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Scenario of webbed foot evolution in birds. The lobate feet observed in the common coot and little grebe were probably created through distinct developmental processes. The lobate foot of the common coot may have evolved through proliferation of interdigital tissue cells that express Gremlin1 along the toes in an anisodactyl-footed ancestor. On the other hand, the little grebe's locate foot may have arisen by loss of Gremlin1 expression at the centre of the interdigital tissues of a palmate-footed ancestor. Although Gremlin1 is expressed in all St. 31 interdigital tissues in the totipalmate-footed great cormorant, its expression disappears in the centre of the interdigital tissues at St. 33. This suggests that the webbing of the great cormorant may have arisen through a distinct developmental mechanism, where BMP signaling plays a fundamental role.
Source publication
The webbed feet of waterbirds are morphologically diverse and classified into four types: the palmate foot, semipalmate foot, totipalmate foot, and lobate foot. To understand the developmental mechanisms underlying this morphological diversity, we conducted a series of comparative analyses. Ancestral state reconstruction based on phylogeny assumed...
Context in source publication
Context 1
... state reconstruction suggested that the common ancestor of the common coot possessed anisodactyl feet, while the common ancestor of the little grebe possessed palmate feet (Fig. 2). These results suggest that the two types of lobate feet arose through distinct developmental processes (Fig. 6). The lobate foot of the common coot probably evolved through a proliferation of interdigital tissue cells that express Gremlin1 along the toes of the anisodactyl ancestor. On the other hand, the lobate foot of the little grebe may have evolved through a contraction of Gremlin1 expression at the centre of the interdigital tissues of the ...
Citations
... One rapidly evolving CNE was separately examined in BMP4 and BMP7 that regulated interdigital cell death. Another one accelerated CNE was located near the GREM1, a known antagonist of BMPs protein [30]. By contrast, there were two identified accelerated CNEs of TBX4 that was specific expression in hindlimb [31]. ...
... A total of 11 mutations were uniquely detected in cetacean lineages, nine of which located in the functional domains of BMP2 (4), BMP4 (2), and BMP7 (3), which support a potential involvement of BMP signaling in cetacean hyperphalangy that would require further investigation. BMPs were also found to promote the interdigital cell apoptosis, but its antagonism (GREM1) allowed the interdigital cells to survive in waterbirds [30]. It was previously reported that cetacean interdigital webbing occurs in the flipper-forelimb because interdigital cell apoptosis is suppressed during embryo development [4]. ...
Background
Cetacean hindlimbs were lost and their forelimb changed into flippers characterized by webbed digits and hyperphalangy, thus allowing them to adapt to a completely aquatic environment. However, the underlying molecular mechanism behind cetacean limb development remains poorly understood.
Results
In the present study, we explored the evolution of 16 limb-related genes and their cis-regulatory elements in cetaceans and compared them with that of other mammals. TBX5 , a forelimb specific expression gene, was identified to have been under accelerated evolution in the ancestral branches of cetaceans. In addition, 32 cetacean-specific changes were examined in the SHH signaling network ( SHH , PTCH1 , TBX5 , BMPs and SMO ), within which mutations could yield webbed digits or an additional phalange. These findings thus suggest that the SHH signaling network regulates cetacean flipper formation. By contrast, the regulatory activity of the SHH gene enhancer—ZRS in cetaceans—was significantly lower than in mice, which is consistent with the cessation of SHH gene expression in the hindlimb bud during cetacean embryonic development. It was suggested that the decreased SHH activity regulated by enhancer ZRS might be one of the reasons for hindlimb degeneration in cetaceans. Interestingly, a parallel / convergent site (D42G) and a rapidly evolving CNE were identified in marine mammals in FGF10 and GREM1, respectively, and shown to be essential to restrict limb bud size; this is molecular evidence explaining the convergence of flipper-forelimb and shortening or degeneration of hindlimbs in marine mammals.
Conclusions
We did evolutionary analyses of 16 limb-related genes and their cis-regulatory elements in cetaceans and compared them with those of other mammals to provide novel insights into the molecular basis of flipper forelimb and hindlimb loss in cetaceans.
