Key Points
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Evolutionary developmental biology faces reciprocal paradoxes: the conservation of similar developmental genetic toolkits despite a diversity of life forms, and the inverse paradox — the development of similar morphologies despite the phylogenetically variable presence of the genetic tools that are thought to be responsible for those forms.
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Phylogenomic analysis, when carried out with care for possible pitfalls, can indicate the orientation of trait gain and loss among diverging lineages.
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Comparative genomic analysis correlated to the loss of an ancestral trait can identify candidate genes that are responsible for the development of that trait.
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Genome contractions in various lineages have diminished genetic toolkits for DNA methylation and for retinoic acid signalling, providing examples of the inverse paradox. It is thought that changes in genome architecture might have disrupted regulatory mechanisms that depend on chromosome territories or long-range enhancers, which would have decreased the importance of genome methylation and patterning by distantly diffusible signals in some animals with determinative development and rapid life cycles.
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Genome expansion, for example, by whole-genome duplication events, can result in the complementary degeneration of gene subfunctions leading to the reduction of pleiotropy and subsequent evolution of toolkit components that are specialized for precise developmental functions, as illustrated by fibroblast growth factor (Fgf) family genes.
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Genome architecture can, in some cases, be related to conserved non-coding elements that act as enhancers located far from the genes they encode; fitness penalties for disrupting these relationships can explain certain human developmental diseases and syntenies that have been conserved over evolutionary time.
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These examples show that genomics bridges the gap between evolutionary biology and developmental biology.
Abstract
Reciprocal questions often frame studies of the evolution of developmental mechanisms. How can species share similar developmental genetic toolkits but still generate diverse life forms? Conversely, how can similar forms develop from different toolkits? Genomics bridges the gap between evolutionary and developmental biology, and can help answer these evo–devo questions in several ways. First, it informs us about historical relationships, thus orienting the direction of evolutionary diversification. Second, genomics lists all toolkit components, thereby revealing contraction and expansion of the genome and suggesting mechanisms for evolution of both developmental functions and genome architecture. Finally, comparative genomics helps us to identify conserved non-coding elements and their relationship to genome architecture and development.
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Acknowledgements
We thank for support R01 RR020833, and P01 HD22486 from the National Institutes of Health, and IOB-0719577, from the US National Science Foundation.
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Glossary
- Developmental genetic toolkit
-
A set of genes that is required for development and is shared widely among species.
- Phylogenomics
-
Phylogenetic inference on a genome-wide scale.
- Ecdysozoan
-
A group of protostomes that unites the phyla Arthropoda (including flies) and Nematoda (including roundworms), among others.
- Cladogenesis
-
The process in which lineages of organisms diverge into separate clades — groups of organisms, all of which are descended from a single common ancestor.
- Homoplastic character
-
Characters that are similar owing to convergent evolution rather than derivation from a single character in the last common ancestor.
- Deuterostomes
-
'Deutero' (second), 'stome' (mouth). Bilaterian animals in which the first opening of the embryo forms the anus, whereas a second opening forms the mouth, in contrast to protostomes — bilaterians in which the first embryonic opening forms the mouth. Deuterostomes include chordates, echinoderms and hemichordates.
- Ambulacraria
-
A taxon containing the phyla Echinodermata (including sea stars and sea urchins) and Hemichordata (including acorn worms).
- Chordates
-
Our own phylum, which includes three subphyla: Vertebrata (including fish, amphibia, reptiles, birds and mammals), Cephalochordates (like amphioxus) and Urochordates (like ascidians and larvaceans).
- Urochordates
-
The subphylum of chordates that is the sister group to the vertebrates, including ascidians (or sea squirts), a class forming a tadpole larva with a chordate body plan that is destroyed by a radical metamorphosis to form a sessile adult, and larvaceans, a class of mostly planktonic animals that maintains a chordate body plan throughout its life cycle. Also called tunicates.
- Olfactores
-
A chordate taxon including the two subphyla Vertebrata and Urochordata.
- DNA methylation
-
A DNA modification in which a methyl group is added to cytosine. Methylation inhibits gene expression and is maintained through DNA replication and cell division.
- Epigenetic
-
Factors that affect gene action without changing nucleotide sequence. Epigenetic modifications act by changing the structure of chromatin, and are facilitated by DNA methylation and histone modification.
- Bilaterians
-
A taxon of animals with a bilaterally symmetrical body plan, in contrast to the basally diverging radiata, which have a radial body plan. Includes cnidarians such as sea anemones and jellyfish.
- Synteny
-
(Same thread). A set of genes on the same chromosome (clearly, two genes in a fish and the orthologues of those two genes in a human are not on the same chromosome and so can't be syntenic).
- Conserved synteny
-
A situation in which a set of syntenic genes in one species has orthologues that are syntenic in another species.
- Determinative development
-
A developmental mode in which cell fate becomes fixed very early in embryonic development.
- Hox clusters
-
A group of tandemly duplicated genes encoding homeodomain-containing transcription factors that control the development of animal body axes.
- Collinearity
-
In Hox clusters, genes located 3′ in the cluster are expressed earlier (temporal collinearity) and more anteriorly (spatial collinearity) than genes that lie more 5′ in the cluster.
- Phylotypic body plan
-
The body organization shared by all members of a phylum.
- Paralogues
-
Genes within the same species that arose by gene duplication within the lineage. For example, Hoxa1 and Hoxb1 in mice, or hoxb1a and hoxb1b in zebrafish.
- Non-functionalization
-
The process whereby a pair of duplicated genes reverts to a single copy as one suffers mutations that produce a non-functional protein.
- Neofunctionalization
-
The process whereby a pair of duplicated genes becomes permanently preserved as one copy acquires mutations conferring a new function that becomes fixed in a population by positive Darwinian selection.
- DDC model
-
(Duplication–degeneration–complementation). A model to explain the evolution of duplicated genes including the complementary loss of subfunctions by degenerative mutations.
- Subfunctionalization
-
The process whereby a pair of duplicated genes becomes permanently preserved because the two gene copies have reciprocally lost essential subfunctions by complementary degenerative mutations.
- Subfunction
-
A specific subset of a gene's regulatory or structural function that, when mutated, establishes a distinct complementation group.
- Subfunction partitioning
-
The distribution of gene subfunctions to one or another gene duplicate subsequent to the preservation of both paralogues by subfunctionalization.
- Pleiotropy
-
A genetic phenomenon in which a single gene affects many traits.
- Population-isolating mechanisms
-
Traits that prevent populations of organisms from interbreeding to produce viable, fertile offspring.
- Eumetazoans
-
All animals (metazoa) except sponges.
- Orthologues
-
Genes in different species that derive from the same gene in the last common ancestor of those species, for example, Hoxb1 in mice, HOXB1 in humans and hoxb1a in zebrafish.
- Conserved non-coding element
-
A DNA sequence that is maintained over evolutionary time but whose information does not ultimately appear in the sequence of a protein.
- Ligule
-
A thin sheet on a grass leaf between the sheath and the stem.
- Co-orthologues
-
A pair of gene duplicates, both of which are orthologues of a single gene in a different species.
- Position-effect human diseases
-
Diseases associated with chromosome rearrangements that change a gene's position, but do not change the genes sequence.
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Cañestro, C., Yokoi, H. & Postlethwait, J. Evolutionary developmental biology and genomics. Nat Rev Genet 8, 932–942 (2007). https://doi.org/10.1038/nrg2226
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DOI: https://doi.org/10.1038/nrg2226
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