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. 2015 Apr 21;112(16):4871-6.
doi: 10.1073/pnas.1403665112.

Organogenesis in deep time: A problem in genomics, development, and paleontology

Joyce Pieretti  1 , Andrew R Gehrke  1 , Igor Schneider  2 , Noritaka Adachi  1 , Tetsuya Nakamura  1 , Neil H Shubin  3
Affiliations

Organogenesis in deep time: A problem in genomics, development, and paleontology

Joyce Pieretti et al. Proc Natl Acad Sci U S A. .

Abstract

The fossil record is a unique repository of information on major morphological transitions. Increasingly, developmental, embryological, and functional genomic approaches have also conspired to reveal evolutionary trajectory of phenotypic shifts. Here, we use the vertebrate appendage to demonstrate how these disciplines can mutually reinforce each other to facilitate the generation and testing of hypotheses of morphological evolution. We discuss classical theories on the origins of paired fins, recent data on regulatory modulations of fish fins and tetrapod limbs, and case studies exploring the mechanisms of digit loss in tetrapods. We envision an era of research in which the deep history of morphological evolution can be revealed by integrating fossils of transitional forms with direct experimentation in the laboratory via genome manipulation, thereby shedding light on the relationship between genes, developmental processes, and the evolving phenotype.

Keywords: development; evolution; fossil record; genomics; limb.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Origin of vertebrate paired fins. Scheme of the gill-arch hypothesis (A) and the fin-fold hypothesis (B), which supposes redeployment of the median fin developmental program through paired lateral fin folds or an unknown process leading to pectoral and pelvic fins. (C) Shared genetic features of gill arches, paired, and median fins in a generalized gnathostome embryo. (D) A phylogenetic tree of early vertebrates, modified from ref. . Taxa with associated illustrations are shown in bold. All vertebrates listed are agnathans except Placodermi and crown gnathostomes.
Fig. 2.
Fig. 2.
Epigenetic profiles and enhancer conservation of the vertebrate “autopod” Hox regulatory region. HoxD13 and HoxA13 show extensive contacts (as defined by 4C-seq and shown generally as red and blue regions above genomic areas) with the region 5′ to the cluster, defining an “autopod building” regulatory topology that is shared in both mouse and zebrafish (blue and red regions above the clusters, respectively) (–42). A number of individual enhancers that drive expression in the wrists and digits of mouse are also present in fish genomes (Island I, CsB, e16, e13, and e10) (–44). Both zebrafish and pufferfish sequences were unable to drive reporter activity in the digits of transgenic mice, whereas those of gar (a nonteleost fish with an unduplicated genome) were able to drive robust expression throughout the autopod of transgenic mice (41, 42).
Fig. 3.
Fig. 3.
Evolutionary diversification of limbs. (A) Phylogeny of mammalian taxa as per ref. , showing groups that have independently lost digits. Symbols denote the developmental mechanism sculpting limbs: cell apoptosis (red circle) and reduced Ptch1 expression (blue triangle) (49, 50). Skeletal limb morphology of adult organisms highlights the extent of digit reduction among taxa. (B) Equine fossil specimens document deviations from a pentadactyl state. (C) Pre- and postdigit patterning changes associated with alterations to limb morphology. (Top) Mouse forelimb showing broad Ptch1 expression in ectoderm and mesenchyme at embryonic day 11.25. (Middle) Cow forelimb expressing Ptch1 restricted to ectoderm at gestational day 34 (50). (Bottom) Schematic of labeled apoptotic cells in horse forelimb at 34 d after conception (49).
Fig. 4.
Fig. 4.
Experimental paleontology. (Left) Fossil evidence demonstrates an anatomical transition of body plan. (Right) Modern epigenomic techniques can identify candidate loci that contributed to this transition in the genome of extant organisms (, , –68). This synthesis of paleontological data and functional genomics form a model of phenotypic change that can be tested by direct manipulations of the genome (Lower) (69), bringing us closer to understanding the evolutionary course of morphological transformations.
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