On the origins of species-specific size

Because of high functional demands, tissue size is tightly regulated during development. This is particularly evident in limb length, where differences in size between matching limbs could have significant impacts on fitness. Although right and left sides of the body develop independently, right and left limbs consistently reach comparable length (Allard & Tabin 2009). Similarly, size differences in the right and left sides of the jaw are involved in many craniofacial malformations, such as cleft lip and palate. Therefore, developmental mechanisms regulating size are highly conserved in order to buffer variation (Leevers & McNeill 2005). Given that evolution requires variation, how then do differences in size evolve? The recent manuscript (Fish et al. 2014), addressed this question from the perspective of the jaw.

HFSP Long-Term Fellow Jennifer Fish and colleagues
authored on Mon, 31 March 2014

Utilizing two avian species, duck and quail, that exhibit remarkably different jaw size, we investigated when, where, and how duck acquire their long bills compared to quail who have short beaks. First, we counted neural crest cells, the progenitors of the jaw skeleton, at several embryonic time points. We found that duck have significantly more pre-migratory neural crest (15%) in the midbrain, the region from which neural crest migrate into the jaw priomordia. By midgestation, duck have twice as many cells in their jaw primordia as do quail. To understand how an initial 15% difference could result in a doubling of the population, we analyzed cell proliferation and cell cycle length, and found that, when developmental rate is taken into account, duck neural crest proliferate relatively faster than quail, which can explain the progressive increase in jaw size in duck embryos.

Figure: Species-specific neural crest allocation. Post-migratory NC was identified by in situ hybridization for Dlx2 at HH13 in (A) quail and (B) duck embryos. The Dlx2-positive NC domain is outlined with black dashed lines and the stomodeum is highlighted with red dashed lines (see inset in B). (C) Migration of quail donor NC into the duck host mandibular arch was evaluated in HH13 chimeric quck embryos. Q¢PN staining (green) identifies nuclei of the donor quail neural crest that have migrated into the host mandibular arch. Dlx2 in situ hybridization (E) of HH13 quck embryos is similar on both donor and host sides of the stomodeum. mx= maxilla; md = mandibule; st = stomodeum. Modified from Fish et al. 2014.

To uncover a mechanism through which duck increase the number of precursor cells that come out of the midbrain, species-specific differences in the expression of brain regionalization markers were assessed.  Comparison of Pax6 (forebrain), Otx2 (fore- and midbrain), Fgf8 (midbrain-hindbrain boundary), and Krox20 (r3 and r5 of the hindbrain) in duck and quail revealed divergent brain shapes and spatial domains of gene expression.  Relative to quail, duck have an anterior shift in brain regionalization and a broader midbrain. This anterior shift is correlated with an elongated primitive mouth (stomodeum), which allows more neural crest to migrate into the jaw primordia, such that duck embryos initially have more jaw precursors (indicated by Dlx2 expression) than quail embryos (Figure 1A,B). In chimeric embryos, where donor quail neural crest is transplanted into duck host embryos, quail neural crest migrate into the jaw primordia in a duck-like fashion (Figure 1C). These data indicate that alterations in brain regionalization may underlie two separate factors that contribute to differences in jaw size. First, the wider midbrain of duck concentrates neural crest in a migratory path towards the jaw primordia, and second, the anterior shift generates a larger spatial domain for the neural crest to migrate into. Overall, our work reveals that modifications to multiple aspects of cell biology, from brain regionalization to species-specific regulation of cell proliferation, may underlie the evolution of jaw size.

Reference

Multiple developmental mechanisms regulate species-specific jaw size. Fish JL, Sklar RS, Woronowicz KC, and Schneider RA. (2014). Development, 141:674-684.

Other References

1) Achieving bilateral symmetry during vertebrate limb development. Semin. Allard, P. and Tabin, C. J. (2009). Cell Dev. Biol. 20, 479-484.

2) Controlling the size of organs and organisms. Leevers, S. J. and McNeill, H. (2005). Cell Biol. 17, 604-609.

Pubmed link (main ref)

Pubmed link (ref 1)

Pubmed link (ref 2)