NMPs As a Development Module Affecting Evolutionary Change in Segment Number and Body Length

The variation in segment number and primary body axis length among different vertebrates suggests that NMP development has evolved, possibly contributing to the diversification of vertebrate body plans. There are several putative mechanisms by which changes to NMPs could affect the body plan, including the initial number of NMPs, the rate at which they are depleted, or the transcription of genes critical for the clock and wavefront patterning of the somites. Although it is difficult to experimentally demonstrate that changes in NMPs have occurred between species that directly impact differences in body plan, there is at least some evidence to suggest that molecular changes in NMPs lead to distinct body plan development. An example is the Brachyury gene, which as previously mentioned functions in an autoregulatory loop with canonical Wnt signaling to maintain the NMP population over the duration of body axis extension (Martin and Kimelman, 2008). In recent years, Brachyury mutations have been identified in naturally occurring tailless dogs and cats (Buckingham et al.. 2013; Haworth et al.. 2001; Hytonen et al.. 2009). These data indicate that manipulating just the Brachyury!Wnt feedback loop is sufficient to change the body plan of animals, such that lowering the amount of functional Brachyury results in loss of tails and a shorter overall body length. This also suggests that evolutionary changes to Brachyury expression levels could modify body length, but there is no direct evidence to show that differential expression levels of Brachyury between species accounts for species-specific differences in body plan development.

Body length, as mentioned earlier, can also be controlled by the timing of Hox gene expression in the NMPs. Since the onset of terminal Hox gene expression correlates with the cessation of body axis extension, developmental changes to Hox gene expression could affect body length and segment number (Denans et al., 2015; Olivera-Martinez et al., 2012; Wymeersch et al., 2019). This was shown to be the case in a mouse HoxBB mutant. HoxBB is one of the terminal Hox genes expressed in NMPs as the most posterior part of the body is developing (Economides et al., 2003). HoxBB homozygous mutant mice have an increase body length and supernumerary segments, suggesting that changes to Hox gene regulation within NMPs could indeed affect the evolution of the vertebrate body.

Another important aspect of the vertebrate body plan is the trunk-to-tail ratio, or the number of trunk segments relative to tail segments. The trunk-to-tail transition point is generally accepted as the somite adjacent to the hindlimbs. Some animals, like snakes, have exceptionally long trunks compared to other vertebrates (Gomez et al., 2008). Although NMPs contribute to the somites along the entire body axis, they display different properties depending on whether they originate in the epiblast and contribute to the trunk, or within the tailbud where they contribute to the tail. NMPs exhibit a differential genetic requirement between the trunk and tail in mouse embryos. The trunk NMPs are dependent on Oct4 transcription factor expression, whereas the tail NMPs depend on GDF11 signaling, which in turn represses the expression of the RNA binding protein Lin28 (Aires et al., 2019; Aires et al., 2016). When Oct4 is artificially sustained in NMPs, there is striking lengthening of the trunk of the embryo, with up to six extra segments in the trunk compared to wild-type embryos (Aires et al., 2016). On the other hand, if Lin28 is artificially sustained in NMPs, there is a lengthening of the tail, with up to five extra tail somites forming on average (Aires et al., 2019). These results indicate that modulations of the genetic networks regulating pre- or post-gastrulation NMPs can affect the evolution of the body plan through differential lengthening or shortening of the trunk vs. tail segment number.

Overall body length, the relative number of trunk vs. tail somites, and the total number of somites that form can impact adaptation to particular ecological niches. For instance, the large number of somites that form in snakes allows undulations associated with slithering on the ground, which is an important aspect of their locomotion and behavior. Since the molecular regulation of the clock and wavefront mechanism begins as mesoderm progenitors are established, changes in the expression of these components would affect the somite number and the ability to adapt to new environments. Thus, genetic changes that affect the induction, maintenance, and proliferation of NMPs, along with their subsequent segmentation after joining the mesoderm, can impact body plan evolution by affecting the length and/or number of segments. A comparison between clock and wavefront components has been made between species with varying segment number, including zebrafish, chicken, mouse, and the corn snake (Gomez et al., 2008). In these species, similar clock and wavefront genes are expressed, but in the corn snake, the rate of oscillations of clock genes relative to the overall rate of development is much faster than in the other species examined. The net result of this difference is the formation of many small somites in the corn snake. Together, the experimental evidence suggests that modulation of NMP maintenance and differentiation, along with clock and wavefront gene expression in NMP-derived mesoderm, is a major determinant of body plan evolution within the vertebrate clade.

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