The Evolution of Appendicular Muscles During the Fin-to-Limb Transition: Possible Insights Through Studies of Soft Tissues, a Perspective

Mansuit, Rohan; Herrel, Anthony

doi:10.3389/fevo.2021.702576

Cited by 4 publications

(5 citation statements)

References 51 publications

(93 reference statements)

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“…This difference indicates a shift occurred during the fin to limb transition in which tetrapods have experienced a reduction of their deep appendicular muscles and an increase of superficial musculature. This shift is suggested to be an adaptation to the mechanical demands required of terrestrial locomotion, needing more strength to support the body against gravity, as opposed to buoyancy in aquatic habits (Mansuit and Herrel, 2021). Our examination of the musculature indicates that the superficial appendicular musculature is more prominent than the deep musculature in C. milii, at least in terms of surface area.…”

Section: Comments On Developmentmentioning

confidence: 76%

“…The prominent size of the superficial musculature in C. milii may have some evolutionary implications for fin muscles. Comparisons of the appendicular musculature between different species of fishes and tetrapods have revealed that superficial muscles are heavier than deep muscles in both limbs of tetrapods whereas deeper muscles are more developed in the fins of fishes (Mansuit and Herrel, 2021). This difference indicates a shift occurred during the fin to limb transition in which tetrapods have experienced a reduction of their deep appendicular muscles and an increase of superficial musculature.…”

Section: Comments On Developmentmentioning

confidence: 99%

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Imaging With the Past: Revealing the Complexity of Chimaeroid Pelvic Musculature Anatomy and Development

et al. 2022

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Chondrichthyans are now widely adopted as models for examining the development and evolution of the stem gnathostome body plan. The fins of some cartilaginous fish are recognized for their plesiomorphic form and mode of muscular development, i.e., epithelial extension. Despite detailed molecular and descriptive examinations of these developmental mechanisms, there has been little contemporary examination of the ontogeny and morphology of the musculature in chondrichthyans including that of the paired fins. This gap represents a need for further examination of the developmental morphology of these appendicular musculatures to gain insight into their evolution in gnathostomes. The elephant shark is a Holocephalan, the sister group of all other chondrichthyans (Holocephali: Callorhinchus milii). Here, we use nano-CT imaging and 3D reconstructions to describe the development of the pelvic musculature of a growth series of elephant shark embryos. We also use historical descriptions from the nineteenth century and traditional dissection methods to describe the adult anatomy. This combined approach, using traditional methods and historical knowledge with modern imaging techniques, has enabled a more thorough examination of the anatomy and development of the pelvic musculature revealing that chimaeroid musculatures are more complex than previously thought. These data, when compared to extant and extinct sister taxa, are essential for interpreting and reconstructing fossil musculatures as well as understanding the evolution of paired fins.

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Section: Comments On Developmentmentioning

confidence: 76%

Section: Comments On Developmentmentioning

confidence: 99%

Imaging With the Past: Revealing the Complexity of Chimaeroid Pelvic Musculature Anatomy and Development

et al. 2022

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“…We have newly identified the gene qkia , which contributes to muscle formation in the fin. Although muscle was not lost in the tetrapod limb, it is possible that the loss of function of qkia may have contributed to the change in muscle architecture from the fish pattern to the tetrapod pattern (Diogo et al, 2016; Mansuit & Herrel, 2021). Overall, we confirmed that some fish‐specific and fin‐expressed genes contribute to the fish‐specific trait.…”

Section: Discussionmentioning

confidence: 99%

Genomic screening of fish‐specific genes in gnathostomes and their functions in fin development

