Abstract
Muscle is a complex tissue that has been studied on numerous hierarchical levels: from gross descriptions of muscle organization to cellular analyses of fiber profiles. In the middle of this space between organismal and cellular biology lies muscle architecture, the level at which functional correlations between a muscle's internal fiber organization and contractile abilities are explored. In this review, we summarize this relationship, detail recent advances in our understanding of this form‐function paradigm, and highlight the role played by The Anatomical Record in advancing our understanding of functional morphology within muscle over the past two decades. In so doing, we honor the legacy of Editor‐in‐Chief Kurt Albertine, whose stewardship of the journal from 2006 through 2020 oversaw the flourishing of myological research, including numerous special issues dedicated to exploring the behavioral correlates of myology across diverse taxa. This legacy has seen the The Anatomical Record establish itself as a preeminent source of myological research, and a true leader within the field of comparative anatomy and functional morphology.
Keywords: adaptation, ecology, morphology, myology, physiological cross‐sectional area
1. INTRODUCTION
Skeletal muscle is a complex and hierarchically organized material responsible for generating the forces that power movements of the body. In Kurt Albertine's years as Editor in Chief of The Anatomical Record, the journal was at the forefront of publishing papers that described variation and organization of muscles across myriad species, and exploring the behavioral correlates of this myology across multiple scales: from gross anatomical analyses of muscle sizes down to the cellular profile of individual muscle fibers. In the middle of this space between organismal and cellular biology lies muscle architecture: the arrangement of individual fascicles (or fiber bundles) within a muscle. In the past two decades, the quantification and interspecific comparison of internal muscle architecture has illuminated our understanding of exactly how the design of individual muscles may be optimized to meet specific physical demands: for example, to maximize force production, contractile velocity, excursion potential, or any combination thereof. In this article, we review recent advances in correlating behavior and ecology with myology, with special emphasis to those published in The Anatomical Record while under the leadership of Albertine.
1.1. Early comparative anatomy
The organization of muscles within the body, both human and non‐human, has held the fascination of scholars and artists alike for centuries (Cole, 1949; Cosans & Frampton, 2015). Historical accounts describe naturalistic experiments that include the dissection and anatomical description of animals from as early as 500 BCE (e.g., Timaeus a Calcidio Translatus Commentarioque Instructus; translated by Waszink & Jensen, 1975). More explicit comparative works can be found in Aristotle's essays Parts of Animals and History of Animals, published c. 350 BCE (for translations see Ogle, 1882; Peck, 1965), which include notes from his own personal dissections of more than 50 species (Cole, 1949; Lones, 1912) alongside synthesized reports from other scholars. These early studies represent the first direct interspecific observations of internal anatomical organization (e.g., “the parts of the body are not arranged in the same way in all animals”; History of Animals III, 4.515) as well as the first attempts to integrate anatomical form and function (e.g., “the absence of randomness, and the presence of purpose, are found”; Parts of Animals I: 5.644). Studies of comparative anatomy would continue through classical antiquity and the middle ages before an explosion of renaissance works by natural philosophers such as Andreas Vesalius (1514–1564), Pierre Belon (1517–1564), and Conrad Gesner (1516–1565). Chief among these in its scientific and medical impact was De humani corporis fabrica (Vesalius, 1543), which provided detailed illustrations and descriptions of muscles throughout the human body, including comprehensive notes on vascular and nervous supply as well as functional role.
It would take a subsequent three centuries, however, for comparative myology in the modern anatomical sense to emerge. Inspired by evolutionary theories of the age (e.g., Darwin, 1859; Lamarck, 1809; Saint‐Hilaire, 1822; Wallace, 1878) describing the selective mechanisms by which an animal's form and function may be related, a huge number (see Cole & Eales, 1917) of descriptive accounts began to rigorously describe and compare muscle size, shape, and organization between taxa (e.g., Chauveau & Arloing, 1885; Fisher, 1946; Howell, 1926; Huber, 1930; Lang, 1896; Wiedersheim, 1907; Wood, 1867). In so doing, such studies laid the groundwork for modern ecomorphological investigations into muscular anatomy and variation therein.
1.2. Understanding muscle architecture
Descriptions of muscle attachments and organization continue to serve as the backbone for many comparative anatomical investigations. However, 20th‐century advances in the theoretical understanding of myological mechanisms encouraged anatomists to consider muscle internal anatomy as well as its macroscopic form (e.g., Gans & Bock, 1965; Schumacher, 1961). Internally, skeletal muscle is composed of muscle fascicles: bundles of muscle fibers which are themselves composed of serially‐arranged sarcomeres. Sarcomeres represent the force‐generating unit of muscle, which is achieved via shortening driven by cross‐interactions between myosin and actin filaments (Edman, 1966; Gordon et al., 1966; Lieber et al., 1984; Ter Keurs et al., 1978). Sarcomere lengths are highly constrained across vertebrates (2–2.5 μm; Goldspink, 1968; Burkholder & Lieber, 2001) such that longer fibers achieve this length by containing a greater number of sarcomeres connected end to end. As sarcomeres within a muscle fiber shorten simultaneously, increasing fiber length is therefore associated with a greater contractile velocity: that is, closing a greater amount of distance per unit of time (Lieber & Fridén, 2000; Sacks & Roy, 1982). Because each sarcomere shortens roughly the same distance and longer fibers contain more sarcomeres in series, longer fascicles also have greater absolute excursion potential (Gans, 1982; Gans & Gaunt, 1991; Lieber, 1986; Lieber & Ward, 2011).
While excursion is driven by the length of a muscle's constituent fascicles, the magnitude of force that a muscle can produce is determined by the number of fibers within a muscle (Gans & Bock, 1965; Gans & de Vree, 1987; Wickiewicz et al., 1983), a property which is proportional to the physiological cross‐sectional area (PCSA) of the muscle (Brand et al., 1986; Maughan et al., 1983; Schumacher, 1961). For any given volume of muscle, PCSA can be optimized by packing a higher number of shorter fascicles into that space. Thus, there exists a fundamental trade‐off within skeletal muscle between velocity/excursion potential on the one hand and contractile force on the other, that is determined by the length of a muscle's constituent fascicles (Gans, 1982; Lieber & Ward, 2011). To this end, if a given muscle needs to produce relatively high force for the same amount of contractile speed or excursion, then it must be relatively larger.
As demonstrated in numerous muscular systems (e.g., An et al., 1981; Anapol & Barry, 1996; Brand et al., 1986; Schumacher, 1961), PCSA can be calculated from cadaveric specimens as a multivariable function of muscle mass, density, and fiber length. To this end, PCSA has been investigated through numerous ecological and behavioral lenses, such as the relationship between diet and bite force (Becerra et al., 2014; Deutsch et al., 2020; Hartstone‐Rose et al., 2012; Hartstone‐Rose et al., 2019a; Hartstone‐Rose et al., 2022; Herrel et al., 2008; Perry et al., 2011; Taylor & Vinyard, 2009), or between limb forces and locomotor mode (Leischner et al., 2018; Marchi et al., 2018; Martin et al., 2019; Michilsens et al., 2009). Several attempts have also been made to quantify age‐related changes to muscle PCSA across myriad taxa, including the effects of both ontogeny and senescence (Boettcher et al., 2020; Dickinson, Fitton, & Kupczik, 2018; Law et al., 2016; Leonard et al., 2020).
1.3. Dietary correlates of jaw adductor PCSA
Feeding is a universal animal behavior that provides the energy needed for life. From an anatomical perspective, bite force represents a key constraint upon dietary selection by restricting potential foods on the basis of their mechanical resistance. A species' bite force is primarily driven by the PCSA of its jaw adductor musculature (though the configuration of the skull may modulate the mechanical efficiency of biting by altering the lever arms of masticatory muscles; see Radinsky, 1981; Greaves, 1983; Greaves, 2012), a critical performance metric that is understood to experience strong adaptive pressures. Accordingly, the overarching hypothesis that species exploiting mechanically challenging diets should exhibit a corresponding increase in jaw adductor PCSA has been explored in numerous vertebrate lineages.
A positive association between dietary hardness and jaw adductor PCSA has been reported in numerous analyses of the bat masticatory apparatus, including both intra‐familial and cross‐order samples (Herrel et al., 2008; Santana et al., 2010). Bats are among the most dietarily diverse mammalian clades, spanning insectivory, frugivory, nectarivory, carnivory, and sanguivory. Among these groups, carnivorous and hard‐fruit specialist frugivores exhibited the greatest relative PCSA values, whereas liquid feeders (e.g., nectarivores and sanguivores) demonstrated lower bite force potential (Santana et al., 2010). Musteloids—a similarly diverse superfamily that includes carnivorous weasels, the frugivorous kinkajou, insectivorous skunks and the durophagous red panda—also show significantly greater jaw adductor PCSAs among obdurate‐feeding taxa (Hartstone‐Rose et al., 2019b; Hartstone‐Rose et al., 2022).
