273This pattern exists throughout the anamniotes (icthyopsids) and the reptiles and
is initially established by cortical rotation in the egg, leading to Wnt/beta-catenin
asymmetry, elevated dorsal Nodal signaling and organizer induction and dorsal
mesoderm involution (Fig. 6.14). Interestingly, much of this sequence of events is
likely specific to the vertebrates. In basal invertebrate chordates, such as
Branchiostoma, cortical rotation and early dorsal enrichment of beta-catenin do not
occur and gastrulation occurs symmetrically via cell ingression, with minimal invo-
lution (Zhang et al. 1997 ; Holland and Onai 2012 ). Early Nodal asymmetry is pres-
ent and likely leads to the induction of organizer/BMP antagonist gene expression
on the dorsal side of the blastopore (Yu et al. 2007 ; Holland and Onai 2012 ). Thus,
a key series of events in early vertebrate evolution was likely the appearance of
cortical rotation, leading to the restriction of gastrulation initiation dorsally, coupled
with a transition to cell involution behavior in the organizer.
In contrast to this early asymmetry mechanism, therian mammals undergo appar-
ent ab embryo axis specification, with the early phase of Wnt asymmetry being lost
and evolving into new mechanisms of symmetry breaking in the blastocyst, based
on cell position and migration in the visceral endoderm. In both ab ovo and ab
embryo cases, the egg and the blastocyst exhibit marked metastability, rendering
development with radial symmetry improbable under normal conditions. The
evolutionary transitions between these mechanisms are not well understood.
Increases in yolk and egg size and the shift to meroblastic cleavage have been sug-
gested to drive the evolution towards primitive streak-based gastrulation (Arendt
and Nübler- Jung 1999 ), although these cannot be the sole factors involved. Reptiles
have large eggs and undergo meroblastic cleavage but still form the organizer first
and develop a horizontal slit blastopore/blastoporal plate, maintaining the ancestral
dorsal involution/lateral ingression pattern. Additionally, teleosts also evolved
meroblastic cleavage but this change resulted in additional adaptations to keep a
blastoporal gastrulation pattern, rather than evolving primitive streak-like move-
ments. Furthermore, the “primitive steak” evolved independently in birds and in
mammals, possibly multiple times, which could explain the differences in cellular
mechanisms underlying formation of the primitive streak, as well as observations
such as the presence of left-right asymmetries around Hensen’s node and lack of
nodal cilia in both chick and pig (Gros et al. 2009 ; Blum et al. 2014 ).
This convergent evolution toward the primitive streak could be correlated with
changes in the development of the hypoblast/anterior endoderm. In amphibians and
reptiles, these cells arise during cleavage from yolky vegetal cells, whereas in birds
and mammals the hypoblast develops from cells delaminating or sorting out from
the epiblast. Formation of the hypoblast in this manner could be a prerequisite for
the emergent behavior of coordinated polonaise-like cell movements in the epiblast,
which themselves are likely sufficient to position and initiate the primitive streak
(Voiculescu et al. 2007 ). Additionally, owing to the more prominent role of hypo-
blast migration in birds and mammals, cell internalization initiates with the primi-
tive streak, not with the organizer. Full organizer formation, in terms of gene
expression and inducing activity, does not occur until mid-gastrulation. Thus, there
is significant heterochrony in the main pattern of axis formation in birds and mam-
6 Vertebrate Axial Patterning: From Egg to Asymmetry