Abstract Studies of vertebrate feeding have predominantly focused on the bones and muscles of the head, not the body. Yet, postcranial musculoskeletal structures like the spine and pectoral girdle are anatomically linked to the head, and may also have mechanical connections through which they can contribute to feeding. The feeding roles of postcranial structures have been best studied in ray-finned fishes, where the body muscles, vertebral column, and pectoral girdle attach directly to the head and help expand the mouth during suction feeding. Therefore, I use the anatomy and motion of the head–body interface in these fishes to develop a mechanical framework for studying postcranial functions during feeding. In fish the head and body are linked by the vertebral column, the pectoral girdle, and the body muscles that actuate these skeletal systems. The morphology of the joints and muscles of the cranio-vertebral and hyo-pectoral interfaces may determine the mobility of the head relative to the body, and ultimately the role of these interfaces during feeding. The postcranial interfaces can function as anchors during feeding: the body muscles and joints minimize motion between the head and body to stabilize the head or transmit forces from the body. Alternatively, the postcranial interfaces can be motors: body muscles actuate motion between the head and body to generate power for feeding motions. The motor function is likely important for many suction-feeding fishes, while the anchor function may be key for bite- or ram-feeding fishes. This framework can be used to examine the role of the postcranial interface in other vertebrate groups, and how that role changes (or not) with morphology and feeding behaviors. Such studies can expand our understanding of muscle function, as well as the evolution of vertebrate feeding behaviors across major transitions such as the invasion of land and the emergence of jaws.
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Functional coupling in the evolution of suction feeding and gill ventilation of sculpins (Perciformes: Cottoidei)
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.
more » « less- NSF-PAR ID:
- 10118456
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 2
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- p. 394-409
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Abstract While functional morphologists have long studied the evolution of anatomical structures, the origin of morphological novelties has received less attention. When such novelties first originate they must become incorporated into an integrated system to be rendered fully functional. Thus, developmental integration is key at the origin of morphological novelties. However, given enough evolutionary time such integration may be broken, allowing for a division of labor that is facilitated by subsequent decoupling of structures. Cypriniformes represent a diverse group of freshwater fishes characterized by several trophic novelties that include: kinethmoid-mediated premaxillary protrusion, a muscular palatal and post-lingual organ, hypertrophied lower pharyngeal jaws that masticate against the base of the neurocranium, novel pharyngeal musculature controlling movement of the hypertrophied lower pharyngeal jaws, and in a few species an incredibly complex epibranchial organ used to aggregate filtered phytoplankton. Here, we use the wealth of such trophic novelties in different cypriniform fishes to present case studies in which developmental integration allowed for the origin of morphological innovations. As proposed in case studies 1 and 2 trophic innovations may be associated with both morphological and lineage diversification. Alternatively, case studies 3 and 4 represent a situation where ecological niche was expanded but with no concomitant increase in species diversity.more » « less
