Hidden limbs in the “limbless skink” Brachymeles lukbani: developmental observations

Daniel Smith-Paredes*, Oliver Griffith, Matteo Fabbri, Laurel Yohe, Daniel G. Blackburn, Cameron D. Siler, Bhart-Anjan S. Bhullar, Günter P. Wagner

*Corresponding author for this work

    Research output: Contribution to journalArticlepeer-review

    1 Citation (Scopus)

    Abstract

    Reduced limbs and limblessness have evolved independently in many lizard clades. Scincidae exhibit a wide range of limb‐reduced morphologies, but only some species have been used to study the embryology of limb reduction (e.g., digit reduction in Chalcides and limb reduction in Scelotes). The genus Brachymeles, a Southeast Asian clade of skinks, includes species with a range of limb morphologies, from pentadactyl to functionally and structurally limbless species. Adults of the small, snake‐like species Brachymeles lukbani show no sign of external limbs in the adult except for small depressions where they might be expected to occur. Here, we show that embryos of B. lukbani in early stages of development, on the other hand, show a truncated but well‐developed limb with a stylopod and a zeugopod, but no signs of an autopod. As development proceeds, the limb's small size persists even while the embryo elongates. These observations are made based on external morphology. We used florescent whole‐mount immunofluorescence to visualize the morphology of skeletal elements and muscles within the embryonic limb of B. lukabni. Early stages have a humerus and separated ulna and radius cartilages; associated with these structures are dorsal and ventral muscle masses as those found in the embryos of other limbed species. While the limb remains small, the pectoral girdle grows in proportion to the rest of the body, with well‐developed skeletal elements and their associated muscles. In later stages of development, we find the small limb is still present under the skin, but there are few indications of its presence, save for the morphology of the scale covering it. By use of CT scanning, we find that the adult morphology consists of a well‐developed pectoral girdle, small humerus, extremely reduced ulna and radius, and well‐developed limb musculature connected to the pectoral girdle. These muscles form in association with a developing limb during embryonic stages, a hint that “limbless” lizards that possess these muscles may have or have had at least transient developing limbs, as we find in B. lukbani. Overall, this newly observed pattern of ontogenetic reduction leads to an externally limbless adult in which a limb rudiment is hidden and covered under the trunk skin, a situation called cryptomelia. The results of this work add to our growing understanding of clade‐specific patterns of limb reduction and the convergent evolution of limbless phenotypes through different developmental processes.
    Original languageEnglish
    Pages (from-to)693-703
    Number of pages11
    JournalJournal of Anatomy
    Volume239
    Issue number3
    Early online date18 Apr 2021
    DOIs
    Publication statusPublished - Sep 2021

    Keywords

    • limb development
    • limb reduction
    • lizard evolution
    • musculoskeletal evolution

    Fingerprint

    Dive into the research topics of 'Hidden limbs in the “limbless skink” Brachymeles lukbani: developmental observations'. Together they form a unique fingerprint.

    Cite this