A polychaete worm - an adult Pomatoceros lamarckii removed from its habitation tube.
Genomes of Ancient Animal Ancestors
Pulling Evo-Devo out of the 'Box
by Dr David Ferrier
The genes present in every organism form the basic instruction set from which each individual grows, develops, and then functions in everyday life.
Together all of the genes of an organism make up its genome, and it is this genetic material that is passed from generation to generation and it is in this material that changes accumulate during evolution. Understanding genomes and how they are organised can help our understanding of how organisms function, and how they came to be as they are.
With increasingly powerful (and cheaper) techniques of sequencing DNA, complete genome sequences are becoming available for more and more animals, and this allows scientists to carry out detailed comparisons of their genes and genomes.
Focusing on similarities in genomes in these comparisons allows researchers to determine which features were present in the last common ancestor of the organisms being studied. In addition, discovering differences in genomes can provide clues to the genes and genomic features that were involved in the origins and diversification of particular species.
An ancestor is the extinct organism from which subsequent lineages arose and diverged. The main groups of animals, such as sponges, jellyfish and sea anemones, insects and crabs, earthworms and leeches, fish and humans, are called phyla (Porifera, Cnidaria, Arthropoda, Annelida and Chordata in these examples), and the ancestor that gave rise to these animal phyla lived at least 545 million years ago, before the famous Cambrian explosion.
Despite such long periods of evolutionary time, and despite the radically different appearances of such animals, many similarities between their genomes can be found. By extension the content and organisation of the genomes of these long dead, extinct ancestors can be reconstructed - on a computer, at least!.
One particularly fruitful route in to comparing genome content and organization, as well as the developmental mechanisms that build animals, has been by examining a group of genes that contain a similar sequence motif called a 'homeobox'...
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Pulling Evo-Devo out of the 'Box
A basic animal phylogeny illustrating the relationships between a small selection of phyla.
Animal relationships (phylogeny).
The relationships between animal phyla can be represented by a ‘tree’ arrangement, with more closely related phyla having branches that join together closer to the tips of the tree than more distantly related phyla. For example, humans and fish, in the phylum Chordata, are more closely related to each other than to an earthworm, in the phylum Annelida. Also, the Chordata and Annelida are more closely related to each other than to the phylum Cnidaria (jellyfish and sea anemones).
Ancestral states can be viewed as existing at the points (nodes) where two branches join together. In recent years our understanding of the animal phylogeny has been revolutionised by analyses of gene sequence data. The analyses and debates are still on-going, but whilst some areas of the phylogeny are still contentious the basic formation is now widely accepted.
Homeobox and Hox: the rejuvenation of evo-devo by molecular biology
In the 1980’s the, then relatively new, techniques of molecular biology were used to determine the sequence of some genes that are important in building the body of the fruit fly (Drosophila melanogaster - a popular species for studying how animals develop). These particular developmental control genes were known to be grouped together in the genome and to control where certain structures developed along the fly’s body, so that legs, wings and mouthparts developed properly and in the correct place. Once the gene sequences of these so-called Homeotic genes were determined, they were all found to contain a similar motif, the homeobox. With this sequence in hand the same genes were quickly found in lots of other animals, including humans, and they have since been found to be working in broadly similar fashions in nearly all animals examined.
Mutations of Hox genes have comparable effects in both mice and flies - transformation of vertebrae identities giving extra ribs and transformation of thoracic segment identities giving extra wings.
[credits: see Authors/Credits ]
The Homeobox allowed relatively rapid comparison of the developmental mechanisms across a wide range of animals at the molecular level. Deep levels of similarity (conservation) across much of the animal kingdom were revealed, which surprised and shocked many, and led to a rejuvenation of the field of Evolutionary Developmental Biology (or Evo-Devo).
Homeoboxes are not just Hox
There is more to homeobox genes than Hox genes. The Hox genes, which are related to the clustered developmental control genes in the fruit fly that determine where structures develop during embryogenesis, are only a small subset of the genes in any particular animal’s genome that contain the homeobox motif. The homeobox gene family is large, with over 200 members in humans, of which only 39 are Hox genes. Like the Hox genes these other homeobox genes also control developmental processes. Also like the Hox genes, many of these other homeobox genes are grouped together in animal genomes. This clustering in the genome may well have implications for how the genes function as well as evolve.
Just as there is more to homeobox genes than Hox, there is more to developmental biology than the homeobox. With the rapid, molecularly inspired, progress of developmental biology many other types of gene have been found to control development. With the rejuvenation of Evo-Devo the conserved and divergent aspects of these genes, and the processes in which they are embedded, are being revealed. Evolutionary similarities as well as the molecular differences and mechanisms that underpin the evolution of biodiversity can begin to be understood.
Animal diversity and homeobox gene diversity:
- Polychaete
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Polychaete
Pomatoceros lamarckii
- Sea anemone
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Sea anemone
Actinia equina
- Amphioxus
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Amphioxus
Branchiostoma lanceolatum
- Red flour beetle
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Red flour beetle
Tribolium castaneum
- Phylogenetic tree
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Phylogenetic tree
...of all homeobox genes from amphioxus (Branchiostoma floridae).
Taken from Takatori et al (2008) Dev Genes Evol 218:579-590.
Gene neighbourhoods and linkage (synteny)
In many animals, including mammals like ourselves, the Hox genes have a particular organisation in the genome, existing as clusters (Hox clusters). These Hox clusters are arranged such that the genes at one end pattern the development of the head-end of the embryo, the genes in the middle of the cluster pattern the middle of the embryo, and genes at the other end pattern the tail-end. This organisation seems to be entwined with how the genes are regulated. Such mechanistic links may well be present in other gene clusters; both homeobox gene clusters (e.g. ParaHox, NK, Irx/Iroquois) and non-homeobox gene clusters (e.g. Runt, Wnt, Sp).
As well as providing mechanistic insights, the organisation of the genes in the genome can be compared across genomes to reveal widely conserved gene neighbourhoods (synteny) that have been inherited from ancient ancestors. These conserved syntenies can be found both at the level of the immediate neighbourhood of a gene or gene cluster, and at the level of conserved linkage onto the same chromosome. In this way some local neighbourhoods (micro-synteny) as well as whole chromosome linkages (macro-synteny) have been determined for such ancient ancestors as the last common ancestor (LCA) of chordates, the LCA of bilaterally symmetrical animals (bilaterians - that constitute well over 90% of animal species), as well as the LCA of all animals (the Urmetazoan).