skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Diverse Tongue Base Retraction Strategies Drive Bolus Propulsion during Mammalian Swallowing
Synopsis During swallowing, a diverse range of mammals—from opossums to humans—propel food boluses out of the oropharynx via tongue base retraction (TBR). The widespread distribution of TBR behavior implies an ancient evolutionary origin, but the biomechanical mechanisms of TBR remain poorly understood. The evolution of TBR behavior is further complicated by the diversity of hyoid and tongue anatomy across mammals: to what extent does hyolingual morphology shape TBR mechanism? Using biplanar videoradiography and the XROMM workflow, we collected high-resolution 3D kinematic data in opossums (Marsupialia), dogs (Placentalia), and macaques (Placentalia) to test hypotheses on the evolutionary conservation of TBR mechanisms. Despite differences in hyolingual morphology and resting hyoid position, both dogs and macaques drive TBR through hyoid movement: hyoid excursions reduce the oral volume and squeeze the tongue base posteriorly, analogous to a hydraulic pump displacing an incompressible fluid. In opossums, however, intrinsic lingual muscles deform the tongue base to initiate TBR, independent of hyoid movement and oral volume change. We suggest that multiple mechanisms are viable for the highly conserved TBR behavior across mammals, and the functional diversity of TBR mechanisms is decoupled from the morphological diversity of the hyolingual system. This decoupling may have facilitated the evolution of novel hyolingual phenotypes while avoiding trade-offs in swallowing performance.  more » « less
Award ID(s):
2315501
PAR ID:
10614362
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Society for Integrative and Comparative Biology
Date Published:
Journal Name:
Integrative And Comparative Biology
ISSN:
1540-7063
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Resolving the phylogenetic relationships among Paleocene mammals has been a longstanding goal in paleontology. Constructing an accurate and comprehensive phylogeny for Paleocene mammals is a worthwhile objective in itself, but it also provides a framework on which we can better understand the origin of placental mammals and the evolutionary processes underlying the diversification of mammals before, during, and after the end-Cretaceous mass extinction. More recently, a robust Palaeocene mammal phylogeny has become a much-coveted tool for reconciling discrepancies between morphological and molecular evidence for the phylogeny and diversification of Placentalia. Here, we present a novel phylogenetic dataset to test hypotheses regarding Paleocene mammal phylogeny and the origin and diversification of Placentalia. To date, our matrix combines phenomic data for 36 extant mammal species and 107 fossil species scored for 2540 morphological characters alongside 26 genes sequenced for 47 species. We utilized a reductive morphological scoring strategy in order to minimize assumptions and test hypotheses on homology. Multiple sequence alignments were performed in MEGA-X for each gene. We then analysed the data using Bayesian methods and explored the effects of different approaches. Relaxed clock analyses using a molecular constraint and an FBD prior are congruent with the diversification of many extant orders prior to the K-Pg boundary. Relaxed clocked total-evidence analyses (morphology and molecules) using an FBD prior resulted in older ages of diversification than those estimated by our relaxed clock molecular constraint model and previous molecular studies. Within Placentalia, our phylogenies provide support for the divergence of Atlantogenata (Afrotheria and Xenarthra) from Boreoeutheria (Euarchontoglires and Laurasiatheria). Among the Paleocene taxa, ‘condylarths’ are distributed along the base of Laurasiatheria with members of ‘Arctocyonidae’ recovered as sister taxa to Artiodactyla; enigmatic groups such as Pantodonta and Taeniodonta are recovered as crown placentals whereas Leptictida is not. Our Paleocene mammal phylogeny is a critical step toward better understanding placental mammal evolution. Ultimately, this work will facilitate the investigation of fundamental questions previously encumbered by the lack of a well-resolved phylogeny. 