... Among others, the streamlined body shape, developed sternal keel, and powerful pectoral and pelvic musculature (Ostrom 1976, Heers & Dial 2012) provided optimal 'starting point' to develop aquatic abilities and due to the rigid body, the production of thrust relies on the limbs (appendicular locomotion) (Gatesy & Dial 1996). However, in order to provide the proper amount of thrust, to propel the body in a denser environment, and to overcome drag forces both submerged and on the water surface, the structure of fore-and hind limbs shows certain adaptations: such as smaller wings (Raikow et al. 1988) or flatter and rigid hydrofoil-like flippers (Louw 1992), webbed or lobbed feet (Johansson & Norberg 2003, Tokita et al. 2020. In order to support the streamlined body shape, some of the most aquatic forms, such as loons, grebes, and penguins incorporated to some extent, the hind limbs into the abdominal skin (Kaiser 2011. ...
... walking or even running) capabilities (Provini et al. 2012). The propulsion is provided by the alternate strokes of the feet (Gough et al. 2015, Fish 2016, and the paddling movements are supported by lobed or webbed feet, which evolved convergently in several taxa with different phylogenetic background (Tokita et al. 2020). Besides progress and resting, eating from the surface could be the advantage of this low-speed movement: such as grasping organisms, or even filtering plankton (Ashmole 1971). ...
Adaptation to an aquatic lifestyle occurred in the evolution of several primarily terrestrial clades of
tetrapods. Among these lineages, aquatic birds’ adaptations differ in many ways from other secondarily aquatic
vertebrates. As a consequence of the evolution of flight, birds with swimming and diving abilities represent
unique locomotion skills and complex anatomical solutions. Here we attempt to overview some of the main
aspects of avian locomotion in water and highlight the diversity of their aquatic habits and locomotion types,
with the best-known extinct and extant examples. The main features that can distinguish the different groups
among these swimmers and divers are their different techniques to overcome buoyancy, the transformation
of wings or hind limbs into aquatic propulsive organs, and their swimming techniques besides the presence
or absence of the flying and/or terrestrial abilities. Understanding how the musculoskeletal system of aquatic
birds evolved to face the requirements of moving in various environments with different physical characteristics
provides a good opportunity to get a better view of convergent and divergent evolution.
... Palmates can be morphologically classi ed in four groups as palmate, semipalmate, totipalmate, and lobate. Foot structure of geese is palmate, which is mostly common (Tokita et al., 2020). The FW of the geese were measured with the help of calipers at the end of the 14th week (Fig. 5). ...
The aim of the study is to examine the performance and carcass characteristics and some behavioral parameters of geese reared in the areas created by using some objects for environmental enrichment (EE) purpose. For this purpose, a total of 72 one-day-old goose goslings of both sexes were used. Geese were accommodated collectively for the first four weeks, then they were divided in three groups in 3 repetitions according to the EE applications and these were expressed as control (C), broom (B), and mirror (M). At the end of 14th week, live weight (LW), beak length (BL), wing length (WL), head diameter (HD), foot width (FW), body temperature (BT), warm carcass (WC), and cold carcass (CC) weights as well as warm and cold pH values (WpH&CpH), and tonic immobility duration (TID) of the groups were measured. Responses presented during the TI test were expressed as non-responses (NR), medium responses (MR), and high responses (HR). Among the groups, group M had the lowest value (110.08±10.69 s) in terms of TID (P > 0.05). Differences in terms of NR, MR, and HR were significant (P > 0.05). The differences between the groups were not statistically significant in terms of the other characteristics (P < 0.05). As a result, it was determined that geese reared by using the EE objects were affected by such environments, however, there were differences between the groups in terms of fear and stress parameters without having any negative effects on yield.
... They include water-adapted species from three clades: Aequiornithines (diving 5 birds, wading birds, shorebirds), Gruiformes (containing rails and cranes) and Anseriformes (ducks and geese) (Prum et al. 2015). With sufficient ornithological interest for their own focus group (e.g., Waterbird Society), waterbirds have been subject to extensive research including recent exploration of the genetic basis underlying interdigital webbing in their feet (Tokita et al. 2020). Waterbirds, known conclusively now to be representatives of at least three phylogenetic assemblages, are nonetheless united ecologically by their proximity to, and dependence on, aquatic or nearshore habitats that has led to convergence in morphology, trophic strategy and locomotor behavior. ...
