Patterning and post-patterning modes of evolutionary digit loss in mammals

Cooper, Kimberly L.; Sears, Karen E.; Uygur, Aysu; Maier, Jennifer; Baczkowski, Karl Stephan; Brosnahan, Margaret M.; Antczak, Douglas F.; Skidmore, J.A.; Tabin, Clifford J.

doi:10.1038/nature13496

Cited by 137 publications

(189 citation statements)

References 35 publications

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“…Similar to the jerboa, cells that may have contributed to the continued development of these medial and lateral digits instead die by apoptotic cell death [110]. Surprisingly, camels, which are highly derived two-toed artiodactyls, do not have the posterior restriction of Ptch1 that is shared among other species of the clade but instead have a more jerboa and horse-like pattern of apoptosis that carves away progenitors of digits II and V to leave only III and IV.…”

Section: Development and Evolution Of Digit Numbermentioning

confidence: 95%

“…The three-toed jerboa, a desert adapted bipedal rodent, has three hind-and five forelimb digits. Expression of 5 0 Hox genes and components of the Shh pathway do not differ from mouse, but Bmp4 and Msx2 are upregulated in the anterior and posterior margins specifically in the hind-but not forelimb [110]. Bmp4 and Msx2 together regulate the pattern of interdigital apoptotic cell death, and indeed their expansion corresponds with domains of apoptosis that encompass the tissue distal to the nascent first and fifth digits.…”

Section: Development and Evolution Of Digit Numbermentioning

confidence: 99%

“…Cattle have two toes (digits III and IV) while pigs have two prominent toes (III and IV) and two that are reduced in size (II and V). Expression of the SHH receptor, Ptch1, is highly reduced and limited to the posterior autopod in developing cow [109] and pig [110] forelimb buds compared with mouse ( figure 1). In addition to its role in derepressing the SMOOTHENED receptor in response to SHH binding, PTCH1 is thought to sequester and restrict SHH protein distribution [112,113].…”

Section: Development and Evolution Of Digit Numbermentioning

confidence: 99%

“…In addition to these two Shh-dependent and apoptosis-mediated mechanisms of digit loss, Fgf8 expression is lost from the AER overlying truncated and missing digits of cow, pig, camel, horse and three-toed jerboa limb buds at digit-forming stages. This suggests that loss of a mitogenic fibroblast growth factor (FGF) signal might play an additional role reinforcing each of the early limb pattern and late apoptotic mechanisms of digit loss [109,110].…”

Section: Development and Evolution Of Digit Numbermentioning

confidence: 99%

“…Given the importance of Shh in determination of digit number, it is perhaps no surprise that the loss of digits in reptiles [107,108] and mammals [109,110] corresponds to changes in the expression of Shh pathway members. Comparison of five different Hemiergis lizard species, with digits ranging from two to five in number, showed that species with the fewest digits were those with the shortest duration of Shh expression in developing limb buds ( figure 1).…”

Section: Development and Evolution Of Digit Numbermentioning

confidence: 99%

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The origins, scaling and loss of tetrapod digits

Saxena

Towers

Cooper

2017

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Evodevo in the genomics era, and the origins of morphological diversity'. Many of the great morphologists of the nineteenth century marvelled at similarities between the limbs of diverse species, and Charles Darwin noted these homologies as significant supporting evidence for descent with modification from a common ancestor. Sir Richard Owen also took great care to highlight each of the elements of the forelimb and hindlimb in a multitude of species with focused attention on the homology between the hoof of the horse and the middle digit of man. The ensuing decades brought about a convergence of palaeontology, experimental embryology and molecular biology to lend further support to the homologies of tetrapod limbs and their developmental origins. However, for all that we now understand about the conserved mechanisms of limb development and the development of gross morphological disturbances, little of what is presented in the experimental or medical literature reflects the remarkable diversity resulting from the 450 million year experiment of natural selection. An understanding of conserved and divergent limb morphologies in this new age of genomics and genome engineering promises to reveal more of the developmental potential residing in all limbs and to unravel the mechanisms of evolutionary variation in limb size and shape. In this review, we present the current state of our rapidly advancing understanding of the evolutionary origin of hands and feet and highlight what is known about the mechanisms that shape diverse limbs.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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Section: Development and Evolution Of Digit Numbermentioning

