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Suction feeding in ray-finned fishes requires substantial muscle power for fast and forceful prey capture. The axial musculature located immediately behind the head has been long known to contribute some power for suction feeding, but recent XROMM and fluoromicrometry studies found nearly all the axial musculature (over 80%) provides effectively all (90–99%) of the power for high-performance suction feeding. The dominance of axial power suggests a new framework for studying the musculoskeletal biomechanics of fishes: the form and function of axial muscles and bones should be analysed for power production in feeding (or at least as a compromise between swimming and feeding), and cranial muscles and bones should be analysed for their role in transmitting axial power and coordinating buccal expansion. This new framework is already yielding novel insights, as demonstrated in four species for which suction power has now been measured. Interspecific comparisons suggest high suction power can be achieved in different ways: increasing the magnitude of suction pressure or the rate of buccal volume change, or both (as observed in the most powerful of these species). Our framework suggests that mechanical and evolutionary interactions between the head and the body, and between the swimming and feeding roles of axial structures, may be fruitful areas for continued study.
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Functional coupling in the evolution of suction feeding and gill ventilation of sculpins (Perciformes: Cottoidei)
Abstract Suction feeding and gill ventilation in teleosts are functionally coupled, meaning that there is an overlap in the structures involved with both functions. Functional coupling is one type of morphological integration, a term that broadly refers to any covariation, correlation, or coordination among structures. Suction feeding and gill ventilation exhibit other types of morphological integration, including functional coordination (a tendency of structures to work together to perform a function) and evolutionary integration (a tendency of structures to covary in size or shape across evolutionary history). Functional coupling, functional coordination, and evolutionary integration have each been proposed to limit morphological diversification to some extent. Yet teleosts show extraordinary cranial diversity, suggesting that there are mechanisms within some teleost clades that promote morphological diversification, even within the highly integrated suction feeding and gill ventilatory systems. To investigate this, we quantified evolutionary integration among four mechanical units associated with suction feeding and gill ventilation in a diverse clade of benthic, primarily suction-feeding fishes (Cottoidei; sculpins and relatives). We reconstructed cottoid phylogeny using molecular data from 108 species, and obtained 24 linear measurements of four mechanical units (jaws, hyoid, opercular bones, and branchiostegal rays) from micro-CT reconstructions of 44 cottoids and 1 outgroup taxon. We tested for evolutionary correlation and covariation among the four mechanical units using phylogenetically corrected principal component analysis to reduce the dimensionality of measurements for each unit, followed by correlating phylogenetically independent contrasts and computing phylogenetic generalized least squares models from the first principle component axis of each of the four mechanical units. The jaws, opercular bones, and branchiostegal rays show evolutionary integration, but the hyoid is not positively integrated with these units. To examine these results in an ecomorphological context, we used published ecological data in phylogenetic ANOVA models to demonstrate that the jaw is larger in fishes that eat elusive or grasping prey (e.g., prey that can easily escape or cling to the substrate) and that the hyoid is smaller in intertidal and hypoxia-tolerant sculpins. Within Cottoidei, the relatively independent evolution of the hyoid likely has reduced limitations on morphological evolution within the highly morphologically integrated suction feeding and gill ventilatory systems.
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- PAR ID:
- 10110606
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 2
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 394 to 409
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/icb/icz022