Synopsis
Wing shape plays a critical role in flight function in birds and other powered fliers and has been shown to be correlated with flight performance, migratory distance, and the biomechanics of generating lift during flight. Avian wing shape and flight mechanics have also been shown to be associated with general foraging behavior and habitat choice. We aim to determine if wing shape in waterbirds, a functionally and ecologically diverse assemblage united by their coastal and aquatic habitats, is correlated with various functional and ecological traits. We applied geometric morphometric approaches to the spread wings of a selection of waterbirds to search for evolutionary patterns between wing shape and foraging behavior, habitat, and migratory patterns. We found strong evidence of convergent evolution of high and low aspect ratio wing shapes in multiple clades. Foraging behavior also consistently exhibits strong evolutionary correlations with wing shape. Habitat, migration, and flight style, in contrast, do not exhibit significant correlation with wing shape in waterbirds. Although wing shape is critical to aerial flight function, its relationship to habitat and periodic locomotor demands such as migration is complex.
... There is vast knowledge about different aspects of the bird foot, mainly with regard to toe orientation and development (e.g., Abourachid et al., 2017;Bock & Miller, 1959;Botelho et al., 2014;Botelho, Smith-Paredes, Soto-Acuña, et al., 2015;de Bakker et al., 2013;Raikow, 1985;Tokita, Matsushita, & Asakura, 2020). Nevertheless, association between the keratinous plantar surface, of ectoderm origin, and skeletal structure of toes, of mesoderm origin, has been little explored with regard to functional foot use by birds. ...
... brasiliensis, the skin extends to the tips of toes II, III, and IV to form a palmate foot. The feet of swimming birds may be palmate, or totipalmate (web between I-II-III-IV) or lobed, with the toes free but edged with leaf-like skin (Raikow, 1985;Tokita, Matsushita, & Asakura, 2020). Some species are semipalmate, with a web only on the first phalanges as in the charadriiform shorebirds. ...
... Embryologically, in the limb buds, the footplate is composed of interdigital tissues that connect the digital rays. During the embryological stages HH30-HH35 apoptosis leads to regression of the skin between the toes in zygodactyls (Carril & Tambussi, 2015) as well as in the anisodactyl Galloanseres (Hamburger & Hamilton, 1951) and also in passerines (Yamasaki & Tonosaki, 1988), but it does not occur in webbed feet species (Tokita, Matsushita, & Asakura, 2020). Apoptosis results from a morphogenetic process, that is, interdigital cell death (ICD), which is facilitated by bone morphogenetic proteins. ...
The skin of the foot provides the interface between the bird and the substrate. The foot morphology involves the bone shape and the integument that is in contact with the substrate. The podotheca is a layer of keratinized epidermis forming scales that extends from the tarsometatarsus to the toe extremities. It varies in size, shape, amount of overlap and interacts with the degree of fusion of the toes (syndactyly). A study of toe shape and the podotheca provides insights on the adaptations of perching birds. Our analysis is based on micro‐CT scans and scanning electron microscopy images of 21 species from 17 families, and includes examples with different orientations of the toes: zygodactyl (toes II and III forward), anisodactyl (toes II, III, and IV forward), and heterodactyl (toes III and IV forward). We show that in these three groups, the skin forms part of a perching adaptation that involves syndactyly to different degrees. However, syndactyly does not occur in Psittacidae that use their toes also for food manipulation. The syndactyly increases the sole surface and may reinforce adherence with the substrate. Scale shape and toe orientation are involved in functional adaptations to perch. Thus, both bone and skin features combine to form a pincer‐like foot. In the feet of birds, the morphological adaptations involve two systems: the osteomuscular and the tegumentary. In perching species, the foot may be syndactyl with the skin forming a sheath that closely associates the phalanges of two or three toes. In Psittacidae, which manipulate with the feet, the toes are free. In raptors and walking birds, loose skin may involve the base of two toes, or in swimmers the entire length of the toes forming a web.