    more » « less
  2. Intra-oral food processing, including chewing, is important for safe swallowing and efficient nutrient assimilation across tetrapods. Gape cycles in tetrapod chewing consist of four phases (fast open and -close, and slow open and -close), with processing mainly occurring during slow close. Basal aquatic-feeding vertebrates also process food intraorally, but whether their chew cycles are partitioned into distinct phases, and how rhythmic their chewing is, remains unknown. Here, we show that chew cycles from sharks to salamanders are as rhythmic as those of mammals, and consist of at least three, and often four phases, with phase distinction occasionally lacking during jaw opening. In fishes and aquatic-feeding salamanders, fast open has the most variable duration, more closely resembling mammals than basal amniotes (lepidosaurs). Across ontogenetically or behaviourally mediated terrestrialization, salamanders show a distinct pattern of the second closing phase (near-contact) being faster than the first, with no clear pattern in partitioning of variability across phases. Our results suggest that distinct fast and slow chew cycle phases are ancestral for jawed vertebrates, followed by a complicated evolutionary history of cycle phase durations and jaw velocities across fishes, basal tetrapods and mammals. These results raise new questions about the mechanical and sensorimotor underpinnings of vertebrate food processing. This article is part of the theme issue ‘Food processing and nutritional assimilation in animals’. 
    more » « less
  3. 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. 
    more » « less
  4. Abstract Background and AimsFew studies of angiosperms have focused on androecial evolution in conjunction with evolutionary shifts in corolla morphology and pollinator relationships. The Western Hemisphere clade of Justiciinae (Acanthaceae) presents the rare opportunity to examine remarkable diversity in staminal morphology. We took a phylogenetically informed approach to examine staminal diversity in this hypervariable group and asked whether differences in anther thecae separation is associated with phylogenetically informed patterns of variation in corolla morphology. We further discuss evidence for associations between anther diversity and pollinators in this lineage. MethodsFor the Dianthera/Sarotheca/Plagiacanthus (DSP) clade of Western Hemisphere Justiciinae, we characterized floral diversity based on a series of corolla measurements and using a model-based clustering approach. We then tested for correlations between anther thecae separation and corolla traits, and for shifts in trait evolution, including evidence for convergence. Key ResultsThere is evolutionary vagility in corolla and anther traits across the DSP clade with little signal of phylogenetic constraint. Floral morphology clusters into four distinct groups that are, in turn, strongly associated with anther thecae separation, a novel result in Acanthaceae and, to our knowledge, across flowering plants. These cluster groups are marked by floral traits that strongly point to associations with pollinating animals. Specifically, species that are known or likely to be hummingbird pollinated have stamens with parallel thecae, whereas those that are likely bee or fly pollinated have stamens with offset, divergent thecae. ConclusionsOur results suggest that anther thecae separation is likely under selection in concert with other corolla characters. Significant morphological shifts detected by our analyses corresponded to putative shifts from insect to hummingbird pollination. Results from this study support the hypothesis that floral structures function in an integrated manner and are likely subject to selection as a suite. Further, these changes can be hypothesized to represent adaptive evolution. 
    more » « less
  5. Abstract Fish skulls are often highly kinetic, with multiple linkage and lever systems powered by a diverse suite of muscles. Comparative analysis of the evolution of soft-tissue structures in the fish skull is often limited under traditional approaches, while new imaging techniques like diceCT (diffusible iodine-based contrast-enhanced computed tomography) allow for high-resolution imaging of muscles in situ. Darters (Percidae: Etheostomatinae) are a diminutive and species-rich clade of lotic freshwater fishes, which show diverse head shapes believed to be associated with different foraging strategies. We used diceCT to sample all major cranial adductors and abductors responsible for movement of the jaw, hyoid, operculum, and suspensorium from 29 species. We applied comparative phylogenetic approaches to analyse the evolutionary trends in muscle size across the clade. We found two major patterns: (i) darter cranial muscles show fundamental trade-offs relating to investment in musculature, as well as buccal expansion vs. biting attributes; early divergence in muscle size appears to be associated with shifts in habitat use and foraging; (ii) darter adductor mandibulae show high variation in architecture (fibre orientation, divisions). This study highlights how new imaging techniques can provide novel insights into the anatomy of even well-sampled/represented clades. 
    more » « less