Functional signals are also reported in other aspects of jaw use. For instance, among raptorial birds, total jaw adductor PCSA is significantly greater in falcons (a lineage that kill prey using their beak) relative to hawks (who primarily kill prey using their talons). Similarly, among rodents, subterranean tooth‐diggers show greater jaw adductor PCSAs than either terrestrial or non‐digging fossorial taxa (Becerra et al., 2014).
However, this functional relationship is not observed within every lineage. Several carnivoran families, including both felids and canids, show no clear relationship between dietary mechanical resistance and bite force (Hartstone‐Rose et al., 2012; Hartstone‐Rose et al., 2022). Conflicting reports are also found within primates. Among callitrichids, tree‐gouging marmosets show increased jaw adductor PCSAs relative to non‐gouging tamarins (Taylor et al., 2009; Taylor & Vinyard, 2004). Meanwhile, the tufted capuchin—a species that consumes mechanically challenging foods—shows an increase in temporalis, but not masseter, PCSA relative to non‐obdurate feeding members of its genus (Taylor & Vinyard, 2009). However, broader‐sample studies (e.g., across suborders, or spanning the primate order as a whole) report no significant differences in jaw adductor PCSA between taxa that exploit obdurate versus mechanically‐non‐challenging diets (Deutsch et al., 2020; Hartstone‐Rose et al., 2018).
Form‐function relationships within the feeding system of extant animals have also been used to reconstruct feeding behaviors within the fossil record. Indeed, within strepsirrhines strong positive correlations (r 2 = 0.61–0.86) have been demonstrated between temporalis, masseter and medial pterygoid PCSA against each muscle's corresponding areas of origination and insertion on the cranium and mandible, respectively (Perry, 2018). Similarly positive relationships between PCSA and various bony proxies have also been demonstrated in carnivorans, though stronger associations—particularly within the temporalis—are noted in feliforms relative to caniforms (Dickinson, Davis, et al., 2021). Using such regression equations, origin and insertion areas on morphologically similar fossil taxa can then be used to estimate PCSA within each muscle (Perry & Prufrock, 2018). Reconstructions of bite force within the fossil record are of broad interest in myriad vertebrate lineages (e.g., Bates & Falkingham, 2012; Blanco et al., 2012; Fabre et al., 2018; Grubich et al., 2012; Lautenschlager, 2013; Miller & Pittman, 2021; Perry & Prufrock, 2018; Sakamoto, 2022; St. Clair et al., 2018; Wroe et al., 2005), and as such an increased understanding of muscle anatomy within modern taxa is critical to refining the accuracy of such projections (Perry & Prufrock, 2018).
1.4. Fascicle lengths in the feeding system
Beyond PCSA, other architectural determinants of muscle function (e.g., fascicle lengths) are also frequently examined within a comparative ecological context. As fascicle lengths reflect a muscle's excursion potential, longer fascicles are anticipated in the jaw muscles of species for whom wide jaw gapes are often required. For example, fascicle lengths across the masticatory apparatus are strongly correlated with food size in musteloids (Hartstone‐Rose et al., 2019a; Hartstone‐Rose et al., 2022). Similar associations have been reported in felids (Hartstone‐Rose et al., 2012), canids (Penrose et al., 2020), and potentially ursids (Hartstone‐Rose et al., 2022), wherein small food specialists exhibit relatively short fascicles whereas taxa that consume larger foods possess relatively and absolutely longer muscle fascicles. However, this observation was not substantiated by more recent reevaluation of the jaw muscles across the Order Carnivora (Hartstone‐Rose et al., 2022).
Within primates, strepsirrhine species that habitually consume large foods also show a consistent increase in jaw adductor fascicle lengths relative to non‐specialist taxa (Perry et al., 2011). This finding is equally observed within anthropoids, particularly within the temporalis (Hartstone‐Rose et al., 2018). Similarly, mirroring trends seen in PCSA, marmosets possess longer jaw adductor fascicles than do tamarins—a difference linked to the tree‐gouging behaviors of the former group which necessitates the frequent use of wide‐gape jaw postures (Eng et al., 2009; Taylor & Vinyard, 2004). More recently, both in vivo and in vitro studies have sought to explore changes in primate masticatory fascicle lengths as a consequence of gape during the chewing cycle; showing, for instance, that fibers in the temporalis undergo an increase of length of up to 75% as they stretch from occlusion to maximum gape (Laird et al., 2020). Such studies underscore the critical demands imposed by wide masticatory gapes and help contextualize the widespread adaptations seen in the primate jaw towards habitual, wide‐gape regimes.
Similar relationships have also been probed in the corresponding jaw abductor muscles (i.e., the muscles that open the jaw). Within primates, fascicle lengths within the lateral pterygoid were significantly greater in species that frequently consumed large food items (Dickinson, Pastor, et al., 2021). Similar trends have also been reported in bats, whereby frugivorous noctilionoids show greater fascicle lengths in the digastric that are associated with the need to accommodate large fruits (Curtis & Santana, 2018). Thus, fascicle lengths appear to represent a relatively robust predictor of food sizes, across multiple muscular systems and various phylogenetic groups, and may reflect a more direct dietary signal than that observed in analyses of PCSA.
1.5. Locomotor correlates of muscle architecture
Similar investigations into the ecological and behavioral correlates of muscle architecture have been conducted within the limb musculature, analyzing differences in hand/foot usage and locomotor modes between taxa.
Within raptors, differences in the PCSA of digital flexor muscles reflect gripping strength and have been thought to reflect prey capture strategies. Differences in digital flexor PCSA between talon‐killing hawks and beak‐killing falcons, however, were only significant at smaller (<250 g) body masses, whereafter the two groups converged (Sustaita, 2008). Additionally, no differences are reported in either PCSA or fascicle lengths between the digital flexors of hawks and owls (Ward et al., 2002).
Functional correlates of limb musculature have been most widely studied, however, in primates, wherein strong links have been drawn between locomotor behaviors and muscle anatomy. Gibbons, which practice a highly specialized mode of suspensory brachiation, are shown to exhibit extremely high PCSA values in muscles associated with the flexion of the elbow and wrist (Michilsens et al., 2009). A similar increase in wrist flexor strength is also reported in chimpanzees relative to humans (Thorpe et al., 1999), further highlighting the importance of these muscles among highly arboreal taxa.
Across multiple functional compartments of the forearm, arboreal species of both new world and old world monkeys exhibit consistently greater fascicle lengths than their terrestrial counterparts (Leischner et al., 2018). Within strepsirrhines and tarsiiformes, however, architectural properties within the forearm musculature are highly conservative, showing no strong relationship with either locomotor mode nor preferred substrate type but instead scaling closely with body mass (Gyambibi & Lemelin, 2013). Fascicle lengths have also been shown to correspond poorly with locomotor speed across primates as a whole (Boettcher et al., 2019).
Broad‐sample investigation of the primate hindlimb yielded no significant associations between muscle architectural properties and either substrate type (e.g., arboreality vs. terrestriality) or locomotor mode (Marchi et al., 2018). Similarly, comparative work on the foot and ankle musculature of gibbons and bonobos found striking similarities in architecture between the two taxa that have dramatically different lower limb use, though the muscle architecture of both differed significantly from that of humans (Vereecke et al., 2005). However, that is not to say that muscle architecture within the hindlimb is static. Indeed, as recently shown by Venkataraman et al. (2013), architectural properties within the human gastrocnemius may vary significantly on the basis of loading history: with significantly longer muscle fascicles in both the medial and lateral gastrocnemius head observed in habitually tree‐climbing populations versus their agricultural counterparts.
1.6. Fiber typing
Muscle fiber architecture is not the sole determinant of contractile function within skeletal muscle; rather, both contractile velocity and fatigability are modulated by the histochemical profile of individual fibers within the muscle (Hazimihalis et al., 2013; Kawai et al., 2009; Korfage et al., 2005; Korfage et al., 2006; Rupert et al., 2014; Schiaffino & Reggiani, 1994; Schiaffino & Reggiani, 2011). Fibers have been traditionally classified on the basis of slow‐versus‐fast twitch fiber profiles (e.g., Crow & Kushmerick, 1982; Eberstein & Goodgold, 1968; Okumura et al., 2005), wherein slow type I fibers are associated with slow contractions and high fatigue resistance whereas fast‐type II fibers are characterized by a faster, but more fatigable contractile profile (Korfage et al., 2005; Rowlerson et al., 1983; Schiaffino & Reggiani, 1994). In reality, however, an enormous and diverse spectrum of fiber types exists, a paradigm further complicated by the prevalence of hybridization between multiple isoforms (Bottinelli et al., 1994; Pette & Staron, 1990). Specific anatomical systems may also possess unique variants of myosin: for example, in carnivorans, nonhuman primates, and some chiropterans, a distinct fiber type (MyHC‐M) is observed within the masticatory musculature (Hoh, 2002; Rowlerson et al., 1983), while other taxa (including kangaroos, rabbits, and humans) express cardiac‐type myosin alongside skeletal muscle fiber types within the jaw musculature (Bredman et al., 1991; Hoh et al., 2000; Korfage & Van Eijden, 2000; for a detailed review on this topic please see Schiaffino and Reggiani (2011)).