Kudoh,

Yonei‐Tamura,

Abe

et al. 2024

Dev Growth Differ

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In this study, we comprehensively searched for fish‐specific genes in gnathostomes that contribute to development of the fin, a fish‐specific trait. Many previous reports suggested that animal group‐specific genes are often important for group‐specific traits. Clarifying the roles of fish‐specific genes in fin development of gnathostomes, for example, can help elucidate the mechanisms underlying the formation of this trait. We first identified 91 fish‐specific genes in gnathostomes by comparing the gene repertoire in 16 fish and 35 tetrapod species. RNA‐seq analysis narrowed down the 91 candidates to 33 genes that were expressed in the developing pectoral fin. We analyzed the functions of approximately half of the candidate genes by loss‐of‐function analysis in zebrafish. We found that some of the fish‐specific and fin development‐related genes, including fgf24 and and1/and2, play roles in fin development. In particular, the newly identified fish‐specific gene qkia is expressed in the developing fin muscle and contributes to muscle morphogenesis in the pectoral fin as well as body trunk. These results indicate that the strategy of identifying animal group‐specific genes is functional and useful. The methods applied here could be used in future studies to identify trait‐associated genes in other animal groups.

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“…The exact mechanisms driving these scaling differences are unclear and require more-explicit analyses of both tissue and elemental content as they relate to body size. We suggest that lower scaling intercepts for aquatic organisms could reflect constraints on the body plan for mechanical adaptations to life in water, such as increases in vertebrate buoyancy (Mansuit & Herrel 2021) and invertebrate exoskeleton thickness (Taylor 2018). Alternatively, diversity in locomotion modes, particularly in aquatic organisms (e.g., drag-based, lifted-based, jetting) may influence elemental-size scaling relationships, if these strategies generate trade-offs between muscle allocation to support increases in body size versus locomotion (Clemente & Richards 2013; Vogel 2008).…”

Section: Discussionmentioning

confidence: 99%

Body size is a better predictor of intra- than interspecific variation of animal stoichiometry across realms

Nessel,

Dézerald,

Merder

et al. 2024

Preprint

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Animal stoichiometry affects fundamental processes ranging from organismal physiology to global element cycles. However, it is unknown whether animal stoichiometry follows predictable scaling relationships with body mass and whether adaptation to life on land or water constrains patterns of elemental allocation. To test both interspecific and intraspecific body-size scaling relationships of the nitrogen (N), phosphorus (P), and N:P content of animals, we used a subset of the StoichLife database encompassing 9,933 individual animals (vertebrates and invertebrates) belonging to 1,543 species spanning 10 orders of magnitude of body size from terrestrial, freshwater, and marine realms. Across species, body mass did not explain much variation in %N and %P composition, although the %P of invertebrates decreased with size. The effects of body size on species elemental content were small in comparison to the effects of taxonomy. Body size was a better predictor of intraspecific than interspecific elemental patterns. Between 42 to 45% in intraspecific stoichiometric variation was explained by body size for 27% of vertebrate species and 35% of invertebrate species. Further, differences between organisms inhabiting aquatic and terrestrial realms were observed only in invertebrate interspecific %N, suggesting that the realm does not play an important role in determining elemental allocation of animals. Based on our analysis of the most comprehensive animal stoichiometry database, we conclude that (i) both body size and realm are relatively weak predictors of animal stoichiometry across taxa, and (ii) body size is a good predictor of intraspecific variation in animal elemental content, which is consistent with tissue-scaling relationships that hold broadly across large groups of animals. This research reveals a lack of general scaling patterns in the elemental content across animals and instead points to a large variation in scaling relationships within and among lineages.

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The Evolution of Appendicular Muscles During the Fin-to-Limb Transition: Possible Insights Through Studies of Soft Tissues, a Perspective

Cited by 4 publications

References 51 publications

Imaging With the Past: Revealing the Complexity of Chimaeroid Pelvic Musculature Anatomy and Development

Imaging With the Past: Revealing the Complexity of Chimaeroid Pelvic Musculature Anatomy and Development

Genomic screening of fish‐specific genes in gnathostomes and their functions in fin development

Body size is a better predictor of intra- than interspecific variation of animal stoichiometry across realms

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