confidence: 95%

Section: Development and Evolution Of Digit Numbermentioning

confidence: 99%

Section: Development and Evolution Of Digit Numbermentioning

confidence: 99%

Section: Development and Evolution Of Digit Numbermentioning

confidence: 99%

Section: Development and Evolution Of Digit Numbermentioning

confidence: 99%

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The origins, scaling and loss of tetrapod digits

Saxena

Towers

Cooper

2017

Phil. Trans. R. Soc. B

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Evolution of Vertebrate Limb Development

Tanaka

2017

Encyclopedia of Life Sciences

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The origin and diversification of fins and limbs have long been a focus of interest to both palaeontologists and developmental biologists. Studies conducted in recent decades have resulted in enormous progress in the understanding of the genetic and developmental bases of the evolution of paired appendages in vertebrates. These discoveries in the areas of genetics and developmental biology have shed light on the mechanisms underlying the evolution of this key morphological innovation in vertebrates. In this article, recent advances in these fields and how they can provide a mechanistic explanation for the origin and evolution of paired appendages have been discussed. Key Concepts Step‐wise changes seem to be involved in the acquisition of paired fins, such as regionalisation of the lateral plate mesoderm (LPM) into the anterior and posterior LPM; sub‐division of the LPM into somatic and splanchnic layers; acquisition of expression of genes that initiate limb formation, such as Tbx4/5 ; and dorso‐ventral compartmentalisation of ectoderm. Morphological changes during the fin‐to‐limb transition include the acquisition of the autopod and the evolutionary modification of skeletal patterns along the anterior–posterior axis. The fin‐to‐limb transition seems to involve changes in transcriptional regulation of HoxA and HoxD clusters, changes in the expression of Gli3 and Shh , loss of the fin fold, and modification of the BMP‐SOX9‐WNT Turing network. Changes in the activity of regulatory elements of genes known to play pivotal roles in limb development seem to be related to the morphological diversification of limbs and the loss of paired fins and limbs.

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Ossification pattern of the unusual pisiform in two‐toed (Choloepus) and three‐toed sloths (Bradypus)

Gavazzi

Kjosness

Reno

2021

The Anatomical Record

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Two-toed (Choloepus sp.) and three-toed (Bradypus sp.) sloths possess short, rounded pisiforms that are rare among mammals and differ from other members of Xenarthra like the giant anteater (Myrmecophaga tridactyla) which retain elongated, rod-like pisiforms in common with most mammals. Using photographs, radiographs, and μCT, we assessed ossification patterns in the pisiform and the paralogous tarsal, the calcaneus, for two-toed sloths, three-toed sloths, and giant anteaters to determine the process by which pisiform reduction occurs in sloths and compare it to other previously studied examples of pisiform reduction in humans and orangutans. Both extant sloth genera achieve pisiform reduction through the loss of a secondary ossification center and the likely disruption of the associated growth plate based on an unusually porous subchondral surface. This represents a third unique mechanism of pisiform reduction among mammals, along with primary ossification center loss in humans and retention of two ossification centers with likely reduced growth periods in orangutans. Given the remarkable similarities between two-toed and three-toed sloth pisiform ossification patterns and the presence of pisiform reduction in fossil sloths, extant sloth pisiform morphology does not appear to represent a recent convergent adaptation to suspensory locomotion, but instead is likely to be an ancestral trait of Folivora that emerged early in the radiation of extant and fossil sloths.

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Patterning and post-patterning modes of evolutionary digit loss in mammals

Cited by 137 publications

References 35 publications

The origins, scaling and loss of tetrapod digits

The origins, scaling and loss of tetrapod digits

Evolution of Vertebrate Limb Development

Ossification pattern of the unusual pisiform in two‐toed (Choloepus) and three‐toed sloths (Bradypus)

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