Just as trends have been established between muscle architecture and muscle function, so too can ecology and behavior be seen to correlate with muscle fiber types. At the broadest scale, differences can be observed in the feeding muscles of grazing ruminants (the profiles of which are generally slow‐contracting; Suzuki, 1977) versus predatory felids that typically express fast‐contracting but fatigable fibers (Rowlerson et al., 1983). However, finer scale differences can also be observed: for instance, within pigeons, leg muscles associated with terrestrial locomotion express higher proportions of slow‐twitch fibers (~20%) than forelimb muscles associated with flight (<1%; Maier, 1983). Similarly, among the closely‐related African great apes, the masticatory muscles of folivorous gorillas express a more fatigue‐resistant profile than frugivorous chimpanzees or bonobos (Taylor & Holmes, 2021). Furthermore, differences in diving behaviors between sperm whales and bottlenose dolphins are manifested in the fiber profiles of epaxial swimming muscles, allowing deep divers to maximize oxygen storage capacity and reduce energetic costs (Kielhorn et al., 2013). Finally, adding to the recent discovery of an additional mimetic muscle in domestic dogs that may improve visual communication with people (Klinkhamer et al., 2019), it has been found that domestic dog mimetic muscles also possess a higher percentage of fast twitch fibers—similar in percentage, in fact, to those found in people (Burrows & Omstead, 2022).
1.7. New frontiers in muscle anatomy
The determination of muscle properties—either architectural or histochemical—typically necessitates the destructive sampling of tissue via gross dissection and either chemical digestion or histological sectioning. Recent innovations within myological imaging, however, have demonstrated the potential for the non‐destructive visualization and reconstruction of muscle anatomy in situ via tomographic techniques. This toolkit is collectively referred to as DiceCT—diffusible, iodine‐based, contrast‐enhanced computed tomography—and uses a staining agent (most frequently the iodine referred to in the acronym, but in some instances phosphotungstic acid, phosphomolybdic acid, or osmium tetroxide) to bind with the glycogen found in muscle fascicles and increase their radioopacity sufficiently as to enable discrimination within CT datasets (Descamps et al., 2014; Gignac et al., 2016; Li et al., 2015; Metscher, 2009). As a non‐destructive and reversible technique, DiceCT facilitates the analysis of specimens that would otherwise be unsuitable for dissection (Early et al., 2020; Lanzetti & Ekdale, 2021; Morhardt & Witmer, 2016), and, importantly, allows the description of muscle gross and fascicular anatomy in situ, maintaining three dimensional relationships heretofore impossible to preserve using traditional dissection techniques (Dickinson et al., 2019; Dickinson et al., 2020). As such, numerous studies over the past decade have applied DiceCT to describe muscle form and illustrate areas of attachment across numerous vertebrate lineages (e.g., Baverstock et al., 2013; Cox & Jeffery, 2011; Holliday et al., 2013; Sahd et al., 2022; Santana, 2018; To et al., 2021).
As iodine binds readily to individual muscle fascicles but not their surrounding collagenous perimysium, several recent studies have demonstrated the applicability of DiceCT to resolving architectural properties of skeletal muscle in situ (Dickinson et al., 2019; Dickinson et al., 2020; Dickinson, Stark, & Kupczik, 2018), and have shown good congruence between fascicle lengths generated via gross dissection versus digital dissection. Increasingly, attempts are also establishing the viability of algorithmic approaches to identifying fascicles within CT datasets, allowing larger numbers to be analyzed with reduced time investment (Dickinson et al., 2022; Dickinson, Stark, & Kupczik, 2018; Holliday et al., 2022; Ratkiewicz et al., 2022; Sullivan et al., 2019). These automated approaches also significantly reduce the potential for human bias in fascicle selection and increase replicability. Indeed, one major benefit of DiceCT approaches in general is the ability for datasets to be shared, replicated, and cross‐analyzed between groups: while it is often impractical for collaborators to share cadaveric specimens, CT datasets can be easily transferred. This benefit also potentially allows for data reuse: for example, a contrast‐enhanced scan used to analyze masticatory muscle tissues may be used years later by researchers interested in extraocular or mimetic muscles with greater ease than might be accomplished through traditional physical dissection of even the best‐preserved fixed specimens. DiceCT techniques also make more accessible the anatomy of deep and hard‐to‐access systems such as the hyolingual musculature (Orsbon et al., 2018). As such, the emergence of DiceCT as a reliable analytical toolkit promises to greatly expand the frontiers of comparative myological study and, as scanning resolution improves and costs continue to decline, looks likely to assume an even greater role within the anatomical literature: both as a standalone toolkit, and in coordination with in vivo (e.g., X‐ray reconstruction of moving morphology or corollary fluoromicrometry; Brainerd et al., 2010; Camp et al., 2016; Orsbon et al., 2018) and in silico (e.g., multibody dynamics analysis; Curtis, 2011) approaches to capturing and reconstructing musculoskeletal kinematics.
1.8. The impact of Kurt Albertine's leadership of The Anatomical Record on myological research
Myological research has evolved enormously over the last couple of decades, and the impact of Kurt Albertine's leadership of The Anatomical Record on this evolution cannot be overstated. Of the papers cited in this overview of functional myology from gross anatomical description to fascicle architecture analysis and fiber type, more than two dozen were published in the journal during his reign as Editor in Charge. And these citations are in no way exhaustive. They do not include the dozens of papers on muscle cell biology and physiology—many of which relied on rodent models (e.g., Baum et al., 2017; Deschenes et al., 2015; Haidarliu et al., 2010; Hesse et al., 2010). There are dozens of other AR myological papers from this era including traditional gross anatomical descriptions. For instance, Fisher et al. (2007) document the forelimb muscles of pygmy hippopotamuses, Carlon and Hubbard (2012) write about the hip and thigh muscles of clouded leopards, Kawashima et al. (2015) write about the shoulder girdle muscles of pangolins and armadillos and a pair of papers (Tomo et al., 2007; Warburton, 2009) document the masticatory muscles of kangaroos and wallabies. During this time, other authors wrote about muscle anatomy in flying squirrels (Kawashima et al., 2017), carnivorous marsupials (Warburton & Marchal, 2017), cows (Gilbert et al., 2006), horses (Meyers & Hermanson, 2006), goats (Elsalanty et al., 2007), alpacas (Williams et al., 2010), moles (Ichikawa et al., 2019), frogs (Lagorio et al., 2020), birds of prey (Bribiesca‐Contreras et al., 2019), pigeons (Liang et al., 2018), and geese (Jackowiak et al., 2011). Many of these are classic anatomical descriptions that harken back to the foundations of the field of comparative anatomy; papers that focus on individual species or even individual muscles and variation therein—attracted to the journal perhaps because of its dedication to unlimited imagery to best document what to some are anatomical minutia, but to others are the foundations of whole careers documenting evolution and functional morphology and adaptive radiation. The journal still takes pride in publishing these examples of “pure science”—true examples of an “Anatomical Record” clearly encouraged under Albertine's leadership.
Furthermore, although there are more specialized discipline‐specific journals, colleagues from other fields submitted important papers to the journal during the Albertine era, again, in part because of the journal's unparalleled emphasis on anatomical documentation. For instance, many of our anthropology (e.g., Burrows et al., 2014; Gyambibi & Lemelin, 2013; Organ et al., 2009) colleagues published myological studies in The Anatomical Record and among the many papers on dinosaur biology included in the journal during Albertine's time, at several (e.g., Klinkhamer et al., 2018; Klinkhamer et al., 2019; Nabavizadeh, 2016; Nabavizadeh, 2020a, 2020b; Snively & Russell, 2007; Toledo et al., 2015) were myological reconstructions. Because so many of the paleontological journals focus almost exclusively on taxonomy and systematics, true anatomical analyses of fossils, especially those beyond osteological description, have become almost a subspecialty of the journal, as emphasized by the two Special Issues focusing on dinosaur anatomy that were published under Kurt's leadership—many papers from which focused on myology and have been cited in this review. This legacy continues with a third Anatomical Record Special Issue on dinosaurs nearing completion.
