Abstract
ABSTRACTThe fin-to-limb transition is heralded as one of the most important events in vertebrate evolution. Over the last few decades our understanding of how limbs evolved has significantly increased; but, hypotheses forwhylimbs evolved are still rather open. Fishes that engage their fins to ‘walk' along substrate may provide some perspective. The charismatic frogfishes are often considered to have the most limb-like fins, yet we still know little about their underlying structure. Here we reconstruct the pectoral fin musculoskeletal anatomy of the scarlet frogfish to identify adaptations that support fin-assisted walking behaviours. The data are compared to three additional anglerfish species: the oval batfish, which represents an independent acquisition of fin-assisted walking; and two pelagic deep-sea swimmers, the triplewart seadevil and ghostly seadevil. Our results clearly show broad musculoskeletal differences between the pectoral fins of swimming and walking anglerfish species. The frogfish and batfish have longer and more robust fins; larger, differentiated muscles; and better developed joints, including a reverse ball-and-socket glenoid joint and mobile ‘wrist'. Further, the frogfish and batfish show finer-scale musculoskeletal differences that align with their specific locomotor ecologies. Within, we discuss the functional significance of these anatomical features in relation to walking, the recurring evolution of similar adaptations in other substrate locomoting fishes, as well as the selective pressures that may underlie the evolution of limbs.
Highlights
The evolution of tetrapod limbs from fish fins is one of the best-studied transitions in vertebrate evolution (Clack 2005, 2009)
Specimens were chosen by their ability to be contrast-enhanced stained and micro-computed tomography (mCT) scanned in a reasonable timeframe, as the largest specimens of some anglerfish species can grow too large to efficiently stain or scan using a standard mCT scanner
Comparing pectoral fin musculoskeletal anatomy of pelagic swimming anglerfish with benthic substrate locomotors has highlighted a number of potential adaptations that may enable
Summary
The evolution of tetrapod limbs from fish fins is one of the best-studied transitions in vertebrate evolution (Clack 2005, 2009). The drying-up-pool hypothesis was favoured, in which stranded fish (e.g., Eusthenopteron) were under selective pressure to evolve more limb-like appendages to return to water (e.g., Romer 1958) This ‘terrestriality before limbs’ scenario has generally fallen by the wayside (Clack 2012; Pierce et al 2013); one reason is that it hinged on the notion that the Devonian red beds were deposited in arid conditions, when such geological signatures can correlate with wet environments. The musculoskeletal data are compared to three additional anglerfishes, including: FP the benthic ‘walking’ oval batfish (Ogcocephalidae; Fig. 1b), which represents an independent acquisition of fin-assisted walking; and two deep-sea pelagic seadevils – the triplewart seadevil (Ceratiidae; Fig. 1d) and the ghostly seadevil (Linophrynidae; Fig. 1e) Through this comparative lens, we discuss potential adaptations of the limb-like pectoral fins in frogfishes (and batfishes), as well as anatomical trade-offs that may enable diverse types of fin-assisted locomotor behaviours
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