Development and Evolution

A unique characteristic of mammals is a vertebral column with anatomically distinct regions, but when and how this trait evolved remains unknown. We reconstructed vertebral regions and their morphological disparity in the extinct forerunners of mammals, the nonmammalian synapsids, to elucidate the evolution of mammalian axial differentiation. Mapping patterns of regionalization and disparity (heterogeneity) across amniotes reveals that both traits increased during synapsid evolution. However, the onset of regionalization predates increased heterogeneity. On the basis of inferred homology patterns, we propose a " pectoral-first " hypothesis for region acquisition, whereby evolutionary shifts in forelimb function in nonmammalian therapsids drove increasing vertebral modularity prior to differentiation of the vertebral column for specialized functions in mammals.

During the time I have been occupied with the nature-nurture opposition, I have become sensitized both to the various guises in which this dichotomy appears and to structurally similar ones in other fields (figure 2). One of the sources of the nature-nurture dichotomy in science is the field of epistemology, in which a classic problem has been the origin of knowledge. The disputes between rationalists, who insisted on innate ideas as the source of knowledge, and empiricists, who credited the senses, did much to set the framework for more recent disputes. Similar oppositions are found in other fields as well.

Psychology, biology, and contemporary philosophy inherited the epistemological question fairly directly, but a number of other contrasting pairs have less obvious ties to the nature-nurture complex per se. Among historians, for instance, one finds internalist and externalist views of historical change, including scientific change. Anthropologists attribute cultural patterns in a society to biology or to culture (a form of nature-nurture dichotomy), and, interestingly enough, argue about cultural versus geographical determinism as well (Netting 1978). What is worth noting in the two anthropological examples is that culture is treated as an external factor in the first case and as a conservative, internal one in the second. This suggests that it is often scale (whether of time or magnitude) or level of analysis that is at issue in these debates, not competing factors of the same type.

Biology might seem the fleshiest of disciplines, but its accounts of ontogeny and phylogeny have long been strangely dematerialized. The discipline's informational turn gave pride of place to genes, those abstract but potent agents of change. Informational genes are conventionally credited with driving development, while change in their frequencies (in disembodied "gene pools") has become the very definition of evolution. In contrast, I offer an account of development, not as the expression of preexisting genetic representations, but as material emergence in organism-environment (developmental) systems. Evolution then becomes change in those systems.

Background: The ancestral arthropod is believed to have had a clustered arrangement of ten Hox genes. Within arthropods, Hox gene mutations result in transformation of segment identities. Despite the fact that variation in segment number/character was common in the diversification of arthropods, few examples of Hox gene gains/losses have been correlated with morphological evolution. Furthermore, a full appreciation of the variation in the genomic arrangement of Hox genes in extant arthropods has not been recognized, as genome sequences from each major arthropod clade have not been reported until recently. Initial genomic analysis of the chelicerate Tetranychus urticae suggested that loss of Hox genes and Hox gene clustering might be more common than previously assumed. To further characterize the genomic evolution of arthropod Hox genes, we compared the genomic arrangement and general characteristics of Hox genes from representative taxa from each arthropod subphylum. Results: In agreement with others, we find arthropods generally contain ten Hox genes arranged in a common orientation in the genome, with an increasing number of sampled species missing either Hox3 or abdominal-A orthologs. The genomic clustering of Hox genes in species we surveyed varies significantly, ranging from 0.3 to 13.6 Mb. In all species sampled, arthropod Hox genes are dispersed in the genome relative to the vertebrate Mus musculus. Differences in Hox cluster size arise from variation in the number of intervening genes, intergenic spacing, and the size of introns and UTRs. In the arthropods surveyed, Hox gene duplications are rare and four microRNAs are, in general, conserved in similar genomic positions relative to the Hox genes. Conclusions: The tightly clustered Hox complexes found in the vertebrates are not evident within arthropods, and differential patterns of Hox gene dispersion are found throughout the arthropods. The comparative genomic data continue to support an ancestral arthropod Hox cluster of ten genes with a shared orientation, with four Hox gene-associated miRNAs, although the degree of dispersion between genes in an ancestral cluster remains uncertain. Hox3 and abdominal-A orthologs have been lost in multiple, independent lineages, and current data support a model in which inversions of the Abdominal-B locus that result in the loss of abdominal-A correlate with reduced trunk segmentation.

Geometric morphometrics is widely used to study underlying causal factors in phenotypic evolution and to reconstruct evolutionary history of phenotypes. However, non-linearities in the phenotypic landscape may exist such that analytical solutions derived from comparison of phenotypes in morphospace may have complex or contradictory relationships in the space of the underlying factors. Ancestral reconstruction of horn morphology based on two mammalian ungulates illustrates how biologically improbable results can arise from the mathematical properties of geometric morphometric morphospaces. Raup’s shell coiling equations are used to illustrate the potential for contradictory conclusions to be drawn from ancestral reconstructions in parameter spaces (such as measurements of levels of gene expression or allele frequencies) versus shape spaces (such as morphospaces based on phenotypic analysis). These examples are generalizable to many real morphometric studies, suggesting that care should be taken when drawing conclusions about genetic, developmental, or environmental processes based on morphometric analyses. Dense sampling of shape space and the use of fully multivariate and, perhaps, non-linear methods can help forestall potential problems.