The flourishing of myological research in the journal under Albertine was personally important for both of us. As a result of The Anatomical Record's dedication to thorough documentation of anatomical form and function—for instance allowing and even encouraging unlimited figures during an era when other journals were either limiting figure count, or requiring additional publication fees for their inclusion—this journal was where author AHR chose to publish the collated and expanded research that grew out of our symposium in the 2016 International Congress of Vertebrate Morphology. That effort, edited collaboratively with Sharlene Santana and Damiano Marchi, resulted in a double issue of the journal (Figure 1), including one of the first published manuscripts by author ED.
FIGURE 1.

The covers of the 2018 Anatomical Record special issues on functional myology guest edited by Hartstone‐Rose, Santana and Marchi, and featuring one of Dickinson's first published papers.
Years before our special issues, Albertine oversaw the special issue coedited by Jean and Joseph Sanger (2014; Figure 2), and wrote its forward with Cynthia Jensen (Albertine & Jensen, 2014) about advances in myological cellular biology and physiology. Thanks to Albertine's commitment to this kind of work, continued under his wonderful successor, Heather Smith, The Anatomical Record has been, and continues to be, a leading source of myological research and one of the first places our colleagues look to publish their work. For this reason and many others, we are grateful for the efforts of our colleague, former leader and continuing mentor, Kurt Albertine.
FIGURE 2.

Cover of the special issue guest edited by Sanger and Sanger (2014) and under the leadership of Albertine.
AUTHOR CONTRIBUTIONS
Edwin Dickinson: Conceptualization; investigation; resources; writing – original draft; writing – review and editing. Adam Hartstone‐Rose: Conceptualization; investigation; project administration; resources; writing – original draft; writing – review and editing.
ACKNOWLEDGMENTS
We are grateful for the invitation to submit this manuscript extended to us by Katherine Yutzey, Lisa Joss‐Moore and Mary “Jane” Black, for the continued leadership of these outstanding special issues by Jeff Laitman under the direction of Heather Smith—who honors Kurt's leadership by furthering the journal's excellent editorial standards and direction along many of the lines that he emphasized. We also thank our anonymous reviewer and Jonathan Perry for both a valuable review and insightful discussion of the first version of the manuscript. And, of course, we are most grateful to Kurt Albertine himself. On a personal note, I (Adam Hartstone‐Rose) came of age professionally, during Kurt's leadership of the journal and so much of my favorite work was shepherded into the world through him and his deputies. I truly learned to refine my approach to science and speak to colleagues through their mentorship and am honored both to have been asked to join the editorial board to, in part, help continue this legacy of mentoring young scholars in our field and to have been given the opportunity to coauthor this piece to say “thank you” to the man himself. Neither would we be the scholars that we are today if it were not for The Anatomical Record under Kurt's direction, nor would myological research have come as far or been as elegantly depicted and curated if it had not found this home under his leadership.
Dickinson, E. , & Hartstone‐Rose, A. (2025). Behavioral correlates of fascicular organization: The confluence of muscle architectural anatomy and function. The Anatomical Record, 308(4), 1265–1277. 10.1002/ar.25187
REFERENCES
- Albertine, K. H. , & Jensen, C. (2014). Special issue: Recent advances in muscle research. The Anatomical Record, 297, 1537–1538. [DOI] [PubMed] [Google Scholar]
- An, K.‐N. , Hui, F. , Morrey, B. F. , Linscheid, R. L. , & Chao, E. Y. (1981). Muscles across the elbow joint: A biomechanical analysis. Journal of Biomechanics, 14, 659–669. [DOI] [PubMed] [Google Scholar]
- Anapol, F. , & Barry, K. (1996). Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons. American Journal of Physical Anthropology, 99, 429–447. [DOI] [PubMed] [Google Scholar]
- Bates, K. T. , & Falkingham, P. L. (2012). Estimating maximum bite performance in tyrannosaurus rex using multi‐body dynamics. Biology Letters, 8, 660–664. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baum, O. , Jentsch, L. , Odriozola, A. , Tschanz, S. A. , & Olfert, I. M. (2017). Ultrastructure of skeletal muscles in mice lacking muscle‐specific VEGF expression. The Anatomical Record, 300, 2239–2249. [DOI] [PubMed] [Google Scholar]
- Baverstock, H. , Jeffery, N. S. , & Cobb, S. N. (2013). The morphology of the mouse masticatory musculature. Journal of Anatomy, 223, 46–60. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Becerra, F. , Echeverría, A. I. , Casinos, A. , & Vassallo, A. I. (2014). Another one bites the dust: Bite force and ecology in three caviomorph rodents (Rodentia, Hystricognathi). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 321, 220–232. [DOI] [PubMed] [Google Scholar]
- Blanco, R. E. , Rinderknecht, A. , & Lecuona, G. (2012). The bite force of the largest fossil rodent (Hystricognathi, Caviomorpha, Dinomyidae). Lethaia, 45, 157–163. [Google Scholar]
- Boettcher, M. L. , Leonard, K. C. , Dickinson, E. , Aujard, F. , Herrel, A. , & Hartstone‐Rose, A. (2020). The forearm musculature of the gray mouse lemur (Microcebus murinus): An ontogenetic study. The Anatomical Record, 303, 1354–1363. [DOI] [PubMed] [Google Scholar]
- Boettcher, M. L. , Leonard, K. C. , Dickinson, E. , Herrel, A. , & Hartstone‐Rose, A. (2019). Extraordinary grip strength and specialized myology in the hyper‐derived hand of Perodicticus potto? Journal of Anatomy, 235, 931–939. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bottinelli, R. , Betto, R. , Schiaffino, S. , & Reggiani, C. (1994). Maximum shortening velocity and coexistence of myosin heavy chain isoforms in single skinned fast fibres of rat skeletal muscle. Journal of Muscle Research & Cell Motility, 15, 413–419. [DOI] [PubMed] [Google Scholar]
- Brainerd, E. L. , Baier, D. B. , Gatesy, S. M. , Hedrick, T. L. , Metzger, K. A. , Gilbert, S. L. , & Crisco, J. J. (2010). X‐ray reconstruction of moving morphology (XROMM): Precision, accuracy and applications in comparative biomechanics research. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 313A, 262–279. [DOI] [PubMed] [Google Scholar]
- Brand, R. A. , Pedersen, D. R. , & Friederich, J. A. (1986). The sensitivity of muscle force predictions to changes in physiologic cross‐sectional area. Journal of Biomechanics, 19, 589–596. [DOI] [PubMed] [Google Scholar]
- Bredman, J. , Wessels, A. , Weijs, W. , Korfage, J. , Soffers, C. , & Moorman, A. (1991). Demonstration of ‘cardiac‐specific’ myosin heavy chain in masticatory muscles of human and rabbit. The Histochemical Journal, 23, 160–170. [DOI] [PubMed] [Google Scholar]
- Bribiesca‐Contreras, F. , Parslew, B. , & Sellers, W. I. (2019). A quantitative and comparative analysis of the muscle architecture of the forelimb myology of diurnal birds of prey (order Accipitriformes and Falconiformes). The Anatomical Record, 302, 1808–1823. [DOI] [PubMed] [Google Scholar]
- Burkholder, T. J. , & Lieber, R. L. (2001). Sarcomere length operating range of vertebrate muscles during movement. Journal of Experimental Biology, 204, 1529–1536. [DOI] [PubMed] [Google Scholar]
- Burrows, A. M. , Durham, E. L. , Matthews, L. C. , Smith, T. D. , & Parr, L. A. (2014). Of mice, monkeys, and men: Physiological and morphological evidence for evolutionary divergence of function in mimetic musculature. The Anatomical Record, 297, 1250–1261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burrows, A. M. , & Omstead, K. M. (2022). Dog faces are faster than wolf faces. The FASEB Journal, 36. [Google Scholar]
