Transcriptional heterochrony in talpid mole autopods

Abstract

Background: Talpid moles show many specializations in their adult skeleton linked to fossoriality, including enlarged hands when compared to the feet. Heterochrony in developmental mechanisms is hypothesized to account for morphological evolution in skeletal elements.

Methods: The temporal and spatial distribution of SOX9 expression, which is an early marker of chondrification, is analyzed in autopods of the fossorial Iberian mole Talpa occidentalis, as well as in shrew (Cryptotis parva) and mouse (Mus musculus) for comparison.

Results and discussion: SOX9 expression is advanced in the forelimb compared to the hind limb in the talpid mole. In contrast, in the shrew and the mouse, which do not show fossorial specializations in their autopods, it is synchronous. We provide evidence that transcriptional heterochrony affects the development of talpid autopods, an example of developmental penetrance. We discuss our data in the light of earlier reported pattern heterochrony and later morphological variation in talpid limbs.

Conclusion: Transcriptional heterochrony in SOX9 expression is found in talpid autopods, which is likely to account for pattern heterochrony in chondral limb development as well as size variation in adult fore- and hind limbs.

Figure 1

Microtomography scan images of adult Talpa occidentalis (A-B) and Cryptotis parva (C-D). The same models of right hands (A, C) and feet (B, D) were also used in Mitgutsch et al.[4] and Mitgutsch et al.[6].

Figure 2

 In situ hybridization with SOX9 on autopods of Talpa occidentalis , Cryptotis parva and Mus musculus . Right hands and feet are in dorsal view, except for O-P, which are left hand and foot in palmar and plantar view, respectively [4]. Images E-N and Q-R were mirrored to make the orientation consistent. Roman numbers indicate digits. Age determination: early 17 d (A-B), 18d (C-D), 19d (E-F), 13.5d (G-H), 15.5d (I-J), 17.5d (K-L), 12.5d (M-N), 13.5d (O-P), and 14.5 d (Q-R).