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Hand/foot splitting and the 're-evolution' of mesopodial skeletal elements during the evolution and radiation of chameleons.

Diaz RE, Trainor PA - BMC Evol. Biol. (2015)

Bottom Line: One of the most distinctive traits found within Chamaeleonidae is their split/cleft autopodia and the simplified and divergent morphology of the mesopodial skeleton.Body size may have played a role in the characteristic mesopodial skeletal architecture of chameleons by constraining deployment of the skeletogenic program in the smaller and earliest diverged and basal taxa.Our study challenges the 're-evolution' of osteological features by showing that 're-evolving' a 'lost' feature de novo (contrary to Dollo's Law) may instead be due to so called 'missing structures' being present but underdeveloped and/or fused to other adjacent elements (cryptic features) whose independence may be re-established under changes in adaptive selective pressure.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, La Sierra University, Riverside, CA, 92515, USA. Lissamphibia@gmail.com.

ABSTRACT

Background: One of the most distinctive traits found within Chamaeleonidae is their split/cleft autopodia and the simplified and divergent morphology of the mesopodial skeleton. These anatomical characteristics have facilitated the adaptive radiation of chameleons to arboreal niches. To better understand the homology of chameleon carpal and tarsal elements, the process of syndactyly, cleft formation, and how modification of the mesopodial skeleton has played a role in the evolution and diversification of chameleons, we have studied the Veiled Chameleon (Chamaeleo calyptratus). We analysed limb patterning and morphogenesis through in situ hybridization, in vitro whole embryo culture and pharmacological perturbation, scoring for apoptosis, clefting, and skeletogenesis. Furthermore, we framed our data within a phylogenetic context by performing comparative skeletal analyses in 8 of the 12 currently recognized genera of extant chameleons.

Results: Our study uncovered a previously underappreciated degree of mesopodial skeletal diversity in chameleons. Phylogenetically derived chameleons exhibit a 'typical' outgroup complement of mesopodial elements (with the exception of centralia), with twice the number of currently recognized carpal and tarsal elements considered for this clade. In contrast to avians and rodents, mesenchymal clefting in chameleons commences in spite of the maintenance of a robust apical ectodermal ridge (AER). Furthermore, Bmp signaling appears to be important for cleft initiation but not for maintenance of apoptosis. Interdigital cell death therefore may be an ancestral characteristic of the autopodium, however syndactyly is an evolutionary novelty. In addition, we find that the pisiform segments from the ulnare and that chameleons lack an astragalus-calcaneum complex typical of amniotes and have evolved an ankle architecture convergent with amphibians in phylogenetically higher chameleons.

Conclusion: Our data underscores the importance of comparative and phylogenetic approaches when studying development. Body size may have played a role in the characteristic mesopodial skeletal architecture of chameleons by constraining deployment of the skeletogenic program in the smaller and earliest diverged and basal taxa. Our study challenges the 're-evolution' of osteological features by showing that 're-evolving' a 'lost' feature de novo (contrary to Dollo's Law) may instead be due to so called 'missing structures' being present but underdeveloped and/or fused to other adjacent elements (cryptic features) whose independence may be re-established under changes in adaptive selective pressure.

No MeSH data available.


Related in: MedlinePlus

SEM of Chamaeleo calyptratus hand and foot morphogenesis. Early stages of morphogenesis show that the chameleon hand develops as a round digital plate (a) which subsequently develops a distal flattening (d, g). In dorsal view, these stages present a very robust AER, relatively larger than that present in A. uniparens (Fig. 3) while in distal view the AER is seen as having a greater thickness along the dorsoventral midline (b, e, h). Significantly, during the stage at which the distal autopodium begins to flatten (g), the distal AER is no longer the stereotypical A-P flattened ectodermal thickening but is instead arched ventrally (h, i). Surprisingly, despite having a robust distal AER, proximal mesenchymal cleft formation has already begun (j, k). At later stages (l-o, p-s), both the forelimb and hindlimb expand the cleft while maintaining the AER quite robust until the thickness tapers and narrows at later stages (while the AER also returns to its expected conformation of a straight distal ridge)
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Fig4: SEM of Chamaeleo calyptratus hand and foot morphogenesis. Early stages of morphogenesis show that the chameleon hand develops as a round digital plate (a) which subsequently develops a distal flattening (d, g). In dorsal view, these stages present a very robust AER, relatively larger than that present in A. uniparens (Fig. 3) while in distal view the AER is seen as having a greater thickness along the dorsoventral midline (b, e, h). Significantly, during the stage at which the distal autopodium begins to flatten (g), the distal AER is no longer the stereotypical A-P flattened ectodermal thickening but is instead arched ventrally (h, i). Surprisingly, despite having a robust distal AER, proximal mesenchymal cleft formation has already begun (j, k). At later stages (l-o, p-s), both the forelimb and hindlimb expand the cleft while maintaining the AER quite robust until the thickness tapers and narrows at later stages (while the AER also returns to its expected conformation of a straight distal ridge)