... A most illustrative example of this fact are the varieties in the pattern of interdigital cell death according to the pattern of digit webbing in species adapted to live in distinct habits. Thus, among the differences in humans, mice or chickens, interdigital cell death is absent or reduced in the developing bat wings (Weatherbee et al., 2006), in the developing flippers of aquatic mammalias (Cooper et al., 2018) and in the feet of swimming aquatic birds (Tokita et al., 2020). The discovery of "cell death genes" directly related to the physiological elimination of specific cells in the worm C. elegans (Ellis and Horvitz, 1986) and their evolutionary conservation in mammals (Peter et al., 1997) provided strong support for this idea. ...
... This process lasts between 36 and 48 h in mouse and chick embryos and its sequence was traditionally mapped by vital staining with Neutral red or Nile blue (Figure 2A). Importantly, the intensity of the degenerating process in different species appears directly associated with the final morphology of the digits (Tokita et al., 2020). It is lower in species with webbed digits and very intense in species with free digits. ...
Digits develop in the distal part of the embryonic limb primordium as radial prechondrogenic condensations separated by undifferentiated mesoderm. In a short time interval the interdigital mesoderm undergoes massive degeneration to determine the formation of free digits. This fascinating process has often been considered as an altruistic cell suicide that is evolutionarily-regulated in species with different degrees of digit webbing. Initial descriptions of interdigit remodeling considered lysosomes as the primary cause of the degenerative process. However, the functional significance of lysosomes lost interest among researcher and was displaced to a secondary role because the introduction of the term apoptosis. Accumulating evidence in recent decades has revealed that, far from being a unique method of embryonic cell death, apoptosis is only one among several redundant dying mechanisms accounting for the elimination of tissues during embryonic development. Developmental cell senescence has emerged in the last decade as a primary factor implicated in interdigit remodeling. Our review proposes that cell senescence is the biological process identified by vital staining in embryonic models and implicates lysosomes in programmed cell death. We review major structural changes associated with interdigit remodeling that may be driven by cell senescence. Furthermore, the identification of cell senescence lacking tissue degeneration, associated with the maturation of the digit tendons at the same stages of interdigital remodeling, allowed us to distinguish between two functionally distinct types of embryonic cell senescence, “constructive” and “destructive.”
... In humans, syndactyly is one of the most prevalent malformations, 59 and many genetic alterations, both in humans and in laboratory animals, show variable levels of syndactyly. These observations, together with the diversity of the webbing in different tetrapods, 60 have often led researchers to suspect the existence of a specific genetic regulation for INZ. However, the functional variety of genes whose mutations are associated with syndactyly and the heterogeneity of the phenotypes present in individuals with the same mutation 59 make it difficult to identify a specific upstream genetic regulatory pathway for the degenerative process. ...
... 79 Consistent with this interpretation, the BMP antagonist Gremlin 1 is a recognized marker of the interdigits in species with webbed digits. 18,60,80 On the other side, the pro-condrogenic influence of BMPs over the skeletal progenitors is dependent on the expression of SOX9. SOX9 is a master gene of chondrogenesis that modifies the configuration of chromatin promoting the expression of downstream chondrogenic genes. ...
Our aim is to critically review current knowledge of the function and regulation of cell death in the developing limb. We provide a detailed, but short, overview of the areas of cell death observed in the developing limb, establishing their function in morphogenesis and structural development of limb tissues. We will examine the functions of this process in the formation and growth of the limb primordia, formation of cartilaginous skeleton, formation of synovial joints, and establishment of muscle bellies, tendons and entheses. We will analyze the plasticity of the cell death program by focusing on the developmental potential of progenitors prior to death. Considering the prolonged plasticity of progenitors to escape from the death process, we will discuss a new biological perspective that explains cell death: this process, rather than secondary to a specific genetic program, is a consequence of the tissue building strategy employed by the embryo based on the formation of scaffolds that disintegrate once their associated neighboring structures differentiate. This article is protected by copyright. All rights reserved.