- Camp, A. L. , Astley, H. C. , Horner, A. M. , Roberts, T. J. , & Brainerd, E. L. (2016). Fluoromicrometry: A method for measuring muscle length dynamics with biplanar videofluoroscopy. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 325, 399–408. [DOI] [PubMed] [Google Scholar]
- Carlon, B. , & Hubbard, C. (2012). Hip and thigh anatomy of the clouded leopard (Neofelis nebulosa) with comparisons to the domestic cat (Felis catus). The Anatomical Record, 295, 577–589. [DOI] [PubMed] [Google Scholar]
- Chauveau, A. , & Arloing, S. (1885). The comparative anatomy of the domesticated animals. D. Appleton & Co. [Google Scholar]
- Cole, F. (1949). A history of comparative anatomy from Aristotle to the eighteenth century. Macmillan and Co. [Google Scholar]
- Cole, F. J. , & Eales, N. B. (1917). The history of comparative anatomy: Part I.—A statistical analysis of the literature. Science Progress, 11, 578–596. [Google Scholar]
- Cosans, C. E. , & Frampton, M. (2015). History of comparative anatomy. eLS, 1–8. [Google Scholar]
- Cox, P. G. , & Jeffery, N. (2011). Reviewing the morphology of the jaw‐closing musculature in squirrels, rats, and Guinea pigs with contrast‐enhanced microCT. The Anatomical Record, 294, 915–928. [DOI] [PubMed] [Google Scholar]
- Crow, M. T. , & Kushmerick, M. J. (1982). Chemical energetics of slow‐and fast‐twitch muscles of the mouse. The Journal of General Physiology, 79, 147–166. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Curtis, A. , & Santana, S. E. (2018). Jaw‐dropping: Functional variation in the digastric muscle in bats. The Anatomical Record, 301, 279–290. [DOI] [PubMed] [Google Scholar]
- Curtis, N. (2011). Craniofacial biomechanics: An overview of recent multibody modelling studies. Journal of Anatomy, 218, 16–25. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Darwin, C. (1859). The origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray. [PMC free article] [PubMed] [Google Scholar]
- Descamps, E. , Sochacka, A. , De Kegel, B. , Van Loo, D. , Van Hoorebeke, L. , & Adriaens, D. (2014). Soft tissue discrimination with contrast agents using micro‐CT scanning. Belgian Journal of Zoology, 144, 20–40. [Google Scholar]
- Deschenes, M. , Haidarliu, S. , Demers, M. , Moore, J. , Kleinfeld, D. , & Ahissar, E. (2015). Muscles involved in naris dilation and nose motion in rat. The Anatomical Record, 298, 546–553. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deutsch, A. R. , Dickinson, E. , Leonard, K. C. , Pastor, F. , Muchlinski, M. N. , & Hartstone‐Rose, A. (2020). Scaling of anatomically derived maximal bite force in primates. The Anatomical Record, 303, 2026–2035. [DOI] [PubMed] [Google Scholar]
- Dickinson, E. , Basham, C. , Rana, A. , & Hartstone‐Rose, A. (2019). Visualization and quantification of digitally dissected muscle fascicles in the masticatory muscles of Callithrix jacchus using nondestructive DiceCT. The Anatomical Record, 302, 1891–1900. [DOI] [PubMed] [Google Scholar]
- Dickinson, E. , Davis, J. S. , Deutsch, A. R. , Patel, D. , Nijhawan, A. , Patel, M. , Blume, A. , Gannon, J. L. , Turcotte, C. M. , Walker, C. S. , & Hartstone‐Rose, A. (2021). Evaluating bony predictors of bite force across the order Carnivora. Journal of Morphology, 282, 1499–1513. [DOI] [PubMed] [Google Scholar]
- Dickinson, E. , Fitton, L. C. , & Kupczik, K. (2018). Ontogenetic changes to muscle architectural properties within the jaw‐adductor musculature of Macaca fascicularis . American Journal of Physical Anthropology, 167, 291–310. [DOI] [PubMed] [Google Scholar]
- Dickinson, E. , Kolli, S. , Schwenk, A. , Davis, C. E. , & Hartstone‐Rose, A. (2020). DiceCT analysis of the extreme gouging adaptations within the masticatory apparatus of the aye‐aye (Daubentonia madagascariensis). The Anatomical Record, 303, 282–294. [DOI] [PubMed] [Google Scholar]
- Dickinson, E. , Pastor, F. , Santana, S. E. , & Hartstone‐Rose, A. (2021). Functional and ecological correlates of the primate jaw abductors. The Anatomical Record, 305, 1245–1263. [DOI] [PubMed] [Google Scholar]
- Dickinson, E. , Ratkiewicz, A. , Hartstone‐Rose, A. , Granatosky, M. , & Molnar, J. (2022). Automating the quantification of muscle architectural properties from tomographic datasets. Tomography for Scientific Advancement. [Google Scholar]
- Dickinson, E. , Stark, H. , & Kupczik, K. (2018). Non‐destructive determination of muscle architectural variables through the use of DiceCT. The Anatomical Record, 301, 363–377. [DOI] [PubMed] [Google Scholar]
- Early, C. M. , Morhardt, A. C. , Cleland, T. P. , Milensky, C. M. , Kavich, G. M. , & James, H. F. (2020). Chemical effects of diceCT staining protocols on fluid‐preserved avian specimens. PLoS One, 15, e0238783. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eberstein, A. , & Goodgold, J. (1968). Slow and fast twitch fibers in human skeletal muscle. American Journal of Physiology, 215, 535–541. [DOI] [PubMed] [Google Scholar]
- Edman, K. (1966). The relation between sarcomere length and active tension in isolated semitendinosus fibres of the frog. The Journal of Physiology, 183, 407–417. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elsalanty, M. , Makarov, M. , Cherkashin, A. , Birch, J. , & Samchukov, M. (2007). Changes in pennate muscle architecture after gradual tibial lengthening in goats. The Anatomical Record, 290, 461–467. [DOI] [PubMed] [Google Scholar]
- Eng, C. M. , Ward, S. R. , Vinyard, C. J. , & Taylor, A. B. (2009). The mechanics of the masticatory apparatus facilitate muscle force production at wide jaw gapes in tree‐gouging marmosets (Callithrix jacchus). Journal of Experimental Biology, 212, 4040–4055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fabre, A.‐C. , Perry, J. , Hartstone‐Rose, A. , Lowie, A. , Boens, A. , & Dumont, M. (2018). Do muscles constrain skull shape evolution in strepsirrhines? Anatomical Record, 301, 291–310. [DOI] [PubMed] [Google Scholar]
- Fisher, H. I. (1946). Adaptations and comparative anatomy of the locomotor apparatus of New World vultures. The American Midland Naturalist, 35, 545–727. [Google Scholar]
- Fisher, R. E. , Scott, K. M. , & Naples, V. L. (2007). Forelimb myology of the pygmy hippopotamus (Choeropsis liberiensis). The Anatomical Record, 290, 673–693. [DOI] [PubMed] [Google Scholar]
- Gans, C. (1982). Fiber architecture and muscle function. Exercise and Sport Sciences Reviews, 10, 160–207. [PubMed] [Google Scholar]
- Gans, C. , & Bock, W. J. (1965). The functional significance of muscle architecture ‐ a theoretical analysis. Ergebnisse der Anatomie Und Entwicklungsgeschichte, 38, 115–142. [PubMed] [Google Scholar]
- Gans, C. , & de Vree, F. (1987). Functional bases of fiber length and angulation in muscle. Journal of Morphology, 192, 62–85. [DOI] [PubMed] [Google Scholar]
- Gans, C. , & Gaunt, A. S. (1991). Muscle architecture in relation to function. Journal of Biomechanics, 24, 53–65. [DOI] [PubMed] [Google Scholar]
- Gignac, P. M. , Kley, N. J. , Clarke, J. A. , Colbert, M. W. , Morhardt, A. C. , Cerio, D. , Cost, I. N. , Cox, P. G. , Daza, J. D. , Early, C. M. , Echols, M. , Henkelman, R. , Herdina, A. , Holliday, C. , Mahlow, Z. , Merchant, S. , Müller, J. , Orsbon, C. , Paluh, D. , … Witmer, L. M. (2016). Diffusible iodine‐based contrast‐enhanced computed tomography (diceCT): An emerging tool for rapid, high‐resolution, 3‐D imaging of metazoan soft tissues. Journal of Anatomy, 228, 889–909. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilbert, R. J. , Wedeen, V. J. , Magnusson, L. H. , Benner, T. , Wang, R. P. , Dai, G. , Napadow, V. J. , & Roche, K. K. (2006). Three‐dimensional myoarchitecture of the bovine tongue demonstrated by diffusion spectrum magnetic resonance imaging with tractography. The Anatomical Record Part A, 288A, 1173–1182. [DOI] [PubMed] [Google Scholar]
- Goldspink, G. (1968). Sarcomere length during post‐natal growth of mammalian muscle fibres. Journal of Cell Science, 3, 539–548. [DOI] [PubMed] [Google Scholar]