Mentions: Current knowledge of cleft formation in autopodia comes from examination of avian and mammalian systems as well as linkage studies in humans, with all work supporting a failure to maintain the integrity of the Apical Ectodermal Ridge (AER), particularly along the distal midline [33–35]. Loss of the AER inhibits not only distal outgrowth of the limb but also leads to the loss or splitting of the digital rays. To determine whether or not AER destabilization is the primary factor driving cleft formation, we examined the AER of A. uniparens in order to first understand how a ‘typical’ AER is structured in pentadactyl lizard autopodia (Fig. 3). At 13 dpo (days post oviposition), a robust distal ectodermal thickening (Fig. 3a-d) is present at the dorso-ventral boundary of the forelimbs and hindlimbs. At 16 dpo (Fig. 3e-h) the AER begins to narrow as the digital rays differentiate within the underlying mesenchyme. By 20–21 dpo (Fig. 3i-l) the AER further narrows prior to the initiation of interdigital cell death. By comparison, in chameleon autopodia, the AER is thicker and more prominent (Fig. 4a-i). Interestingly, upon distal flattening of the digital plate (Fig. 2d, j; Fig. 4g, J, k), commencement of distal clefting in chameleon interdigital tissue is visible despite the retainment of a very robust AER. Syndactylous digit clusters diverge toward the anterior and posterior poles, increasing the angle between clusters and further expanding the cleft. The proximodistal size of the autopodium remains unchanged during these stages. Overall, autopodial shape shifts from a distally flattened rounded paddle to one that is rectangular shaped (Fig. 4l-o). It is interesting to note that as the AER is maintained, it appears slightly thicker in the region overlying the clefting mesenchyme (Fig. 4q, s), which may be compensatory to maintain interdigital tissue proliferation during this midline mesenchymal expansion in concert with digit bundle realignment prior to cleft formation.Fig. 3


Hand/foot splitting and the 're-evolution' of mesopodial skeletal elements during the evolution and radiation of chameleons.

Diaz RE, Trainor PA - BMC Evol. Biol. (2015)

SEM of Chamaeleo calyptratus hand and foot morphogenesis. Early stages of morphogenesis show that the chameleon hand develops as a round digital plate (a) which subsequently develops a distal flattening (d, g). In dorsal view, these stages present a very robust AER, relatively larger than that present in A. uniparens (Fig. 3) while in distal view the AER is seen as having a greater thickness along the dorsoventral midline (b, e, h). Significantly, during the stage at which the distal autopodium begins to flatten (g), the distal AER is no longer the stereotypical A-P flattened ectodermal thickening but is instead arched ventrally (h, i). Surprisingly, despite having a robust distal AER, proximal mesenchymal cleft formation has already begun (j, k). At later stages (l-o, p-s), both the forelimb and hindlimb expand the cleft while maintaining the AER quite robust until the thickness tapers and narrows at later stages (while the AER also returns to its expected conformation of a straight distal ridge)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4574539&req=5

