Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins‐to‐limbs transition

Abstract

The question of how tetrapod limbs evolved from fins is one of the great puzzles of evolutionary biology. While palaeontologists, developmental biologists, and geneticists have made great strides in explaining the origin and early evolution of limb skeletal structures, that of the muscles remains largely unknown. The main reason is the lack of consensus about appendicular muscle homology between the closest living relatives of early tetrapods: lobe-finned fish and crown tetrapods. In the light of a recent study of these homologies, we re-examined osteological correlates of muscle attachment in the pectoral girdle, humerus, radius, and ulna of early tetrapods and their close relatives. Twenty-nine extinct and six extant sarcopterygians were included in a meta-analysis using information from the literature and from original specimens, when possible. We analysed these osteological correlates using parsimony-based character optimization in order to reconstruct muscle anatomy in ancestral lobe-finned fish, tetrapodomorph fish, stem tetrapods, and crown tetrapods. Our synthesis revealed that many tetrapod shoulder muscles probably were already present in tetrapodomorph fish, while most of the more-distal appendicular muscles either arose later from largely undifferentiated dorsal and ventral muscle masses or did not leave clear correlates of attachment in these taxa. Based on this review and meta-analysis, we postulate a stepwise sequence of specific appendicular muscle acquisitions, splits, and fusions that led from the ancestral sarcopterygian pectoral fin to the ancestral tetrapod forelimb. This sequence largely agrees with previous hypotheses based on palaeontological and comparative work, but it is much more comprehensive in terms of both muscles and taxa. Combined with existing information about the skeletal system, our new synthesis helps to illuminate the genetic, developmental, morphological, functional, and ecological changes that were key components of the fins-to-limbs transition.

Anatomical network analysis of the musculoskeletal system reveals integration loss and parcellation boost during the fins-to-limbs transition

“…; Molnar et al. , ). In limbs, we find a wider variety of muscles between two extremes (higher H ): some limb muscles establish a few short‐range connections and function more locally (e.g., intermetatarsales, flexores breves profundi, and contrahentes pedis, each of which has two connections), while others establish many long‐range connections and function more globally (e.g., flexor digitorum communis, contrahentium caput longum, extensor digitorum longus) (Diogo and Abdala ).…”

“…The study of the origin of limbs involves working with uncertain homologies between anatomical structures, reconstructing soft tissue in transitional fossil taxa, and gathering information from the few extant taxa close to the fins‐to‐limbs transition (e.g., Molnar et al. ). These circumstances present a challenge for quantitative methods comparing the anatomical organization of appendages, especially in very disparate forms.…”

“…; Molnar et al. ; Santos et al. ), and to quantify patterns of morphological complexity, integration, and modularity in a manner not available for comparative methods that focus on shape and size (Kerkman et al.…”

“…), to bracket the fins‐to‐limbs transition and to infer transitional morphologies (Molnar et al. ). Likewise, we rely on extant species to understand how the anatomical organization of appendages has evolved, and how pectoral‐pelvic similarity changed before and after the fins‐to‐limbs transition.…”

“…Although at first sight the limbs and lobe-fins of extant species look different, they share some deep similarities in their anatomical organization-the way in which bones and muscles are arranged together-that reveal their common origin. The study of the origin of limbs involves working with uncertain homologies between anatomical structures, reconstructing soft tissue in transitional fossil taxa, and gathering information from the few extant taxa close to the fins-to-limbs transition (e.g., Molnar et al 2017). These circumstances present a challenge for quantitative methods comparing the anatomical organization of appendages, especially in very disparate forms.…”