- Gordon, A. , Huxley, A. F. , & Julian, F. (1966). The variation in isometric tension with sarcomere length in vertebrate muscle fibres. The Journal of Physiology, 184, 170–192. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Greaves, W. S. (1983). A functional analysis of carnassial biting. Biological Journal of the Linnean Society, 20, 353–363. [Google Scholar]
- Greaves, W. S. (2012). The Mammalian Jaw: A Mechanical Analysis. Cambridge: Cambridge University Press. [Google Scholar]
- Grubich, J. R. , Huskey, S. , Crofts, S. , Orti, G. , & Porto, J. (2012). Mega‐bites: Extreme jaw forces of living and extinct piranhas (Serrasalmidae). Scientific Reports, 2, 9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gyambibi, A. , & Lemelin, P. (2013). Comparative and quantitative myology of the forearm and hand of prosimian primates. The Anatomical Record, 296, 1196–1206. [DOI] [PubMed] [Google Scholar]
- Haidarliu, S. , Simony, E. , Golomb, D. , & Ahissar, E. (2010). Muscle architecture in the Mystacial pad of the rat. The Anatomical Record, 293, 1192–1206. [DOI] [PubMed] [Google Scholar]
- Hartstone‐Rose, A. , Deutsch, A. R. , Leischner, C. L. , & Pastor, F. (2018). Dietary correlates of primate masticatory muscle fiber architecture. The Anatomical Record, 301, 311–324. [DOI] [PubMed] [Google Scholar]
- Hartstone‐Rose, A. , Dickinson, E. , Deutsch, A. R. , Worden, N. , & Hirschkorn, G. A. (2022). Masticatory muscle architectural correlates of dietary diversity in Canidae, Ursidae, and across the order Carnivora. The Anatomical Record, 305, 477–497. [DOI] [PubMed] [Google Scholar]
- Hartstone‐Rose, A. , Hertzig, I. , & Dickinson, E. (2019a). Bite force and masticatory muscle architecture adaptations in the dietarily diverse Musteloidea. The Anatomical Record, 302, 2287–2299. [DOI] [PubMed] [Google Scholar]
- Hartstone‐Rose, A. , Hertzig, I. , & Dickinson, E. (2019b). Bite force and masticatory muscle architecture adaptations in the Dietarily diverse Musteloidea (Carnivora). The Anatomical Record, 302, 2287–2299. [DOI] [PubMed] [Google Scholar]
- Hartstone‐Rose, A. , Perry, J. , & Morrow, C. J. (2012). Bite force estimation and the fiber architecture of felid masticatory muscles. Anatomical Record, 295, 1336–1351. [DOI] [PubMed] [Google Scholar]
- Hazimihalis, P. J. , Gorvet, M. A. , & Butcher, M. T. (2013). Myosin isoform fiber type and fiber size in the tail of the Virginia Opossum (Didelphis virginiana). The Anatomical Record, 296, 96–107. [DOI] [PubMed] [Google Scholar]
- Herrel, A. , De Smet, A. , Aguirre, L. F. , & Aerts, P. (2008). Morphological and mechanical determinants of bite force in bats: Do muscles matter? Journal of Experimental Biology, 211, 86–91. [DOI] [PubMed] [Google Scholar]
- Hesse, B. , Fischer, M. S. , & Schilling, N. (2010). Distribution pattern of muscle fiber types in the perivertebral musculature of two different sized species of mice. The Anatomical Record, 293, 446–463. [DOI] [PubMed] [Google Scholar]
- Hoh, J. F. , Kim, Y. , Sieber, L. G. , Zhong, W. W. , & Lucas, C. A. (2000). Jaw‐closing muscles of kangaroos express α‐cardiac myosin heavy chain. Journal of Muscle Research & Cell Motility, 21, 673–680. [DOI] [PubMed] [Google Scholar]
- Hoh, J. F. Y. (2002). 'Superfast' or masticatory myosin and the evolution of jaw‐closing muscles of vertebrates. The Journal of Experimental Biology, 205, 2203–2210. [DOI] [PubMed] [Google Scholar]
- Holliday, C. M. , Sellers, K. C. , Lessner, E. J. , Middleton, K. M. , Cranor, C. , Verhulst, C. D. , Lautenschlager, S. , Bader, K. , Brown, M. A. , & Colbert, M. W. (2022). New frontiers in imaging, anatomy, and mechanics of crocodylian jaw muscles. The Anatomical Record, 305, 3016–3030. [DOI] [PubMed] [Google Scholar]
- Holliday, C. M. , Tsai, H. P. , Skiljan, R. J. , George, I. D. , & Pathan, S. (2013). A 3D interactive model and atlas of the jaw musculature of Alligator mississippiensis. PLoS One, 8, e62806. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Howell, A. B. (1926). Anatomy of the wood rat: Comparative anatomy of the subgenera of the American wood rat (genus Neotoma). Williams & Wilkins. [Google Scholar]
- Huber, E. (1930). Evolution of facial musculature and cutaneous field of trigeminus. The Quarterly Review of Biology Part I, 5, 133–188. [Google Scholar]
- Ichikawa, H. , Matsuo, T. , Higurashi, Y. , Nagahisa, H. , Miyata, H. , Sugiura, T. , & Wada, N. (2019). Characteristics of muscle fiber‐type distribution in moles. The Anatomical Record, 302, 1010–1023. [DOI] [PubMed] [Google Scholar]
- Jackowiak, H. , Skieresz‐Szewczyk, K. , Godynicki, S. , Iwasaki, S. , & Meyer, W. (2011). Functional morphology of the tongue in the domestic goose (Anser Anser f. Domestica). The Anatomical Record, 294, 1574–1584. [DOI] [PubMed] [Google Scholar]
- Kawai, M. , Minami, Y. , Sayama, Y. , Kuwano, A. , Hiraga, A. , & Miyata, H. (2009). Muscle fiber population and biochemical properties of whole body muscles in thoroughbred horses. The Anatomical Record, 292, 1663–1669. [DOI] [PubMed] [Google Scholar]
- Kawashima, T. , Thorington, R. W. , Bohaska, P. W. , Chen, Y. J. , & Sato, F. (2015). Anatomy of shoulder girdle muscle modifications and walking adaptation in the scaly Chinese pangolin (Manis Pentadactyla Pentadactyla: Pholidota) compared with the partially Osteoderm‐clad armadillos (Dasypodidae). The Anatomical Record, 298, 1217–1236. [DOI] [PubMed] [Google Scholar]
- Kawashima, T. , Thorington, R. W. , Bohaska, P. W. , & Sato, F. (2017). Evolutionary transformation of the palmaris longus muscle in flying squirrels (Pteromyini: Sciuridae): An anatomical consideration of the origin of the uniquely specialized Styliform cartilage. The Anatomical Record, 300, 340–352. [DOI] [PubMed] [Google Scholar]
- Kielhorn, C. E. , Dillaman, R. M. , Kinsey, S. T. , McLellan, W. A. , Mark Gay, D. , Dearolf, J. L. , & Ann, P. D. (2013). Locomotor muscle profile of a deep (Kogia breviceps) versus shallow (Tursiops truncatus) diving cetacean. Journal of Morphology, 274, 663–675. [DOI] [PubMed] [Google Scholar]
- Klinkhamer, A. J. , Mallison, H. , Poropat, S. F. , Sinapius, G. H. K. , & Wroe, S. (2018). Three‐dimensional musculoskeletal modeling of the Sauropodomorph hind limb: The effect of postural change on muscle leverage. The Anatomical Record, 301, 2145–2163. [DOI] [PubMed] [Google Scholar]
- Klinkhamer, A. J. , Mallison, H. , Poropat, S. F. , Sloan, T. , & Wroe, S. (2019). Comparative three‐dimensional moment arm analysis of the sauropod forelimb: Implications for the transition to a wide‐gauge stance in Titanosaurs. The Anatomical Record, 302, 794–817. [DOI] [PubMed] [Google Scholar]
- Korfage, J. A. , Koolstra, J. H. , Langenbach, G. E. , & Van Eijden, T. M. (2005). Fiber‐type composition of the human jaw muscles—(part 1) origin and functional significance of fiber‐type diversity. Journal of Dental Research, 84, 774–783. [DOI] [PubMed] [Google Scholar]
- Korfage, J. A. , & Van Eijden, T. M. (2000). Myosin isoform composition of the human medial and lateral pterygoid muscles. Journal of Dental Research, 79, 1618–1625. [DOI] [PubMed] [Google Scholar]
- Korfage, J. A. M. , Van Wessel, T. , Langenbach, G. E. J. , & Van Eijden, T. (2006). Heterogeneous postnatal transitions in myosin heavy chain isoforms within the rabbit temporalis muscle. The Anatomical Record Part A, 288A, 1095–1104. [DOI] [PubMed] [Google Scholar]
- Lagorio, A. D. , Grewal, K. , Djuhari, S. , Le, K. , Mulhim, R. , & Gridi‐Papp, M. (2020). The Arylabialis muscle of the Tungara frog (Engystomops pustulosus). The Anatomical Record, 303, 1966–1976. [DOI] [PubMed] [Google Scholar]
- Laird, M. F. , Granatosky, M. C. , Taylor, A. B. , & Ross, C. F. (2020). Muscle architecture dynamics modulate performance of the superficial anterior temporalis muscle during chewing in capuchins. Scientific Reports, 10, 13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lamarck, J.‐B. (1809). Philosophie Zoologique. Musee d'Histoire Naturelle. [Google Scholar]