Fig4: SEM of Chamaeleo calyptratus hand and foot morphogenesis. Early stages of morphogenesis show that the chameleon hand develops as a round digital plate (a) which subsequently develops a distal flattening (d, g). In dorsal view, these stages present a very robust AER, relatively larger than that present in A. uniparens (Fig. 3) while in distal view the AER is seen as having a greater thickness along the dorsoventral midline (b, e, h). Significantly, during the stage at which the distal autopodium begins to flatten (g), the distal AER is no longer the stereotypical A-P flattened ectodermal thickening but is instead arched ventrally (h, i). Surprisingly, despite having a robust distal AER, proximal mesenchymal cleft formation has already begun (j, k). At later stages (l-o, p-s), both the forelimb and hindlimb expand the cleft while maintaining the AER quite robust until the thickness tapers and narrows at later stages (while the AER also returns to its expected conformation of a straight distal ridge)
Mentions: Current knowledge of cleft formation in autopodia comes from examination of avian and mammalian systems as well as linkage studies in humans, with all work supporting a failure to maintain the integrity of the Apical Ectodermal Ridge (AER), particularly along the distal midline [33–35]. Loss of the AER inhibits not only distal outgrowth of the limb but also leads to the loss or splitting of the digital rays. To determine whether or not AER destabilization is the primary factor driving cleft formation, we examined the AER of A. uniparens in order to first understand how a ‘typical’ AER is structured in pentadactyl lizard autopodia (Fig. 3). At 13 dpo (days post oviposition), a robust distal ectodermal thickening (Fig. 3a-d) is present at the dorso-ventral boundary of the forelimbs and hindlimbs. At 16 dpo (Fig. 3e-h) the AER begins to narrow as the digital rays differentiate within the underlying mesenchyme. By 20–21 dpo (Fig. 3i-l) the AER further narrows prior to the initiation of interdigital cell death. By comparison, in chameleon autopodia, the AER is thicker and more prominent (Fig. 4a-i). Interestingly, upon distal flattening of the digital plate (Fig. 2d, j; Fig. 4g, J, k), commencement of distal clefting in chameleon interdigital tissue is visible despite the retainment of a very robust AER. Syndactylous digit clusters diverge toward the anterior and posterior poles, increasing the angle between clusters and further expanding the cleft. The proximodistal size of the autopodium remains unchanged during these stages. Overall, autopodial shape shifts from a distally flattened rounded paddle to one that is rectangular shaped (Fig. 4l-o). It is interesting to note that as the AER is maintained, it appears slightly thicker in the region overlying the clefting mesenchyme (Fig. 4q, s), which may be compensatory to maintain interdigital tissue proliferation during this midline mesenchymal expansion in concert with digit bundle realignment prior to cleft formation.Fig. 3

Bottom Line: One of the most distinctive traits found within Chamaeleonidae is their split/cleft autopodia and the simplified and divergent morphology of the mesopodial skeleton.Body size may have played a role in the characteristic mesopodial skeletal architecture of chameleons by constraining deployment of the skeletogenic program in the smaller and earliest diverged and basal taxa.Our study challenges the 're-evolution' of osteological features by showing that 're-evolving' a 'lost' feature de novo (contrary to Dollo's Law) may instead be due to so called 'missing structures' being present but underdeveloped and/or fused to other adjacent elements (cryptic features) whose independence may be re-established under changes in adaptive selective pressure.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, La Sierra University, Riverside, CA, 92515, USA. Lissamphibia@gmail.com.

ABSTRACT

Background: One of the most distinctive traits found within Chamaeleonidae is their split/cleft autopodia and the simplified and divergent morphology of the mesopodial skeleton. These anatomical characteristics have facilitated the adaptive radiation of chameleons to arboreal niches. To better understand the homology of chameleon carpal and tarsal elements, the process of syndactyly, cleft formation, and how modification of the mesopodial skeleton has played a role in the evolution and diversification of chameleons, we have studied the Veiled Chameleon (Chamaeleo calyptratus). We analysed limb patterning and morphogenesis through in situ hybridization, in vitro whole embryo culture and pharmacological perturbation, scoring for apoptosis, clefting, and skeletogenesis. Furthermore, we framed our data within a phylogenetic context by performing comparative skeletal analyses in 8 of the 12 currently recognized genera of extant chameleons.

Results: Our study uncovered a previously underappreciated degree of mesopodial skeletal diversity in chameleons. Phylogenetically derived chameleons exhibit a 'typical' outgroup complement of mesopodial elements (with the exception of centralia), with twice the number of currently recognized carpal and tarsal elements considered for this clade. In contrast to avians and rodents, mesenchymal clefting in chameleons commences in spite of the maintenance of a robust apical ectodermal ridge (AER). Furthermore, Bmp signaling appears to be important for cleft initiation but not for maintenance of apoptosis. Interdigital cell death therefore may be an ancestral characteristic of the autopodium, however syndactyly is an evolutionary novelty. In addition, we find that the pisiform segments from the ulnare and that chameleons lack an astragalus-calcaneum complex typical of amniotes and have evolved an ankle architecture convergent with amphibians in phylogenetically higher chameleons.

Conclusion: Our data underscores the importance of comparative and phylogenetic approaches when studying development. Body size may have played a role in the characteristic mesopodial skeletal architecture of chameleons by constraining deployment of the skeletogenic program in the smaller and earliest diverged and basal taxa. Our study challenges the 're-evolution' of osteological features by showing that 're-evolving' a 'lost' feature de novo (contrary to Dollo's Law) may instead be due to so called 'missing structures' being present but underdeveloped and/or fused to other adjacent elements (cryptic features) whose independence may be re-established under changes in adaptive selective pressure.

No MeSH data available.


Related in: MedlinePlus