Limits...
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

Chondrogenic differentiation in chameleon carpus. During distal flattening and expansion (a-c), the digital rays are already present and are lightly stained by Alcian Blue. The first elements of the mesopodium to form as cartilage are the Fi, dc4, and metacarpals 3–5. Distal carpal 3 and 5 form next (d, e) with later appearance of the intermedium, metacarpal 2 (f-h) and ultimately the radiale and pisiform (i-j). All embryos were at 107 dpo from clutchmates
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig11: Chondrogenic differentiation in chameleon carpus. During distal flattening and expansion (a-c), the digital rays are already present and are lightly stained by Alcian Blue. The first elements of the mesopodium to form as cartilage are the Fi, dc4, and metacarpals 3–5. Distal carpal 3 and 5 form next (d, e) with later appearance of the intermedium, metacarpal 2 (f-h) and ultimately the radiale and pisiform (i-j). All embryos were at 107 dpo from clutchmates

Mentions: In our skeletal analysis of Chamaeleo calyptratus, we identified 2 rows of skeletogenesis during development of the carpals (Fig. 11a-j; Fig. 15a-c, g-j): 4 proximal carpal elements (pisiform, ulnare, intermedium, radiale) and 5 distal elements (distal carpals 1–5). Tarsal elements also developed from two rows (Fig. 12a-g; Fig. 14b, c; Fig. 15d-f, k-m): 3 proximal elements (fibulare, intermedium, tibiale) and 4 distal elements (distal tarsal 2–5; summarized in Fig. 16). Interestingly, the intermedium appears to condense in association with different mesopodial elements, from the distal medial radius in the hand and from the distal medial fibula in the foot (Fig. 15). Thus, C. calyptratus retains more mesopodial elements than previously acknowledged, with only the medial and lateral centrale of Lepidosauria failing to develop Additional file 2. Centralia are generally the last elements to form ontogenetically [64, 65] and are consistent with a heterochronic terminal truncation. A clear series of proximal condensations is not present in the outgroup taxa Aspidoscelis uniparens and Pogona vitticeps, as observed by the increased and more diffuse alcian blue staining present across this domain (Fig. 13).Fig. 11


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)

Chondrogenic differentiation in chameleon carpus. During distal flattening and expansion (a-c), the digital rays are already present and are lightly stained by Alcian Blue. The first elements of the mesopodium to form as cartilage are the Fi, dc4, and metacarpals 3–5. Distal carpal 3 and 5 form next (d, e) with later appearance of the intermedium, metacarpal 2 (f-h) and ultimately the radiale and pisiform (i-j). All embryos were at 107 dpo from clutchmates
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig11: Chondrogenic differentiation in chameleon carpus. During distal flattening and expansion (a-c), the digital rays are already present and are lightly stained by Alcian Blue. The first elements of the mesopodium to form as cartilage are the Fi, dc4, and metacarpals 3–5. Distal carpal 3 and 5 form next (d, e) with later appearance of the intermedium, metacarpal 2 (f-h) and ultimately the radiale and pisiform (i-j). All embryos were at 107 dpo from clutchmates
Mentions: In our skeletal analysis of Chamaeleo calyptratus, we identified 2 rows of skeletogenesis during development of the carpals (Fig. 11a-j; Fig. 15a-c, g-j): 4 proximal carpal elements (pisiform, ulnare, intermedium, radiale) and 5 distal elements (distal carpals 1–5). Tarsal elements also developed from two rows (Fig. 12a-g; Fig. 14b, c; Fig. 15d-f, k-m): 3 proximal elements (fibulare, intermedium, tibiale) and 4 distal elements (distal tarsal 2–5; summarized in Fig. 16). Interestingly, the intermedium appears to condense in association with different mesopodial elements, from the distal medial radius in the hand and from the distal medial fibula in the foot (Fig. 15). Thus, C. calyptratus retains more mesopodial elements than previously acknowledged, with only the medial and lateral centrale of Lepidosauria failing to develop Additional file 2. Centralia are generally the last elements to form ontogenetically [64, 65] and are consistent with a heterochronic terminal truncation. A clear series of proximal condensations is not present in the outgroup taxa Aspidoscelis uniparens and Pogona vitticeps, as observed by the increased and more diffuse alcian blue staining present across this domain (Fig. 13).Fig. 11

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