- Lang, A. (1896). Textbook of comparative anatomy. Macmillan and Company. [Google Scholar]
- Lanzetti, A. , & Ekdale, E. G. (2021). Enhancing CT imaging: A safe protocol to stain and de‐stain rare fetal museum specimens using diffusible iodine‐based staining (diceCT). Journal of Anatomy, 239, 228–241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lautenschlager, S. (2013). Cranial myology and bite force performance of Erlikosaurus andrewsi: A novel approach for digital muscle reconstructions. Journal of Anatomy, 222, 260–272. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Law, C. J. , Young, C. , & Mehta, R. S. (2016). Ontogenetic scaling of theoretical bite force in southern sea otters (Enhydra lutris nereis). Physiological and Biochemical Zoology, 89, 347–363. [DOI] [PubMed] [Google Scholar]
- Leischner, C. , Crouch, M. , Allen, K. , Marchi, D. , Pastor, F. , & Hartstone‐Rose, A. (2018). Scaling of primate forearm muscle architecture as it relates to locomotion and posture. The Anatomical Record, 301, 484–495. [DOI] [PubMed] [Google Scholar]
- Leonard, K. C. , Boettcher, M. L. , Dickinson, E. , Malhotra, N. , Aujard, F. , Herrel, A. , & Hartstone‐Rose, A. (2020). The ontogeny of masticatory muscle architecture in Microcebus murinus . The Anatomical Record, 303, 1364–1373. [DOI] [PubMed] [Google Scholar]
- Li, Z. , Clarke, J. A. , Ketcham, R. A. , Colbert, M. W. , & Yan, F. (2015). An investigation of the efficacy and mechanism of contrast‐enhanced X‐ray computed tomography utilizing iodine for large specimens through experimental and simulation approaches. BMC Physiology, 15, 5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liang, X. X. , Yu, J. L. , Wang, H. , & Zhang, Z. H. (2018). Post‐hatching growth of the pectoralis muscle in pigeon and its functional implications. The Anatomical Record, 301, 1564–1569. [DOI] [PubMed] [Google Scholar]
- Lieber, R. , Yeh, Y. , & Baskin, R. (1984). Sarcomere length determination using laser diffraction. Effect of beam and fiber diameter. Biophysical Journal, 45, 1007–1016. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lieber, R. L. (1986). Skeletal muscle adaptability. I: Review of basic properties. Developmental Medicine & Child Neurology, 28, 390–397. [DOI] [PubMed] [Google Scholar]
- Lieber, R. L. , & Fridén, J. (2000). Functional and clinical significance of skeletal muscle architecture. Muscle & Nerve, 23, 1647–1666. [DOI] [PubMed] [Google Scholar]
- Lieber, R. L. , & Ward, S. R. (2011). Skeletal muscle design to meet functional demands. Philosophical Transactions of the Royal Society of London B, 366, 1466–1476. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lones, T. (1912). Aristotle's researches in natural science. West, Newman and Co. [Google Scholar]
- Maier, A. (1983). Difference in muscle spindle structure between pigeon muscles used in aerial and terrestrial locomotion. American Journal of Anatomy, 168, 27–36. [DOI] [PubMed] [Google Scholar]
- Marchi, D. , Leischner, C. L. , Pastor, F. , & Hartstone‐Rose, A. (2018). Leg muscle architecture in primates and its correlation with locomotion patterns. The Anatomical Record, 301, 515–527. [DOI] [PubMed] [Google Scholar]
- Martin, M. L. , Travouillon, K. J. , Sherratt, E. , Fleming, P. A. , & Warburton, N. M. (2019). Covariation between forelimb muscle anatomy and bone shape in an Australian scratch‐digging marsupial: Comparison of morphometric methods. Journal of Morphology, 280, 1900–1915. [DOI] [PubMed] [Google Scholar]
- Maughan, R. , Watson, J. , & Weir, J. (1983). Strength and cross‐sectional area of human skeletal muscle. The Journal of Physiology, 338, 37–49. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Metscher, B. D. (2009). MicroCT for comparative morphology: Simple staining methods allow high‐contrast 3D imaging of diverse non‐mineralized animal tissues. BMC Physiology, 9, 11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meyers, R. A. , & Hermanson, J. W. (2006). Horse soleus muscle: Postural sensor or vestigial structure? The Anatomical Record Part A, 288A, 1068–1076. [DOI] [PubMed] [Google Scholar]
- Michilsens, F. , Vereecke, E. E. , D'août, K. , & Aerts, P. (2009). Functional anatomy of the gibbon forelimb: Adaptations to a brachiating lifestyle. Journal of Anatomy, 215, 335–354. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller, C. V. , & Pittman, M. (2021). The diet of early birds based on modern and fossil evidence and a new framework for its reconstruction. Biological Reviews, 96, 2058–2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morhardt, A. C. , & Witmer, L. M. (2016). Diffusible iodine‐based contrast enhancement of large, post‐embryonic, intact vertebrates for CT scanning: staining, destaining, and long‐term storage. In: ICVM. Washington, DC: The Anatomical Record; pp. 89–90.
- Nabavizadeh, A. (2016). Evolutionary trends in the jaw adductor mechanics of ornithischian dinosaurs. The Anatomical Record, 299, 271–294. [DOI] [PubMed] [Google Scholar]
- Nabavizadeh, A. (2020a). Cranial musculature in herbivorous dinosaurs: A survey of reconstructed anatomical diversity and feeding mechanisms. The Anatomical Record, 303, 1104–1145. [DOI] [PubMed] [Google Scholar]
- Nabavizadeh, A. (2020b). New reconstruction of cranial musculature in ornithischian dinosaurs: Implications for feeding mechanisms and buccal anatomy. The Anatomical Record, 303, 347–362. [DOI] [PubMed] [Google Scholar]
- Ogle, W. (1882). Translation of: Parts of animals (originally written by Aristotle, c. 350 BCE). Kegan Paul, Trench and Co. [Google Scholar]
- Okumura, N. , Hashida‐Okumura, A. , Kita, K. , Matsubae, M. , Matsubara, T. , Takao, T. , & Nagai, K. (2005). Proteomic analysis of slow‐and fast‐twitch skeletal muscles. Proteomics, 5, 2896–2906. [DOI] [PubMed] [Google Scholar]
- Organ, J. M. , Teaford, M. F. , & Taylor, A. B. (2009). Functional correlates of fiber architecture of the lateral caudal musculature in prehensile and nonprehensile tails of the Platyrrhini (primates) and Procyonidae (Carnivora). The Anatomical Record, 292, 827–841. [DOI] [PubMed] [Google Scholar]
- Orsbon, C. , Gidmark, N. , & Ross, C. (2018). Dynamic musculoskeletal functional morphology: Integrating diceCT and XROMM. Anatomical Record, 301, 378–406. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peck, A. (1965). Translation of: History of animals (originally by Aristotle, c. 350 BCE). Heinemann. [Google Scholar]
- Penrose, F. , Cox, P. , Kemp, G. , & Jeffery, N. (2020). Functional morphology of the jaw adductor muscles in the Canidae. The Anatomical Record, 303(11), 2878–2903. [DOI] [PubMed] [Google Scholar]
- Perry, J. (2018). Inferring the diets of extinct giant lemurs from osteological correlates of muscle. Anatomical Record, 301, 343–362. [DOI] [PubMed] [Google Scholar]
- Perry, J. M. G. , Hartstone‐Rose, A. , & Wall, C. E. (2011). The jaw adductors of strepsirrhines in relation to body size, diet, and ingested food size. The Anatomical Record, 294, 712–728. [DOI] [PubMed] [Google Scholar]
- Perry, J. M. G. , & Prufrock, K. A. (2018). Muscle functional morphology in Paleobiology: The past, present, and future of "Paleomyology". The Anatomical Record, 301, 538–555. [DOI] [PubMed] [Google Scholar]
- Pette, D. , & Staron, R. S. (1990). Cellular and molecular diversities of mammalian skeletal muscle fibers. Reviews of Physiology, Biochemistry and Pharmacology, 116, 1–76. [DOI] [PubMed] [Google Scholar]
- Radinsky, L. B. (1981). Evolution of skull shape in carnivores I: Representative modern carnivores. Biological Journal of the Linnean Society, 15, 369–388. [Google Scholar]
- Ratkiewicz, A. , Granatosky, M. , Young, M. , Molnar, J. , & Dickinson, E. (2022). Sensitivity assessment of muscle fascicle reconstruction via an automated algorithmic approach. Tomography for Scientific Advancement. [Google Scholar]
