a limited range of feeding. Thus, the evolution of extreme morphologies may have carry-over effects, even after the morphology is lost, limiting ecological diversification of lineages.

Divergence in digestive and metabolic strategies matches habitat differentiation in juvenile salmonids

“…Adaptive trade‐offs impose fundamental constraints on phenotypic evolution and shape biodiversity patterns by allowing the coexistence of taxa along environmental gradients (Careau et al, 2010 ; Finstad et al, 2011 ). Although morphological and behavioral trade‐offs have received considerable attention (e.g., cranial versus fin morphology: Gilbert et al, 2021 ; shy versus bold behaviors: Stamps, 2007 ), physiological trade‐offs, and their impacts on fitness correlates (e.g., growth and survival: Monaghan et al, 2009 ) may also drive considerable phenotypic and ecological differentiation (Braendle et al, 2011 ; Careau & Garland, 2012 ). Cryptic trade‐offs among competing physiological processes, however, are less well studied, despite the potential to generate significant biological diversity in nature (Agrawal et al, 2010 ).…”

Breaking constraints: The development and evolution of extreme fin morphology in the Bramidae

“…Lastly, others have found that quantifying evolutionary rates by using the initial principal component axes can bias the results to mirror an EB evolutionary model (Uyeda et al, 2015). We, therefore, urge caution in these interpretations and refer to our previous paper (Gilbert et al, 2021) for other results supporting an EB model.…”

“…Methods for acquiring both geometric morphometric data and linear measures are described in detail in Gilbert et al (2021). In short, the left lateral surfaces of specimens were imaged and then digitized using STEREOMORPH (Olsen & Westneat, 2015) in R (R Core Team, 2018).…”

“…Ontogenetic trajectories of select traits have been previously studied in this group (Mead, 1972), but data were unable to be interpreted through a phylogenetic lens, rendering hypotheses about evolutionary relationships and constraints untestable. Here, we expand on this previous work (e.g., Gilbert et al, 2021;Mead, 1972) by comparing anatomical divergence across the Bramidae at early and adult lifehistory stages in a phylogenetic context. Specifically, we will assess the degree to which the evolution of extreme fin morphologies has limited the evolution of other ecomorphological traits.…”

Relaxed Feeding Constraints Facilitate the Evolution of Mouthbrooding in Neotropical Cichlids

“…Throughout an organism's lifetime, most structures will serve more than one function. This multifunctionality is often framed as a core constraint of phenotypic evolution: the more functions a structure directly serves, the more the evolution of that structure is constrained by the increasingly narrow range of phenotypes that will sufficiently serve all of those functions (Corn et al, 2021;Gilbert et al, 2021). Most of the functions an animal must perform -feeding, respiration, locomotion, and reproduction -do not change, even if their particular mode (e.g.…”