- Rowlerson, A. , Mascarello, F. , Veggetti, A. , & Carpenè, E. (1983). The fibre‐type composition of the first branchial arch muscles in Carnivora and primates. Journal of Muscle Research & Cell Motility, 4, 443–472. [DOI] [PubMed] [Google Scholar]
- Rupert, J. E. , Schmidt, E. C. , Moreira‐Soto, A. , Herrera, B. R. , Vandeberg, J. L. , & Butcher, M. T. (2014). Myosin isoform expression in the prehensile tails of Didelphid marsupials: Functional differences between arboreal and terrestrial opossums. The Anatomical Record, 297, 1364–1376. [DOI] [PubMed] [Google Scholar]
- Sacks, R. D. , & Roy, R. R. (1982). Architecture of the hind limb muscles of cats: Functional significance. Journal of Morphology, 173, 185–195. [DOI] [PubMed] [Google Scholar]
- Sahd, L. , Bennett, N. C. , & Kotzé, S. H. (2022). Hind foot drumming: Volumetric micro‐computed tomography investigation of the hind limb musculature of three African mole‐rat species (Bathyergidae). Journal of Anatomy, 240, 23–33. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saint‐Hilaire, G. (1822). Philosophie anatomique. Méquignon‐Marvis. [Google Scholar]
- Sakamoto, M. (2022). Estimating bite force in extinct dinosaurs using phylogenetically predicted physiological cross‐sectional areas of jaw adductor muscles. PeerJ, 10, 19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanger, J. M. , & Sanger, J. W. (2014). Recent advances in muscle research. The Anatomical Record, 297, 1539–1542. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Santana, S. E. (2018). Comparative anatomy of bat jaw musculature via diffusible iodine‐based contrast‐enhanced computed tomography. The Anatomical Record, 301, 267–278. [DOI] [PubMed] [Google Scholar]
- Santana, S. E. , Dumont, E. R. , & Davis, J. L. (2010). Mechanics of bite force production and its relationship to diet in bats. Functional Ecology, 24, 776–784. [Google Scholar]
- Schiaffino, S. , & Reggiani, C. (1994). Myosin isoforms in mammalian skeletal muscle. Journal of Applied Physiology, 77, 493–501. [DOI] [PubMed] [Google Scholar]
- Schiaffino, S. , & Reggiani, C. (2011). Fiber types in mammalian skeletal muscles. Physiological Reviews, 91, 1447–1531. [DOI] [PubMed] [Google Scholar]
- Schumacher, G. (1961). Funktionelle morphologie der kaumuskulatur. Fisher. [Google Scholar]
- Snively, E. , & Russell, A. P. (2007). Functional variation of neck muscles and their relation to feeding style in tyrannosauridae and other large theropod dinosaurs. The Anatomical Record, 290, 934–957. [DOI] [PubMed] [Google Scholar]
- St. Clair, E. M. , Reback, N. , & Perry, J. M. G. (2018). Craniomandibular variation in phalangeriform marsupials: Functional comparisons with primates. Anatomical Record, 301, 227–255. [DOI] [PubMed] [Google Scholar]
- Sullivan S, McGechie F, Middleton K, Holliday C. 2019. 3D muscle architecture of the pectoral muscles of European Starling (Sturnus vulgaris). Integrative organismal biology 1:oby010. [DOI] [PMC free article] [PubMed]
- Sustaita, D. (2008). Musculoskeletal underpinnings to differences in killing behavior between north American accipiters (Falconiformes: Accipitridae) and falcons (Falconidae). Journal of Morphology, 269, 283–301. [DOI] [PubMed] [Google Scholar]
- Suzuki, A. (1977). A comparative histochemical study of the masseter muscle of the cattle, sheep, swine, dog, Guinea pig, and rat. Histochemistry, 51, 121–131. [DOI] [PubMed] [Google Scholar]
- Taylor, A. B. , Eng, C. M. , Anapol, F. C. , & Vinyard, C. J. (2009). The functional correlates of jaw‐muscle fiber architecture in tree‐gouging and nongouging callitrichid monkeys. American Journal of Physical Anthropology, 139, 353–367. [DOI] [PubMed] [Google Scholar]
- Taylor, A. B. , & Holmes, M. A. (2021). Fiber‐type phenotype of the jaw‐closing muscles in Gorilla gorilla, pan troglodytes, and pan paniscus: A test of the frequent recruitment hypothesis. Journal of Human Evolution, 151, 102938. [DOI] [PubMed] [Google Scholar]
- Taylor, A. B. , & Vinyard, C. J. (2004). Comparative analysis of masseter fiber architecture in tree‐gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids. Journal of Morphology, 261, 276–285. [DOI] [PubMed] [Google Scholar]
- Taylor, A. B. , & Vinyard, C. J. (2009). Jaw‐muscle fiber architecture in tufted capuchins favors generating relatively large muscle forces without compromising jaw gape. Journal of Human Evolution, 57, 710–720. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ter Keurs, H. , Iwazumi, T. , & Pollack, G. (1978). The sarcomere length‐tension relation in skeletal muscle. Journal of General Physiology, 72, 565–592. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thorpe, S. K. , Crompton, R. H. , Guenther, M. M. , Ker, R. F. , & McNeill, A. R. (1999). Dimensions and moment arms of the hind‐and forelimb muscles of common chimpanzees (Pan troglodytes). American Journal of Physical Anthropology, 110, 179–199. [DOI] [PubMed] [Google Scholar]
- To, K. H. , O’Brien, H. D. , Stocker, M. R. , & Gignac, P. M. (2021). Cranial musculoskeletal description of black‐throated finch (Aves: Passeriformes: Estrildidae) with DiceCT. Integrative Organismal Biology, 3, obab007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Toledo, N. , Bargo, M. S. , & Vizcaino, S. F. (2015). Muscular reconstruction and functional morphology of the hind limb of Santacrucian (Early Miocene) sloths (Xenarthra, Folivora) of Patagonia. The Anatomical Record, 298, 842–864. [DOI] [PubMed] [Google Scholar]
- Tomo, S. , Tomo, I. , Townsend, G. C. , & Hirata, K. (2007). Masticatory muscles of the great‐gray kangaroo (Macropus giganteus). The Anatomical Record, 290, 382–388. [DOI] [PubMed] [Google Scholar]
- Venkataraman, V. V. , Kraft, T. S. , & Dominy, N. J. (2013). Tree climbing and human evolution. Proceedings of the National Academy of Sciences, 110, 1237–1242. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vereecke, E. E. , D'Août, K. , Payne, R. , & Aerts, P. (2005). Functional analysis of the foot and ankle myology of gibbons and bonobos. Journal of Anatomy, 206, 453–476. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vesalius, A. (1543). De Humani Corporis Fabrica. Basel: Joannes Oporinus.
- Wallace, A. R. (1878). Tropical nature, and other essays. Macmillan and Company. [Google Scholar]
- Warburton, N. M. (2009). Comparative jaw muscle anatomy in kangaroos, wallabies, and rat‐kangaroos (Marsupialia: Macropodoidea). The Anatomical Record, 292, 875–884. [DOI] [PubMed] [Google Scholar]
- Warburton, N. M. , & Marchal, C. R. (2017). Forelimb myology of carnivorous marsupials (Marsupialia: Dasyuridae): Implications for the ancestral body plan of the Australidelphia. The Anatomical Record, 300, 1589–1608. [DOI] [PubMed] [Google Scholar]
- Ward, A. B. , Weigl, P. D. , & Conroy, R. M. (2002). Functional morphology of raptor hindlimbs: Implications for resource partitioning. The Auk, 119, 1052–1063. [Google Scholar]
- Waszink, J. , & Jensen, P. (1975). Translation of: Timaeus a Calcidio Translatus Commentarioque Instructus (originally written by Calcidius, c. 400 BCE). In Klibansky R. (Ed.), Plato Latinus. Leiden. [Google Scholar]
- Wickiewicz, T. L. , Roy, R. R. , Powell, P. L. , & Edgerton, V. R. (1983). Muscle architecture of the human lower limb. Clinical Orthopaedics and Related Research, 179, 275–283. [PubMed] [Google Scholar]
- Wiedersheim, R. (1907). Comparative anatomy of vertebrates. Macmillan and Company, Limited. [Google Scholar]
- Williams, S. H. , Sidote, J. , & Stover, K. K. (2010). Occlusal development and masseter activity in alpacas (Lama pacos). The Anatomical Record, 293, 126–134. [DOI] [PubMed] [Google Scholar]
- Wood, J. (1867). On human muscular variations and their relation to comparative anatomy. Journal of Anatomy and Physiology, 1, 44–59. [PMC free article] [PubMed] [Google Scholar]
- Wroe, S. , McHenry, C. , & Thomason, J. (2005). Bite club: Comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa. Proceedings of the Royal Society B‐Biological Sciences, 272, 619–625. [DOI] [PMC free article] [PubMed] [Google Scholar]
